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Tomato molecular biology – special collection of papers for molecular horticulture

  • Graham B. Seymour 1 &
  • Jocelyn K. C. Rose 2  

Molecular Horticulture volume  2 , Article number:  21 ( 2022 ) Cite this article

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Tomato ( Solanum lycopersicum ) is the second most important vegetable crop globally, after potato, with about 100 million tons fresh fruit being grown on 3.7 million hectares (FAO 2021 ), and is of great importance in the human diet due to the large amount of fruit consumed. The fruit are eaten both fresh and, equally importantly, as a processed product in puree, soups and canned products. They provide an important dietary source of vitamins and minerals, such as K, Fe and Ca, and are known for the large number of health promoting secondary metabolites, including the carotenoid and flavonoid pigments that give the fruit a spectrum of yellow, red and orange colours.

Tomato commercial production and breeding is supported by a long history of research that has led to the identification of regions of the tomato genome that control a host of important traits including disease resistance, yield and fruit quality. The first tomato genome was sequenced a decade ago and the sequence is now in its fifth iteration with 100 s of genome sequences from a wide spectrum of wild species crop relatives and cultivated varieties. The diploid nature of tomato, genomic resources and a wide range of single gene mutants make it an excellent model plant to study dicot crop species and especially those with fleshy fruits.

In this special collection, we bring together a range of papers to explore the latest developments and scientific insights in tomato molecular biology. This brief editorial summarises the key features of the papers that collectively set the scientific discovery in the context of plant development and highlight relevance to horticulture.

Plant architecture is a critical determinant of crop productivity and influences, among other factors, the number of reproductive shoots. The hormonal control of plant architecture has been the subject of studies for well over 100 years, but recent advances in genomics have accelerated our understanding of its molecular basis. Tomato is an especially useful model to investigate the association between plant architectural features and their impact on crop performance. Side branching in tomato is undesirable and results in unwanted labour and management costs. Three main phytohormone classes are known to influence side branching: auxins, cytokinins (CKs) and strigolactones. Auxin inhibits the outgrowth of axillary buds and maintains apical dominance. CKs act antagonistically to auxin, suppressing apical dominance and allowing release of axillary buds from dormancy. Auxin modulates CK concentration by repressing its levels, while strigolactones affect bud inhibition by modulating auxin transport. In addition, there seems to be some interplay between CK and strigolactone levels, and the overall picture highly complex. In this special issue, Pino et al. ( 2022 ) report that tomato plants overexpressing the cytokinin-deactivating gene CYTOKININ OXIDASE 2 ( CKX2 ) showed excessive growth of axillary shoots, which is opposite to the phenotype expected of plants with reduced CK content. The authors suggest that CKs cause their paradoxical effects on branching by disturbing auxin status, and by altering the expression of genes associated with branching and CK homeostasis. The study highlights the intricacy of the molecular control of side branching, and the importance of this research in understanding the control of plant architecture for crop improvement.

The architecture of plant roots is as important as that of above ground organs and this is an area of particular interest to growers of grafted vegetable crops. Many Solanaceous crops, including tomato, pepper and eggplant, are grown as elite scion genotypes grafted onto to superior performing rootstocks, and this is especially widespread for commercial tomato production in Europe and the USA. The root stocks can be chosen to enhance scion resistance to diseases and abiotic stress, involving conditions such as low nutrient availability and high salinity. The genetic basis of root traits in tomato and other crops is relatively poorly understood and this knowledge is an important prerequisite for a rational approach to breeding for improved root traits. In this issue, Kevei et al. ( 2022 ) report their work on a tomato mutant, bushy root-2 ( brt-2 ), which has a twisting tap root and a high density of lateral roots, giving a bushy appearance. These lateral roots are also abnormal in that they twist and curl, and plant growth is slower than that of wild type. The brt-2 candidate gene was identified by genetic mapping as a class B heat shock factor protein encoded by SolycHsfB4a. Whole genome resequencing and SNP (single nucleotide polymorphism) and KASP (Kompetitive allele specific PCR) markers were used to fine map the brt-2 gene and a SNP was identified as a strong candidate for the causal brt- 2 mutation. The authors discuss reasons why such a mutation could influence the function of the protein encoded by the gene at the brt-2 locus and how this might result in the bushy root phenotype. The study provides an important extension to our knowledge of root architecture in tomato. Moreover, since a related Arabidopsis thaliana gene, ATHSFB4 , is induced by root knot nematode (RKN) infection, and its loss-of-function mutants are resistant to RKNs, BRT-2 could be a target gene for RKN resistance, an important trait in tomato rootstock breeding.

Studies have shown that the action of auxin, CKs, and gibberellins (GAs) can reduce plant resistance to water deficiency, and there is evidence that inhibition of GA activity can enhance plant performance under stress conditions. In this collection, Shohat et al. ( 2021 ) review the importance of GAs in tomato, including in regulating responses to abiotic stresses, such as drought. They authors consider how drought affects GA biosynthesis and signalling in tomato and discuss possible ways in which knowledge of GA pathways could be used to generate drought tolerant plants. These include interrupting GA binding to its receptor, GID1, altering the effectiveness of the downstream signalling pathway and, perhaps most promisingly, through deactivation of GA itself.

Irregular watering and other factors can result in devastating losses in commercial tomato operations due to a physiological disorder known as blossom-end rot (BER). Typical symptoms of BER appear as small, light-coloured, water-soaked spots on the blossom end of the fruit, which is associated with cell plasmolysis and leaky membranes. After BER induction, BER-affected areas often expand in the form of brown necrotic regions covering a significant proportion of the fruit and, in some extreme cases, can affect the entire fruit. The condition affects tomato, but also many other fruits, including pepper ( Capsicum annuum L.), watermelon ( Citrullus lanatus (Thunb.) and eggplant ( Solanum melongena L.). In this special collection, Topcu et al. ( 2022 ) review the latest information of the biological basis of BER as well as the genetic and molecular underpinnings of this important physiological disorder. The paper presents information on the role of altered Ca 2+ homeostasis among different cellular compartments, and especially the role of Ca 2+ and interactions with pectin in the fruit primary cell walls. Other important factors include reactive oxygen species (ROS), which appear to be a critical component of BER development and are linked to changes in Ca 2+ deficiency. Tomato varieties show variation in their susceptibility to BER, which suggests a possible underlying genetic basis for the condition. Genetic mapping and differential expression analysis has uncovered possible candidate BER-associated genes, but further work is needed to develop genetic approaches to prevent this physiological disorder.

Tomato fruit are the most widely used model to investigate the developmental regulation of ripening in fleshy fruited species, and there is a deep set of resources to help dissect the biochemical, molecular, and genetic events linked to tomato fruit ripening control. In this special collection, Zhu et al. ( 2021 ) review the metabolic changes that effect fruit quality during tomato ripening. The review focuses on the transcriptional and post-translational control of the networks that affect the accumulation of important biochemical components in fruit tissues, from pigments and sugars through to other metabolites with health promoting properties. The review links the biochemistry of the ripening process with the key genes underlying these processes and the associated quality traits.

One of the key processes determining fruit quality is the rate of softening and tomato again represents one of the model organisms where this process has been researched in some considerable depth. The review in this collection by Wang and Seymour ( 2022 ) summarises the most recent data available on the control of softening in tomato. The authors first describe the hormonal cues, epigenetic priming and transcriptional control linked with the softening process. These areas of research are still fragmented and there is a limited understanding of the interrelationship between such high-level events. However, the actual biochemical changes involved in texture changes are a little clearer, although the specific timing and role of particular biochemical events still generally remain obscure. In essence, it seems that modification of pectic polysaccharides plays a major role in softening through the action of enzymes such as pectate lyase (PL), polygalacturonase (PG) and several other activities. Gene editing of tomato to silence these genes leads to an inhibition of softening in the case of PL, although it is not the only factor involved in textural changes and studies of the transcriptional control of softening are providing new insights. Understanding the molecular basis of softening is providing targets for molecular breeding that will likely improve shelf life, and possibly fruit that are more resilient to fungal and bacterial spoilage.

A primary barrier to pathogen invasion and spoilage is the fruit cuticle. In this issue Bres et al. ( 2022 ) describe how they screened a mutant collection of the miniature tomato cultivar Micro-Tom for fruit cracking mutants and found a mutant with a glossy fruit phenotype. The authors then used a mapping-by-sequencing strategy to identify the causal mutation as an amino acid change in the SlSHN2 transcription factor, which is specifically expressed in outer epidermis of growing fruit. The mutation has a marked effect on cuticle composition. In addition to the direct effects on cuticle formation and composition, the mutation resulted in a wide range of other gene expression changes that link the SlSHN2 gene to coordination of cuticle deposition, epidermal patterning and defence against biotic and abiotic stresses.

New insights into the molecular control of plant growth and fruit ripening will likely come with a better understanding of the role of genome structural variation and epigenetics in controlling gene expression. The paper in this special collection by Jobson and Roberts ( 2022 ) reviews the current understanding of genomic structural variation (SV) in tomato and its role in plant immunity. Structural variation for the purpose of this review is defined as changes that range from greater than 30 base pairs to several megabases. These can include inversions, duplications and deletions. The authors discuss the various molecular mechanisms leading to common structural changes. Drawing on information from several species, including tomato, they then discuss identification of SVs in plant genomes. The main part of the review focuses on the potential roles of SV in responses to biotic and abiotic stress. The authors conclude with a section on engineering immunity in tomato using SVs.

Other articles published in Molecular Horticulture, outside this current collection that may also be of interest to readers include those on tomato fruit size control by a zinc finger protein regulating pericarp cell size (Zhao et al. 2021 ), tomato SlRUP as a negative regulator of UV-B photomorphogenesis (Zhang et al. 2021 ) and genome-wide binding analysis of the tomato transcription factor SlDof1 and its regulatory impacts on fruit ripening (Wang et al. 2021 ).

The papers in this special collection highlight a broad range of exciting discoveries, technology platforms and resources that illustrate the tremendous and growing significance of tomato as an experimental model, and socially important crop. The future for tomato research remains bright!

Bres C, Petit J, Reynoud N, et al. The SlSHN2 transcription factor contributes to cuticle formation and epidermal patterning in tomato fruit. Mol Hortic. 2022;2:14. https://doi.org/10.1186/s43897-022-00035-y .

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Kevei Z, Ferreira SDS, Casenave CMP, et al. Missense mutation of a class B heat shock factor is responsible for the tomato bushy root-2 phenotype. Mol Hortic. 2022;2:4. https://doi.org/10.1186/s43897-022-00025-0 .

Pino LE, Lima JE, Vicente MH, et al. Increased branching independent of strigolactone in cytokinin oxidase 2-overexpressing tomato is mediated by reduced auxin transport. Mol Hortic. 2022;2:12. https://doi.org/10.1186/s43897-022-00032-1 .

Shohat H, Eliaz NI, Weiss D. Gibberellin in tomato: metabolism, signaling and role in drought responses. Mol Hortic. 2021;1:15. https://doi.org/10.1186/s43897-021-00019-4 .

Topcu Y, Nambeesan SU, van der Knaap E. Blossom-end rot: a century-old problem in tomato (Solanum lycopersicum L.) and other vegetables. Mol Hortic. 2022;2:1. https://doi.org/10.1186/s43897-021-00022-9 .

Wang D, Seymour GB. Molecular and biochemical basis of softening in tomato. Mol Hortic. 2022;2:5. https://doi.org/10.1186/s43897-022-00026-z .

Wang Y, Wang P, Wang W, et al. Genome-wide binding analysis of the tomato transcription factor SlDof1 reveals its regulatory impacts on fruit ripening. Mol Hortic. 2021;1:9. https://doi.org/10.1186/s43897-021-00011-y .

Zhang C, Zhang Q, Guo H, et al. Tomato SlRUP is a negative regulator of UV-B photomorphogenesis. Mol Hortic. 2021;1:8. https://doi.org/10.1186/s43897-021-00010-z .

Zhao F, Zhang J, Weng L, et al. Fruit size control by a zinc finger protein regulating pericarp cell size in tomato. Mol Hortic. 2021;1:6. https://doi.org/10.1186/s43897-021-00009-6 .

Zhu F, Wen W, Cheng Y, et al. The metabolic changes that effect fruit quality during tomato fruit ripening. Mol Hortic. 2021;2:2. https://doi.org/10.1186/s43897-022-00024-1 .

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Seymour, G.B., Rose, J.K.C. Tomato molecular biology – special collection of papers for molecular horticulture. Mol Horticulture 2 , 21 (2022). https://doi.org/10.1186/s43897-022-00042-z

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  • Saudi J Biol Sci
  • v.20(4); 2013 Oct

Improved growth, productivity and quality of tomato ( Solanum lycopersicum L.) plants through application of shikimic acid

A field experiment was conducted to investigate the effect of seed presoaking of shikimic acid (30, 60 and 120 ppm) on growth parameters, fruit productivity and quality, transpiration rate, photosynthetic pigments and some mineral nutrition contents of tomato plants. Shikimic acid at all concentrations significantly increased fresh and dry weights, fruit number, average fresh and dry fruit yield, vitamin C, lycopene, carotenoid contents, total acidity and fruit total soluble sugars of tomato plants when compared to control plants. Seed pretreatment with shikimic acid at various doses induces a significant increase in total leaf conductivity, transpiration rate and photosynthetic pigments (Chl. a, chl. b and carotenoids) of tomato plants. Furthermore, shikimic acid at various doses applied significantly increased the concentration of nitrogen, phosphorus and potassium in tomato leaves as compared to control non-treated tomato plants. Among all doses of shikimic acid treatment, it was found that 60 ppm treatment caused a marked increase in growth, fruit productivity and quality and most studied parameters of tomato plants when compared to other treatments. On the other hand, no significant differences were observed in total photosynthetic pigments, concentrations of nitrogen and potassium in leaves of tomato plants treated with 30 ppm of shikimic acid and control plants. According to these results, it could be suggested that shikimic acid used for seed soaking could be used for increasing growth, fruit productivity and quality of tomato plants growing under field conditions.

1. Introduction

Tomato ( Solanum lycopersicum L.) is one of the most popular and widely consumed vegetable crops all over the world, and high-quality yield is an essential prerequisite for its economical success in the Saudi Arabia. Tomato has been recently gaining attention in relation to the prevention of some human diseases. This interest is due to the presence of carotenoids and particularly lycopene, which is an unsaturated alkylic compound, that appears to be an active compound in the prevention of cancer, cardiovascular risk and in slowing down cellular aging ( Gerster, 1997; Di Cesare et al., 2012; Abdel-Monaim, 2012 ). Lycopene is found in fresh, red-ripe tomatoes as all-trans (79–91%) and cis- (9–21%) isomers ( Shi et al., 1999; Boileau et al., 2002; Abdel-Fattah and Al-Amri, 2012 ).

Soils in the arid and semiarid regions like Saudi Arabia have little nutrient and mineral contents, which adversely affect plant growth and quality. One of the cost-effective strategies for counteracting deficiencies of soil minerals involves the application of chemical fertilizers. Increasing growth and quality of tomato plants through increasing the productivity per unit area as well as with expanding the cultivated area in newly reclaimed lands is the major important national target by application of cheap efficient strategies. Shikimic acid is the known precursor of aromatic amino acids, l -phenylalanine and l -tyrosine. These compounds are phenylpropane (C 6 –C 3 ) derivatives as are the building units of lignin ( Aldesuquy and Ibrahim, 2000 ). Phenylalanine is an excellent precursor in all plants but tyrosine in only really effective in the grasses ( Stafford, 1974 ). The shikimic pathway, a collection of seven enzymatic reactions whose end product is chorismate, has been studied for many years in a variety of microorganisms and plants. In plants, chorismate is the precursor not only for the synthesis of aromatic amino acids (i.e. phenylalanine, tyrosine and tryptophan), but also for many secondary metabolites with diverse physiological roles ( Weaver and Herrmann, 1997 ). Shikimic acid is used in several plants without side effects and also used in a large scale for growth enhancement and improving fruit quality of crop and vegetable plants for many years ( Aldesuquy and Ibrahim, 2000; Elwan and El-Hamahmy, 2009 ).

In most plants, sucrose is the major product of photosynthesis and the major form of carbohydrate transported to non-photosynthetic organs ( Favati et al., 2009 ). It can be involved in numerous metabolic pathways. Elwan and El-Hamahmy (2009) concluded that the quality of fruit pepper was positively correlated with the high amount of total soluble sugars. The shikimic acid pathway participates in the biosynthesis of plant phenolics ( Logemann et al., 1995 ), where the most abundant classes of phenolic compounds in plants are derived from phenylalanine via elimination of an ammonia molecule to from cinnamic acid ( Hahlbrock and Scheel, 1989 ). Phenolic compounds play an important role in the regulation of plant growth and metabolism and they are no longer considered to be a passive by-product. In some cases, phenolic treatment induces expression of the same genes and resistance against the same spectrum of pathogens as pathogen induced resistance ( Lawton et al., 1996 ).

In the light of the above limited reviews, the present work aimed to evaluate the influence of seed presoaking with shikimic acid on growth parameters, fruit quality, transpiration rate, total leaf conductivity, photosynthetic pigments, mineral contents and productivity of tomato plants growing in field conditions.

2. Materials and methods

2.1. plant and growth conditions.

Seeds of tomato ( Solanum lycopersicum Mill.) were surface sterilized in 7% sodium hypochlorite for 10 min, subsequently washed thoroughly with distilled water. The sterilized seeds were divided into four sets. Seeds of the 1st set were soaked in distilled water to serve as control, the other three sets (2nd, 3rd and 4th) were soaked in shikimic acid at 30, 60 and 120 ppm, respectively for about four hours, then washed with distilled water. All these treated seeds were left to germinate for 5 days on a moistened filter paper in dark at 25 °C. Uniform germinated seedlings were sown in a 8 × 8 × 9 cm 3 plastic plate containing moist-autoclaved vermiculite soil and left to grow in a greenhouse under controlled conditions. Three weeks later, plants were transplanted into plots (25 × 25 cm 2 ) in a randomized complete block design, three plots for each treatment and each plot had ten plants having inter row and inter plant spacing that were 70 and 40 cm, respectively, at the research experimental farm of the Facility of Science, King Saud University, Riyadh, Egypt in March 2012. The physical and chemical analyses of the soil used in this study are listed in Table 1 . Soil characteristics were pH 7.58, electrical conductivity 1.51 ds cm −1 , total organic matter 0.74%, total nitrogen 70.0 mg kg −1 , total phosphorus 15.3 mg kg −1 , potassium 132 mg kg −1 , magnesium 114 mg kg −1 and calcium 560 mg kg −1 . All plants were watered as needed with tap water to maintain soil moisture near field capacity (75–80%) and fed once weekly with 35 g N m −2 as potassium nitrate and 35 g P m −2 as superphosphate as a nutritive solution. Harvesting (ten plants per each treatment) was carried out 12 weeks after transplant.

Physical and chemical analyses of soil used throughout this study.

2.2. Measurements

2.2.1. growth and fruit yield parameters.

At harvest, shoot height and leaf number per plant were recorded. Fresh and dry (70 °C for 48 h) weights of shoots and roots were determined. Leaf area was measured using a leaf area meter (Li-Cor, Lincoln, NE, USA). Fruit number for each treatment was also recorded. Fruit thickness was measured by a caliper. Average weight of fruit’s fresh and dry masses in each treatment was recorded.

2.2.2. Estimation of fruit quality

Total acidity in fruits for each treatment was determined in the supernatant obtained by extracting 10 g of fruit with distilled water according to the method of Wills and Ku (2002) using citric acid as a reference. Total soluble sugars in fruit extracts were determined with antheron reagent spectrophotometrically at 620 nm according to Stewart (1974) . Fruit carotenoids were extracted from the fruit pericarp by acetone (85%) and determined spectrophotometrically according to Lichtenthaler and Weliburn (1983) . Vitamin C in the fruit extract was estimated according to Pearson (1970) . Lycopene content in the fruit extracts was assessed by RP-HPLC (Allteck, Milano, Italy), the pigment was separated using a C 18 luna column equipped with a luna C 18 guard column, utilizing a solution of MeOH/THF as mobile phase. The flow rate was set at 2 ml/min and the elution of the compounds was obtained at isocratic conditions. Detection was performed at 450 nm and the peaks were tentatively identified by comparing their retention times to those of the lycopene standard (Sigma, USA).

2.2.3. Estimation of photosynthetic pigments

Photosynthetic pigments (chlorophyll a, chlorophyll b and carotenoids) in leaves were assayed according to Hiscox and Israelstam (1979) . The extraction was made from 100 mg of fresh sample in acetone (80%) in the dark at the room temperature and was measured with a UV/VIS spectrophotometer (Shimadzu UV-160, Kyoto, Japan).

2.2.4. Nutrient analysis

Oven-dried leaf plant tissues were grounded and sieved through a 0.5 mm sieve. A known weight of the grounded material was digested in a digestion flask containing a triple acid mixture (HNO 3 :H 2 SO 4 :60% HCl 4 , with a ratio of 10:1:4; respectively) for analysis of phosphorus and potassium. Phosphorus (P) was extracted by nitric–perchloric acid digestion and measured using the Vanadomolybdophosphoric acid colorimetric method ( Jackson, 1973 ). Potassium (K) was assayed using a flame spectrophotometer (Corning 400, UK). Total nitrogen (N) was determined by the Kjeldahl method ( Nelson and Sommers, 1973 ).

2.2.5. Measurements of total leaf conductance and transpiration rate

Total leaf conductance and transpiration rate of the tomato leaves were measured using Li-Cor, 6400XT, Lincoln, NE, USA.

2.3. Statistical analysis

A randomized block design with ten replicates was adopted. The data were statistically analyzed using one-way analysis of variance, and the means were separated by Duncan’s multiple range test by the least significant difference (LSD, P  ⩽ 0.05) method using Costat software (Cohort, Berkeley, CA).

3. Results and discussion

3.1. plant growth.

As compared to control plants, seeds presoaked with various concentrations of shikimic acid significantly increased shoot height, number of leaves, leaf number, fresh and dry weight of tomato plants ( Table 2 ). The magnitude of increase appears to depend mainly on the concentration used, whereas with the concentration increase there is a simultaneous increase up to the limit in the above growth parameters. 60 ppm of shikimic acid was most efficient in its ability to increase plant growth in comparison with other treatments. Shikimic acid being a precursor of phenolic compounds has been shown to be of great importance in the regulation of growth and they are no longer considered to be passive by-products ( Jain and Srivastava, 1981 ). The improvement in growth parameters of tomato plants in response to shikimic acid application might be mediated through the increased longevity of leaves by retaining chlorophylls and increasing mineral contents which perhaps contributed to increased plant growth ( Neera and Garg, 1989; Gupta, 1990 ). In addition, the results obtained here are in agreement with the results of Aldesuquy and Ibrahim (2000) who stated that seed priming with shikimic acid increased growth and yield of cowpea plants grown under greenhouse conditions through increasing the total soluble sugars protein content and photosynthetic activity.

Effect of seed presoaking in shikimic acid on growth responses and leaf area of tomato plants.

The increase in the leaf area of tomato plants in response to shikimic acid application could have resulted from the rapid rate of movement of nutrients and hormones transported through transpiration stream from the root, which can accelerate the rate of leaf expansion in the developing leaves ( Aldesuquy and Ibrahim, 2000 ). In connection with these results, it was reported that a low concentration of salicylic acid increases the growth of maize seedlings, with the higher concentration inhibiting it ( Jain and Srivastava, 1981 ). Furthermore, Abo-hamed et al. (1987) reported that the soil drenched with salicylate led to an increase in the fresh and dry weight of shoot and at lower concentration appeared to enhance plant height and leaf area of wheat plant.

3.2. Fruit yield and quality

It is clear from Table 3 that the application of shikimic acid at various concentrations greatly affected the flower yield and quality of tomato plants. Thus seed presoaking with shikimic acid at all doses increased significantly fruit number, average fruit weight and fruit thickness of tomato plants compared with control plants. Our findings are supported by the results of Aldesuquy and Ibrahim (2000) who stated that shikimic acid induced an increase in growth and yield of cowpea plants. The beneficial effects of shikimic acid on fruit yield may have been due to the translocation of more photoassimilation to fruits, thereby increasing fruit weight ( Gunes et al., 2007; Elwan and El-Hamahmy, 2009; Favati et al., 2009 ). In the same direction, the significant highest value of total acidity in fruit juice was increased by 66.4% with the treatment of 60 ppm of shikimic acid over the control treatment.

Effect of seed presoaking in shikimic acid on fruit yield and quality of tomato plants.

The data in Table 3 showed that high vitamin C and carotenoids were significantly increased in fruits of tomato plants treated with shikimic acid, particularly 60 ppm, compared with non-treated control plants. Since ascorbic acid (vitamin C) plays an important role as an antioxidant and protects the plant during oxidative damage by scavenging free radicals and ROS that are generated by various stresses ( Schulthesis et al., 2002; Elwan and El-Hamahmy, 2009 ). Higher content of ascorbic acid might maintains relatively lower levels of ROS in pepper and tomato fruit resulting in less damage caused by ROS after stress. In addition, regarding the protection role of ascorbic acid against oxidative damage, several epidemiological and experimental studies have shown that the consumption of foods rich in vitamin C is associated with a decreased risk of several chronic diseases, including cardiovascular disease and cancer ( Jacob and Sotoudeh, 2002 ).

In general, seed priming of tomato plants with shikimic acid significantly increased total soluble sugar content in fruits compared with control treatment ( Table 3 ). These results are in agreement with the results of Ethness and Roitsch (1997) who demonstrated that carbohydrate metabolism in tomato plants is regulated by different plant hormones. Furthermore, shikimic acid is a precursor of many phenolic compounds and these substances are known to provide protection to auxins against oxidation ( Schneider and Whitman, 1974 ). The increased levels of auxins may result in an increase in invertase enzymes as it has been demonstrated by Glaszou et al. (1966) . This fact could explain the observed increase in total soluble sugar content in developing seeds.

Lycopene, which is responsible for the red color of tomatoes, is greatly affected by the application of shikimic acid. It has been shown that shikimic acid at various concentrations induced drastic increases in lycopene in tomato plants particularly at 60 ppm. These results are in agreement with the results of Garcia and Barret (2006) and Favati et al. (2009) who stated that the content of lycopene in fresh tomato fruit was strongly dependent on agricultural techniques and processing methods.

3.3. Photosynthetic pigments

It is clear from Table 4 that shikimic acid at all concentrations significantly increased the contents of the photosynthetic pigments (chlorophyll a, chlorophyll b and carotenoids) in leaves of tomato plants when compared to non-treated control plants. Such stimulations in these contents were highly remarked at 60 ppm. The stimulative effect exerted by shikimic acid on pigment biosynthesis might presumably be due to the fact that shikimic acid increases the rate of transpiration and this will possibly increase the rate of transpiration of minerals and cytokinin from the root to the developing shoot ( Aldesuquy and Ibrahim, 2000 ). Moreover, Uheda and Kuraishi (1978) found that kinetin increased both transpiration and chlorophyll synthesis. In this study, higher concentrations of lycopene corresponded to higher chlorophyll “a” values, confirming the correlation between lycopene and chlorophyll “a” ( Arias et al., 2000 ).

Effect of seed presoaking in shikimic acid on the content of photosynthetic pigments in leaves of tomato plants.

3.4. Nutrient contents

The results in Fig. 1 A–C showed that the application of shikimic acid significantly increased the concentrations of N, P and K in leaves of tomato plants comparing to control plants. The magnitude of increase in these nutrients was markedly observed at 60 ppm of shikimic acid. On the other hand, no significant differences were observed in N and K concentrations in leaves of tomato plants between plants treated with 30 ppm of shikimic acid and control plants. In connection to these results, Xu and Tian (2008) concluded that the application of nitrogen and salicylic acid at low concentration positively increased the foliage fresh and dry weight, fruit yield and mineral contents of pepper plants. Furthermore, the results in this study were in good agreement with those obtained by Aldesuquy and Ibrahim (2000) who demonstrated that seeds’ retreatment with shikimic acid significantly increased mineral contents like P, N. Mg and K in leaves of cowpea plants under natural conditions.

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Effect of seed presoaking in shikimic acid on concentration of nitrogen (A), phosphorus (B) and potassium (C) of tomato plants. Data labeled with different letters are significantly different at P  ⩽ 0.05.

3.5. Total leaf conductivity and transpiration rate

In general, presoaking of tomato seeds with shikimic acid at 30, 60 and 120 ppm induced a drastic increase in total leaf conductance and transpiration rate of tomato leaves when compared to control plants ( Fig. 2 A and B). The magnitude of response varied among the concentration of shikimic acid applied. 60 ppm gave the highest response in the transpiration rate of tomato plants among all treatments. The increase in transpiration rate of tomato plants in response to shikimic acid application may result from the fact that shikimic acid increases the biosynthesis of phenolic compounds particularly coumarin ( Saito et al., 1997 ) which increases the number of both stomata and epidermal cells and therefore increase the rate of water vapor loss through stomata and finally resulted in an obvious increase in total leaf conductance in plants ( Gupta, 1992 ). These results of this study are in agreement with those obtained by Aldesuquy and Ibrahim (2000) in cowpea plants. The analysis of the results in this study (data not shown) revealed that the qualitative parameters of fruit yield and quality were positively related with the amount of transpiration rate and total conductivity in leaves of tomato plants.

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Effect of seed presoaking in shikimic acid on transpiration rate (A) and total leaf conductance (B) of tomato plants. Data labeled with different letters are significantly different at P  ⩽ 0.05.

4. Conclusions

This study has clearly concluded that seed priming with shikimic acid improves plant growth, and fruit quality of tomato plants grown under field conditions by increasing photosynthetic pigments, transpiration rate, enhancing vitamin C, lycopene and carotenoid contents, accumulation of sugars in fruits and nutrient contents of tomato plants. It was observed that 60 ppm of shikimic acid is needed for high yield and better fruit quality of tomato plants when compared to other treatments. In future, this study will be extended to include further investigations on the effect of shikimic acid on some metabolic pathways, different enzymes and endogenous hormonal levels.

Acknowledgements

Author wish to thank the College of Science and Art Research Center and the Deanship of Scientific Research, Shaqra University, Saudi Arabia for supporting this work.

Peer review under responsibility of King Saud University.

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Object name is fx1.jpg

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Peer-reviewed

Research Article

Effect of tomato variety, cultivation, climate and processing on Sola l 4, an allergen from Solanum lycopersicum

Roles Formal analysis, Investigation, Methodology, Validation, Writing – original draft

Affiliation Biotechnology of Natural Products, Technische Universität München, Freising, Germany

Roles Conceptualization, Funding acquisition, Project administration, Supervision, Writing – review & editing

Affiliation Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria, Unità di ricerca per i processi dell’industria agroalimentare (CREA-IT), Milan, Italy

Roles Formal analysis, Writing – review & editing

Roles Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Writing – review & editing

* E-mail: [email protected]

ORCID logo

  • Elisabeth Kurze, 
  • Roberto Lo Scalzo, 
  • Gabriele Campanelli, 
  • Wilfried Schwab

PLOS

  • Published: June 14, 2018
  • https://doi.org/10.1371/journal.pone.0197971
  • Reader Comments

Fig 1

Tomatoes ( Solanum lycopersicum ) are one of the most consumed vegetables worldwide. However, tomato allergies in patients suffering from birch pollen allergy occur frequently. Due to highly similar protein structures of the tomato allergen Sola l 4 and the major birch pollen allergen Bet v 1, patients cross-react with allergenic proteins from tomato as well as other fruits or vegetables. The aim of this study was to quantify Sola l 4 in various tomatoes differing in color, size and shape for identification of varieties with a reduced allergen level. Therefore, an indirect competitive ELISA using a specific polyclonal Sola l 4 antibody was developed. In addition, two varieties, both cultivated either conventionally or organically and furthermore dried with different methods, were analyzed to investigate the influence of the cultivation method and processing techniques on Sola l 4 level. Within 23 varieties, Sola l 4 content varied significantly between 0.24 and 1.71 μg Sola l 4/g FW. The tomato cultivars Rugantino and Rhianna showed the significantly lowest level, whereas in cultivars Farbini and Bambello the significantly highest concentration was determined. Drying of tomatoes in the oven and by sun resulted in a significant decrease. The thermal instability was verified for the recombinant Sola l 4 emphasizing the results for the native protein in dried tomato samples. Overall, the Sola l 4 content is cultivar-dependent and no correlation between color and Sola l 4 amount was found. During the drying process of tomatoes Sola l 4 level was significantly reduced due to thermal instability. Growing conditions have a minor effect whereas seasonal effects show a more pronounced impact. These findings could extend the knowledge about the allergen level of different tomato varieties and may help to improve food safety to potentially increase the life quality of patients suffering from birch pollen allergy.

Citation: Kurze E, Lo Scalzo R, Campanelli G, Schwab W (2018) Effect of tomato variety, cultivation, climate and processing on Sola l 4, an allergen from Solanum lycopersicum . PLoS ONE 13(6): e0197971. https://doi.org/10.1371/journal.pone.0197971

Editor: Hsin-Chih Lai, Chang Gung University, TAIWAN

Received: March 25, 2018; Accepted: May 13, 2018; Published: June 14, 2018

Copyright: © 2018 Kurze et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: This work was supported by Bundesanstalt für Landwirtschaft und Ernährung (BLE) ( https://www.ble.de ) “FaVOR-DeNonDe: Drying, Juices and Jams of Organic Fruit and Vegetables: What happens to Desired and Non-Desired compounds?” (project number 14OE008).

Competing interests: The authors have declared that no competing interests exist.

Introduction

Tomato ( Solanum lycopersicum ) is the most commonly grown and consumed vegetable worldwide [ 1 ]. Due to its high content of lycopene and ß-carotene, acting as antioxidants and free radical scavenger, tomato is beneficial to health decreasing the risk of cancer and cardiovascular diseases [ 2 ]. On the other hand, the consumption of tomatoes can provoke allergic reactions attributed to the presence of various allergenic proteins [ 3 ]. The prevalence of food allergy increased during the last decades affecting 3–4% of the adult population and 5% of children [ 4 ]. Due to varying geographical distribution of specific pollen allergens as well as local dietary habits, geographical diversities in sensitizations patterns between patients suffering from food allergies occur [ 5 ].

A wide range of allergens from plant origin belongs to the pathogenesis-related proteins comprising 17 different protein families [ 6 ]. Induced in plants by various stress conditions these proteins are part of the defense response system. Pathogens such as viruses, bacteria or fungi, application of harsh chemicals (herbicides, fungicides), wounding or diverse environmental changes (dryness, UV light) evoke the expression of PR-genes and the synthesis of PR-proteins. The widespread occurrence and the conservation of the PR-10 protein family within the plant kingdom emphasize an important role of this family [ 7 ]. The major birch pollen allergen Bet v 1 as well as homologous plant food allergens from Rosaceae such as apple (Mal d 1), peach (Pru p 1), cherry (Pru av 1) or strawberry (Fra a 1) belong to the group of intracellular PR-10 proteins with a molecular weight of 16–18 kDa [ 8 ]. The presence of a hydrophobic cavity indicates a potential role in binding nonpolar molecules. Many PR-10 proteins share about 50% of amino acid sequence identity [ 9 ]. However, cross-reactivity occurs due to the high three-dimensional structure similarity. IgE antibodies recognize similar cross-reactive conformational allergen epitopes of different plant sources [ 6 ].

Tomatoes are common sources of plant food allergens [ 10 ]. Approximately 1.5% of the population in Northern Europe [ 11 ] and up to 16% in Italy [ 12 ] is affected by allergy towards tomato. Symptoms of an immunological reaction to tomato can affect the skin (urticarial or dermatitis) but can also lead to oral allergy syndrome, rhinitis or abdominal pain [ 13 ]. Food allergies are associated with a reduced life quality and excluding specific fruits or vegetables from the daily diet. People with food allergies against PR-10 homologous allergens develop symptoms after consumption of fresh fruits. On the contrary, processed products can be tolerated [ 5 ].

Currently, 26 potential proteins from tomato have been reported to provoke allergenic reactions, including different isoforms ( http://www.allergome.org ). Recently, two isoforms of the pathogenesis-related (PR) protein Sola l 4.01 and Sola l 4.02, homologous proteins to Bet v 1, the major birch pollen allergen from Betula verrucosa , have been identified [ 14 ]. Bet v 1.0101 (Acc. No. X15877, UniProt P15494) and the homologous proteins Sola l 4.01 (Acc. No. KF682291) and Sola l 4.02 (Acc. No. KF682292, UniProt K4CWC4) from tomato share 44.0 and 42.5% amino acid identity, respectively [ 14 ].

It has been shown that the allergenic potential of tomatoes is rather dependent on the cultivar and the developmental stages than environmental cultivation conditions [ 5 ]. Since numerous tomato cultivars are available, it might be possible that the concentration of Sola l 4 in some genotypes is sufficiently low, so that patients suffering from birch-pollen related tomato allergy can tolerate these.

Therefore, the aim of this study was to develop an enzyme-linked immunosorbent assay (ELISA) method to quantify Sola l 4 in various tomato cultivars with a specific polyclonal antibody. To analyze a wide range, varieties differing in size, shape and color were chosen. Furthermore, the influence of cultivation conditions (organic vs. conventional) as well as different processing methods (solar, oven and freeze-drying of tomato fruits) on the Sola l 4 content was investigated. It was hypothesized that the Sola l 4 content varies with the color of the mature fruits, the growing condition and the processing method. The results of this study could help to identify tomato fruits with a reduced allergen level to further improve food safety and life quality of birch pollen allergenic patients.

Material and methods

All chemicals were purchased from Sigma-Aldrich (Taufkirchen, Germany), Merck (Darmstadt, Germany) and Roth (Karlsruhe, Germany) unless otherwise noted.

Plant material

Twenty-three different tomato varieties differing in color, size and shape ( S1 Table ) were provided by garden center Böck (Neufarn, Munich, Germany) and grown in the green house under equal temperature, light and water conditions. Fruits were harvested in July 2017 at full maturity (day post anthesis 40–45) of healthy plants without visible symptoms of pathogen infestation and stored at -20 °C until analysis. In the years 2015 and 2016, a local tomato cultivar SAAB and a commercial hybrid HF1 Perbruzzo were cultivated either conventionally or with two types of organic growing in the experimental field of CREA-OF (lat. 42° 53’ N, long. 13° 48’ E) in Central Italy Monsampolo del Tronto, Marche Region. Conventional cultivation soil was tilled and harrowed using Mater-Bi as artificially mulch (conv). Organic farming soil was coated with hairy vetch ( Vicia villosa R.) and mulched either artificially with Mater-Bi (org) or naturally (norg) with mulch film out of lodged vetch. Fruits were harvested at full maturity in August 2015 and 2016.

RNA isolation and cloning of Sola l 4.02

Commercially available tomatoes (cultivar Lyterno) were frozen in liquid nitrogen and homogenized to a fine powder using a Retsch mixer mill (Retsch MM400, Germany). Total RNA isolation and RNA precipitation were performed according to literature [ 15 ], except that the extraction buffer was prepared without spermidine. The concentration of the RNA preparation was determined with NanoDrop 1000 (Thermo Scientific, Germany) and the integrity was confirmed by agarose gel electrophoresis.

First strand cDNA synthesis was applied according to the manufacturer’s instructions (Promega, Germany). The open reading frame (ORF) sequence of the Sola l 4 . 02 gene was amplified with PCR using gene-specific primers published from Wangorsch et al. [ 14 ]. PCR products were cloned into pGEM ® -T Easy vector system according to manufacturer’s instruction (Promega, Germany). In order to obtain the expression vector the gene was amplified with two primers introducing a Sph I site ( Sph I sola l 4 forward ACA TGC ATG CTT GGT GTA AAC ACC TTT ACT ) and Bgl II site ( Bgl II sola l 4 reverse CGGA AGA TCT AGC GTA GAC AGA AGG ATT ) at its 5’end and 3’-end, respectively. The resulting PCR product was digested with Sph I and Bgl II and ligated into the predigested pQE70 vector (Quiagen, Hilden, Germany). After verification of the sequence by Eurofins (Ebersberg, Germany), pQE70- Sola l 4 . 02 plasmid construct was transformed in Escherichia coli BL21 (DE3)pLysS (Novagen, Darmstadt, Germany).

Heterologous expression and purification of Sola l 4.02 protein

Recombinant Sola l 4.02 was expressed in Escherichia coli ( E . coli ) BL21(DE3)pLysS as a fusion protein with a C-terminal His-tag. Cells were grown in 1 l LB medium supplemented with 100 μg/ml ampicillin and 34 μg/ml chloramphenicol at 37 °C to an optical density of 0.6. Gene expression was induced with 1 mM isopropyl β-D-1-thiogalactopyranoside (IPTG) and cultures were incubated for 20 h at 18 °C. Cells were harvested by centrifugation (10 min; 5292 g ; 4 °C) and cell pellets were stored at -80 °C.

Protein purification was performed via immobilized metal affinity chromatography using Profinity Immobilized Metal Ion Affinity Chromatography (IMAC) resin (Bio-Rad Laboratories, Germany). Cell pellets were suspended in 10 ml binding buffer (20 mM sodium phosphate pH 7.4; 0.5 M sodium chloride; 20 mM imidazole) and 0.5 mM PMSF, ultrasonicated and centrifuged for 30 min at 21191 g at 4 °C. The supernatant containing soluble proteins was incubated for 2 h at 4 °C with the IMAC resin. After two washing steps with 10 ml of binding buffer each Sola l 4.02 protein was eluted with elution buffer (20 mM sodium phosphate pH 7.4; 0.5 M sodium chloride; 500 mM imidazole). The purity of the protein fractions was analyzed by SDS-PAGE. Five μg protein were separate in a 12% acrylamide stacking gel at 100 V for 2.5 h under non-reducing and reducing conditions with ß-mercaptoethanol. For protein staining Coomassie Brilliant Blue was used. PageRuler Prestained Protein Ladder (Thermo Scientific) was used as molecular weight marker. Elution fractions containing the respective protein were pooled and dialyzed against Phosphate-Buffered Saline (PBS) pH 7.4 at 4 °C for 20 h. Insoluble particles were removed by centrifugation and the protein solution was used as standard for indirect competitive ELISA.

Production of polyclonal antibodies with specificity for Sola l 4.02

Specific polyclonal Sola l 4 antibody was produced by Davids Biotechnologie GmbH (Regensburg, Germany). Elution fractions of recombinant Sola l 4.02 protein purified from soluble fraction were pooled and used for immunization of rabbits according to a 63-day protocol. Antiserum was further purified via affinity chromatography using a column with Sola l 4 bound to the carrier matrix. Anti-Rabbit-Horseradish peroxidase (HRP) as secondary antibody was purchased from Carl Roth.

Purification of Sola l 4.02 from insoluble fraction (inclusion bodies)

Sola l 4.02 was also purified from the insoluble fractions (inclusion bodies) to examine the ability of refolding of the protein and whether IgG recognition, analyzed by Western blot, was possible. The remaining pellet after cell lysis, ultra-sonication and centrifugation was used. The pellet was resolved in denaturation buffer (20 mM sodium phosphate pH 7.4; 0.5 M sodium chloride; 20 mM imidazole; 8 M urea) at 4 °C over night, centrifuged (1 h; 21191 g ; 4 °C) and refolded against refolding buffer (20 mM sodium phosphate pH 7.4; 0.5 M sodium chloride; 20 mM imidazole) at 4 °C over night via dialysis. After centrifuged (1 h; 21,200 g ; 4 °C) the supernatant was incubated with IMAC resin for 2 h at 4 °C. Protein purification was performed as described above for the soluble protein fraction. Purity of the protein fractions was evaluated by SDS-PAGE and Coomassie staining.

Thermal treatment of rSola l 4.02

Five μg of recombinant Sola l 4.02 of purified pooled elution fractions from soluble fraction was incubated for 10, 20, 30, 60 and 90 min at 99 °C in a Thermoblock (Thermomixer comfort, Eppendorf) and immediately cooled on ice. Untreated protein solution was used as control. The integrity of the protein was further analyzed by SDS-PAGE. IgG binding was investigated via Western blot analysis using a specific polyclonal antibody against Sola l 4.02.

Protein determination

The total protein concentration was determined in microtiter plates (Greiner 96 well plates, polypropylene, Sigma-Aldrich) using Roti ® -Nanoquant following the manufacturer’s instructions (Carl Roth, Germany) with bovine serum albumin (BSA) as standard protein. Absorption at 450 nm and 590 nm was detected with the CLARIOstar plate reader (BMG Labtech, Germany).

Drying of tomato fruits

Ripe fruits were cut into halves or quarters and further dried with three different methods upon constant dry weight. Oven drying was performed at 55 °C for 72 h in a conventional oven dryer (Thermo-Lab, Codogno, Italy). For solar drying only solar irradiance was used and performed in a miniaturized plant (TermoTend System-GTek, Carpi, Italy) for 7 to 10 days. Due to day-night-cycle, temperature varies between 25 °C and 45°C. Freeze-drying was performed for 96 h in an air-forced tunnel and lyophilized using a Dura-Stop tray dryer, combined with a Dura-Dry condenser module (FTS Systems, Stone Ridge, New York) from -35 °C to room temperature and samples were powdered before storage. The water loss was calculated from the difference between fresh and dried weight of the tomato fruit samples. All samples were stored at -20 °C until analysis. Dried fruits were compared to fresh, unprocessed tomatoes, which were only available in the year 2016.

Tomato extracts

For the extraction of proteins from fresh tomatoes an established method [ 16 ] was applied. To reduce the intra- and inter-tomato variability of allergen distribution, eight frozen fruits of one variety were cut into halves or quarters, pooled and grind to a fine powder with a commercial blender (Personal Blender PB 250). For each variety protein extracts were prepared in triplicates. Tomato powder was supplemented with extraction buffer (10 mM KH 2 PO 4; 10 mM K 2 HPO 4 ; 10 mM Na-DIECA; 2 mM EDTA; 2% (w/v) PVPP) containing 0.5 mM phenylmethylsulfonyl fluoride (PMSF) and protease inhibitor cocktail (Complete Protease Inhibitor Cocktail, Roche) 1:2 (w/v) and incubated at 4 °C for 4 h under shaking end over end. For dried plant material a ratio of 1:4 (w/v) was used to ensure proper mixing. Tomato extract were centrifuged for 15 min at 5292x g at 4 °C and dialyzed (3.4 kDa molecular weight cut-off, ZelluTrans, Carl Roth) against PBS pH 7.4. To remove any precipitates, a second centrifugation was performed for 10 min at 16100x g at 4 °C. Extracts were directly used for indirect competitive ELISA.

Indirect competitive ELISA

The Sola l 4 content of tomato samples was determined by indirect competitive ELISA. Recombinant Sola l 4.02 from soluble E . coli fraction was used as competitor. Microtitre plates (immunoGrade ™ Brand) were coated with 100 μl/well purified recombinant Sola l 4.02 protein (0.1 μg/ml) in coating buffer (PBS pH 7.4) and incubated at 4 °C overnight. After plates were washed three times with 300 μl washing buffer (0,05% (v/v) Tween 20 in PBS), free binding sites were blocked with 200 μl 2% BSA in PBS for 2 h at room temperature and washed as before. Dialyzed tomato extracts were diluted in washing buffer and 50 μl were pipetted to each well as “free” Sola l 4. Competition between immobilized and free allergen was performed by adding 50 μl of 2 μg/ml polyclonal Sola l 4-rabbit antibody and incubated for 4 h at 4 °C. Plates were washed four times and sequentially incubated with 100 μl of 1 μg/ml Anti-Rabbit-HRP (Carl Roth, Germany) for 1 h at room temperature. Following a final washing step, 100 μl of 1-Step Ultra 3,3’,5,5’-tetramethylbenzidine (TMB) ELISA solution (Thermo Scientific) were added and the color development was stopped with 100 μl 2 M sulfuric acid after 15 min. The absorption at 450 nm and 620 nm was measured with CLARIOstar plate reader (BMG Labtech, Germany). Standard curves and a negative control were applied on each microplate. The quantification of Sola l 4 allergen in tomato extracts was determined based on the standard curve with recombinant Sola l 4.02 protein. Fifty μl/well of serial dilutions (0.0001–25 μg/ml) of recombinant Sola l 4.02 was pipetted as “free” allergen and followed by the same procedure as the tomato samples. For data analysis the MARS software (BMG Labtech, Germany) was used. Sola l 4 content was expressed as μg Sola l 4 /g fresh weight respectively μg Sola l 4/ g dry weight. Dry matter was converted to fresh weight considering the loss of water in percent during drying process.

Statistical analysis

For the analysis of the experimental data as well as for the box plots the statistical analysis software R (The R Foundation for Statistical Computing, R version i386 3.3.3) was used. Statistical significance levels between the variable groups were calculated using one-way analysis of variance (ANOVA). P values of ≤ 0.05 were considered as significant. For comparisons of mean values Tukey test was performed.

Purification of recombinant Sola l 4.02 protein from soluble and insoluble (inclusion body) fraction

Recently, the two isoforms Sola l 4.01 and Sola l 4.02 have been identified as Bet v 1-related allergens in Solanum lycopersicum in tomato fruits from cultivar Verona [ 14 ]. Sola l 4.02 showed higher immunological activity in comparison to Sola l 4.01 and was therefore selected for the purpose of this study. The corresponding gene was isolated and cloned from tomato cultivar Lyterno showing complete sequence identity with the Sola l 4 . 02 gene (Acc. No. KF682292; [ 14 ]).

Recombinant Sola l 4.02 was produced in E . coli BL21(DE3)pLysS and affinity purified from soluble and insoluble fraction, respectively. Whereas SDS-PAGE analysis of the Sola l 4.02 protein isolated from the soluble fraction showed only a band at the predicted molecular weight of 18 kDa ( Fig 1A ) Sola l 4.02 after denaturation and refolding from inclusion bodies displayed a second band with a molecular weight of approximately 36 kDa ( Fig 1B ). SDS-PAGE under reducing conditions with ß-mercaptoethanol showed only one specific band at 18 kDa ( Fig 1C ).

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(A) Purification from soluble protein fraction, SDS-PAGE under reducing condition with ß-mercaptoethanol (A1 crude extract; A2 flow through; A3 washing; A4 elution 1; A5 elution 2; A6 elution 3). (B) insoluble protein fractions, SDS-PAGE under non-reducing conditions (B1 denaturation; B2 refolding; B3 flow through; B4 elution 1; B5 elution 2; B6 elution 3). (C) insoluble protein fraction (C1 pooled elution 1–3). Under non-reducing conditions, (B) two distinct protein bands were visible in the elution fractions at 18 kDa and 36 kDa. Under reducing condition with ß-mercaptoethanol (A, C) only one band at approximately 18 kDa appeared. Five μg protein per lane were visualized by Coomassie Brilliant Blue G250. M: PageRuler Plus Prestained Protein Ladder.

https://doi.org/10.1371/journal.pone.0197971.g001

Specific polyclonal antibodies against Sola l 4 were produced via immunization of rabbit with purified recombinant protein from the soluble fraction. Western Blot analysis showed that the antibody recognized both, the soluble Sola l 4.02 as well as the refolded protein from inclusion bodies ( S1 Fig ). Furthermore, Western Blot analysis confirmed that the polyclonal antibody specifically recognizes native Sola l 4 allergen extracted from tomato fruits ( S2 Fig ).

Thermal treatment of recombinant Sola l 4.02 protein

Pooled elution fractions of purified recombinant Sola l 4.02 from the soluble protein fraction were thermally treated and analyzed by SDS-PAGE ( Fig 2A ) and Western blot ( Fig 2B ) to investigate the effect of heat on integrity and IgG recognition. After 10 to 30 min at 99 °C the rSola l 4.02 protein was still detectable showing a clear band at 18 kDa in Coomassie stained SDS-PAGE gel ( Fig 2A ). Prolonged heating of 60 min or even of 90 min resulted in diffuse protein bands. Moreover, IgG-binding activity decreased considerably already after 10 min of thermal treatment of the Sola l 4.02 protein and was barely visible after 90 min at 99 °C ( Fig 2B ).

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(A) SDS-PAGE and (B) Western-Blot analysis of purified pooled elution fractions of the recombinant Sola l 4.02 protein heated for 10, 20, 30, 60 and 90 min at 99 °C. Untreated protein served as control (0). SDS-PAGE was performed under reducing conditions. Coomassie Brilliant Blue G250 was used for protein staining. For Western blot analysis specific polyclonal Sola l 4-antibody was used. M: PageRuler Prestained Protein Ladder.

https://doi.org/10.1371/journal.pone.0197971.g002

Validation of the ELISA and extraction method

An indirect competitive ELISA was developed using recombinant Sola l 4.02 as solid phase-bound antigen and as standard protein to determine the Sola l 4 content in various fresh and dried tomato samples. A polyclonal rabbit antibody directed to Sola l 4 was used to detect the Bet v 1-related allergen in tomato extracts. The ELISA showed a typical standard curve ranging was from 0.01 to 10.0 μg/ml ( S3 Fig ). To reduce the intra- and inter-tomato variability of allergen distribution, fine powder of eight frozen fruits of one variety was pooled and further used for protein extraction. Protein extracts were prepared in triplicates and extracts were diluted 2- and 4-fold for ELISA measurement. Finally the Sola l 4 content of one variety was calculated for the three extraction replicates from two dilutions and three technical replicates on the microtiter plate. The Sola l 4 content measured with ELISA was comparable in all three protein extracts ( S3 Fig ).

Influence of tomato variety on Sola l 4 content

Twenty-three different colored tomato varieties of varying sizes and shapes were investigated to analyze the genetic (cultivar-to-cultivar) factor on the expression of Sola l 4 at a translational level in the fruit ( Fig 3A ). Total protein levels of 113.5 to 584 μg soluble protein /g fresh weight (FW) could be extracted from fresh tomatoes ( S1 Table ). Sola l 4 levels ranged from 0.24 to 1.71 μg/g FW ( Fig 3B ). The colors of the box plots represent the respective fruit color. The significantly lowest level of Sola l 4 was found in the cultivars Rugantino and Rhianna with 0.24 and 0.29 μg Sola l 4/g FW, respectively whereas the significantly highest concentration was determined in cultivars Farbini and Bambello with 1.71 and 1.5 μg Sola l 4/g FW, respectively. Ten significance groups (letters a-j) were calculated according to the Tukey Test with 5% of significance level. The percentage of Sola l 4 referred to the total soluble protein amount varied between 0.094% for cultivar Rugantino and 0.658% for cultivar Supersweet ( S1 Table ).

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(A) Diversity of tomato cultivars (bar = 2 cm) and (B) corresponding Sola l 4 content in μg/g fresh weight (FW) determined with indirect competitive ELISA. The color of the box plots corresponds to the color of the ripe tomato fruit. Significant differences for each cultivar were calculated at a significance level of 5%.

https://doi.org/10.1371/journal.pone.0197971.g003

Effect of cultivation and processing methods on Sola l 4 content in dried tomatoes

The influence of cultivation conditions, seasonal effects and processing techniques on the Sola l 4 allergen content in dried tomatoes was studied by ELISA. The two cultivars SAAB and Perbruzzo are genotypes well adapted for the growing conditions in Central East Italy. SAAB is very suitable for growing in organic crop management whereas Perbruzzo, a similar type is more adapted for commercial purposes. Tomatoes were grown in Italy in the years 2015 and 2016 either conventionally or organically, with further classification into conventionally grown with artificial mulch (conv), organically grown with artificial mulch (org) and organically grown with natural mulch (norg). After harvest, ripe fruits were dried in the oven (oven), in the sun (solar) or via freeze-drying (freeze). Water loss in percent was calculated from the difference of fresh and dry weight and was further included for conversion of allergen content of dry matter to fresh matter.

Dried tomato products of both genotypes contained significantly lower levels of Sola l 4 than the fresh fruits ( Fig 4 ), when referring the allergen content of the samples to the corresponding fresh weight, regardless of the cultivation technique. Compared to dried fruits, fresh SAAB and Perbruzzo tomatoes of 2016 contained between 3.66 to 6.25 μg and 3.19 to 3.74 Sola l 4/g FW, respectively.

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(A) Allergen content in μg Sola l 4/g fresh weight (FW) of tomato cultivars SAAB and (B) Perbruzzo determined with indirect competitive ELISA. Plants were grown in Italy in 2015 and 2016 conventionally with artificial mulch (conv), organically with artificial mulch (org) and organically with natural mulch (norg). Tomato fruits were dried via freeze-drying (freeze), in the oven (oven) and in the sun (solar). Allergen content of dried tomato samples was referred to μg Sola l 4/g FW and compared with fresh tomatoes (fresh). Significant differences for each group were calculated at a significance level of 5%.

https://doi.org/10.1371/journal.pone.0197971.g004

In the dried products of the SAAB genotype the allergen content ranged from 1.24 μg Sola l 4/g dry weight (DW) for freeze-dried tomatoes grown organically with natural mulch in 2015 up to 3.93 μg Sola l 4/g DW for solar dried fruits grown organically with artificial mulch in 2016 ( Fig 5A ). This corresponded to 0.07 and 0.23 μg Sola l 4/g FW, respectively ( Fig 4A ). When comparing the two consecutive years, all dried samples of the SAAB genotype from 2016 showed higher allergen content than samples from 2015 ( Fig 5A ) with significant effects for some samples. No significant differences were observed for the influence of the cultivation method when comparing dried SAAB tomato samples from one year and fruits were dried with the same method. Furthermore, there were no significant differences between the three drying methods when comparing dried SAAB samples from one year and plants were grown under the same conditions.

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(A) Allergen content in μg Sola l 4/g dry weight (DW) of tomato cultivars SAAB and (B) Perbruzzo determined with indirect competitive ELISA. Plants were grown in Italy in 2015 and 2016 conventionally with artificial mulch (conv), organically with artificial mulch (org) and organically with natural mulch (norg). Tomato fruits were dried via freeze-drying (freeze), in the oven (oven) and in the sun (solar). Significant differences for each group were calculated at a significance level of 5%.

https://doi.org/10.1371/journal.pone.0197971.g005

The allergen content of dried Perbruzzo samples ( Fig 5B ) ranged from 1.04 μg Sola l 4/g DW for freeze-dried tomatoes grown organically in 2016 with natural mulch up to 10.28 μg Sola l 4/g DW for oven dried fruits grown organically with artificial mulch in 2016. This corresponded to 0.05 and 0.58 μg Sola l 4/g FW ( Fig 4B ). Compared to fresh fruits dried tomatoes showed a significantly lower allergen content ( Fig 4 ). When comparing the two consecutive years, oven and solar dried samples from cltivar Perbruzzo showed higher allergen content in 2016 than samples from 2015 ( Fig 5B ) with significant effects. Strikingly, freeze-dried tomatoes exhibited no significant differences between the two years. The influence of the cultivation method showed no significant effect on the allergen content of Perbruzzo products when comparing dried tomatoes from one year and fruits were dried with the same method.

In Northern Europe, individuals allergic to birch pollen often show cross-reactivity to allergens from Rosaceae fruits or other vegetables and nuts [ 17 ]. IgE antibodies directed to Bet v 1 induced in a primary sensitization reaction to birch pollen can also react with Bet v 1-related proteins from various plant origin [ 18 ]. Here, we have analyzed the Bet v 1-like Sola l 4.02 protein of the PR-10 family whose gene was identified in the S . lycopersicum genome only recently [ 14 ]. We studied the effects of the genotype, cultivation, climate and processing methods on the level of Sola l 4.

Biochemical and immunological properties of recombinant Sola l 4.02

The protein Sola l 4.02 (K4CWC4) shares 42.5% amino acid similarity with Bet v 1.0101 (P15494). SDS-PAGE analysis of the recombinant protein under nonreducing conditions showed that Sola l 4.02 exists in a monomeric and a dimeric form, with a molecular weight of 18 kDa and 36 kDa, respectively ( Fig 1 ). Two cysteine residues at position C113 and C115 might be able to form disulfide bonds. SDS-PAGE under reducing conditions with ß-mercaptoethanol resulted in only one band at 18 kDa, probably due to the cleavage of the disulfide bond. Dimerization did not affect the structure of the protein epitopes as the binding of IgG antibodies and immunological reactivity of the dimers maintained ( Fig 1 ). Dimerization or even oligomerization of recombinant allergens and naturally-occurring allergens was observed previously [ 19 – 21 ]. Similarly, Bet v 1 has been reported to exist as a dimer [ 22 – 25 ]. Although Bet v 1.0101 does not comprise a cysteine residue in its amino acid sequence and the mechanism of dimerization has not been fully elucidated, dimer formation can be induced by mutation of position 5 to a cysteine residue [ 24 ].

Besides of the property of the polyclonal antibody to recognize recombinant Sola l 4 purified from soluble fraction, the purification of Sola l 4 from insoluble inclusion body fraction showed that antibody binding to the refolded protein occurs. After denaturation with urea and refolding of Sola l 4, essential epitopes for antigen-antibody reaction must be present ( S1 Fig ). An important observation is, that the antibody recognizes specifically the allergen extracted from tomato fruits ( S2 Fig ). Purification of proteins from cell pellet under denaturating conditions and refolding is a common method, when the amount of soluble protein is too low. High purity and application in enzyme allergosorbent test, Western blots and basophil histamine release were described for recombinant Pyr c 1, showing similar allergenic activity to the natural allergen from pear [ 26 ]. Furthermore, specific IgE from pear-allergenic patient sera recognized the recombinant protein, purified from inclusion body fraction.

PR-10 (Bet v 1 related) proteins from Rosaceae family are unstable to heat and sensitive to proteases. Therefore, allergic symptoms are restricted to the upper intestinal tract (mouth) since Bet v 1-related proteins are digested by proteases in the lower intestinal tract [ 27 ]. Similarly, heat inactivation of rSola l 4.02 purified from soluble protein fraction was demonstrated ( Fig 2 ). Thermal treatment of the recombinant allergen changed the protein structure in such a way, that recognition of the allergen epitopes by anti-Sola l 4 was remarkably reduced ( Fig 2 ). The same phenomenon has been shown for rPru av 1 from cherry [ 27 ] and the apple allergen Mal d 1 [ 28 ].

Allergenic potential of tomatoes is cultivar dependent

Tomato allergy is often accompanied with pollen allergies [ 29 ]. Depending on the regional distribution of pollen allergens, tomato allergic patients can be sensitized towards several tomato allergens from different protein families [ 5 ]. The best-known groups are allergens homologous to Bet v 1, profilins, and lipid transfer proteins (LTP). Tomato allergy is more common in Southern Europe where allergic reactions are caused by the major allergens Sola l 6 and Sola l 7, proteins belonging to non-specific LTP [ 3 ]. These allergens are heat stable and provoke severe symptoms. However, in Northern Europe Bet v 1 related Sola l 4 allergy is prevalent. Sola l 4 was recognized in 76% of birch/tomato allergic patients highlighting Sola l 4 as major allergen in tomato fruits [ 14 ].

Thus, an indirect competitive ELISA was established using a polyclonal antibody directed to Sola l 4.02 and differently colored tomato genotypes were analyzed as fruit color has been recently correlated with allergen content [ 30 ]. Among 23 different varieties, the allergen content varied between 0.24 and 1.71 μg Sola l 4/g FW, independent of the total soluble protein amount respectively the percentage of Sola l 4 allergen and the color. The high variation in allergen content supports recent results, which showed that patients exhibited different antibody-binding profiles because of varying allergenic activities of tomato cultivars verified with skin prick tests and basophil activation test [ 31 ]. Besides, it seems that Sola l 4 does not function in carotenoid biosynthesis, the major group of colorants in tomato.

Fresh tomato fruits from cultivars SAAB and Perbruzzo from Italy show generally higher Sola l 4 allergen content compared to the collection of varieties from garden center Böck (Germany). Different locations and climatic conditions are an important parameter affecting [ 32 ] the allergen level, previously shown for Mal d 1 content in apples. Besides this, tomatoes from Germany were cultivated in the greenhouse.

Allergenicity of fruits is cultivar dependent as evaluated for the major apple allergen Mal d 1 [ 32 , 33 ]. Allergen level of the Bet v 1-homologous Mal d 1 in apple varied between 3.8 and 72.5 μg/g pulp [ 33 ] or between 2.3 and 20.1 μg/g FW [ 32 ]. Thus, the content of Bet v 1-homologous proteins in apples is higher than the corresponding protein in tomatoes ( Fig 3 ). Apple allergies affect up to 2% of the population in Europe and Northern America. The prevalence of tomato allergies caused by PR-10 related allergens, however, is rare. The lower Sola l 4 allergen level in tomato compared to apple fruits might be a reason for that. Especially in the Mediterranean area tomato allergy is more relevant with severe symptoms provoked by allergens from LTPs and profilins.

It has to be taken into account that, in addition to Sola l 4.01 and Sola l 4.02, additional isoforms might be expressed in tomato fruits playing a role for PR-10 allergenic patients. The severity of an allergic reaction to fruit is related to the individual sensitivity of the patient and moreover depended on the cultivar. Identification of specific IgE-antibodies in patient sera and skin prick test with different varieties reveal in most of the cases a wide range from low to high allergenic reactivity. Thus, the results of the ELISA have to be confirmed by further immune tests but can be helpful to improve the quality of tomato cultivars.

Drying processing of tomato fruits has major effect on allergen content

During food processing the allergenic properties of food allergens can be altered by various parameters. Washing or peeling of the food material, breaking up through grinding or cutting, thermal treatment, fermentation processes or even purification steps in the manufacturing procedure may have an effect on the allergenic properties of food allergens [ 34 ]. Changes in epitope protein structure can be the factor for both, decreasing or increasing allergenic activity.

Non-specific LTPs are a major elicitor of tomato allergies. Both, in fresh fruits as well as in industrial products LTP are contained in crucial amounts, triggering severe allergic symptoms [ 35 ]. Due to the high resistance to proteases and heat, these proteins maintain their immunological activity [ 3 ]. In contrast, Bet v 1 related proteins are heat-labile and patients allergic to PR-10 proteins might tolerate processed food or food products. The loss of allergenicity due to thermal processing was investigated for several Bet v 1-related allergens, such as Mal d 1 [ 28 ] and Pru av 1 [ 27 ]. Furthermore, we showed that recombinant Sola 1 4.02 is also heat sensitive ( Fig 2 ).

Since dried tomatoes are a common product in food industry, the Sola l 4 amount was determined in a number of differently dried fruits. Due to thermal treatment, the level of the Sola l 4 allergen decreased significantly ( Fig 4 ). Considering the loss of water during the drying process, dried tomatoes contain considerably lower Sola l 4 amount than fresh tomatoes. Both, the experiment with the recombinant protein and with tomato extracts from dried fruits affirm the heat-sensitivity of this PR-10 protein. Although freeze-drying is a gentle drying method known to preserve the protein structure, freeze-dried tomato samples contained the same low allergen content as oven and solar dried fruits. Due to the loss of water during drying, the protein structure of the soluble Sola l 4 protein becomes altered and is not recognized any more by the antibody. In addition to that, the protein might be degraded and therefore the antibody is unable to recognize the protein fragments. No significant changes in Sola l 4 levels between freeze-, solar-, and oven drying were observed for cultivar Perbruzzo in 2015 ( Fig 5 ). In contrast, differences were detected in 2016. Removal of water by oven and solar-drying seemed to be less effective in 2016 promoting protein solubility and allergen stability. For cultivar SAAB the differences were insignificant between freeze-, solar-, and oven drying in both years 2015 and 2016.

According to the meteorological data ( Table 1 ) from the growing region of tomato cultivars SAAB and Perbruzzo in Monsampolo del Tronto, the rainfall was significantly higher in 2016 than in the previous year. From May to August 2015 167.6 liter per square meter were measured, compared to 267.2 liter per square meter during the same season in the following year. The average daily temperatures from May to August were slightly lower in 2016 with 21.6 °C compared to 2015 with 22.9 °C, which is in accordance with higher rainfall in 2016. Sola l 4 allergen levels of dried tomato fruits were higher in 2016 than in 2015 for the majority of analyzed samples. Due to strong rain and high humidity, the pathogen infestation is increased and might lead to upregulation of PR-10 genes. Thus, varying weather conditions including average temperature, precipitation and humidity seem to have a more important effect on the allergen content than conventional or organic growing including the fact that pathogen growing is promoted under specific climatic conditions leading to induction of PR-10 genes. We conclude that growing conditions and seasonal effects such as low humidity and high temperature, which reduce the propagation of pathogens, would also reduce Sola l 4 content.

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https://doi.org/10.1371/journal.pone.0197971.t001

In summary, the level of Bet v 1-related allergen in tomato fruits varied significantly between cultivars. Furthermore, the heat sensitivity of the PR-10 protein Sola l 4 was confirmed for the recombinant protein as well as for tomato samples, when fruits were exposed to heat during the drying process. Sola l 4.02 may be a marker for breeding hypoallergenic tomato varieties.

Supporting information

S1 fig. recombinant sola l 4.02 protein purified from inclusion body fraction..

(A) SDS-PAGE and (B) Western-Blot analysis of pooled elution fractions of the recombinant Sola l 4.02 protein purified from insoluble fraction (IB). SDS-PAGE was performed under reducing conditions. Coomassie Brilliant Blue G250 was used for protein staining. For Western blot analysis specific polyclonal Sola l 4-antibody was used. M: PageRuler Prestained Protein Ladder.

https://doi.org/10.1371/journal.pone.0197971.s001

S2 Fig. Protein pattern of tomato extracts.

(A) SDS-PAGE and (B) Western-Blot analysis of native tomato protein extracts exemplarily shown for different commercially available tomato cultivars. SDS-PAGE was performed under reducing conditions. Coomassie Brilliant Blue G250 was used for protein staining. For Western blot analysis specific polyclonal Sola l 4-antibody was used. The 18 kDa band, corresponding to the native Sola l 4, is marked with an arrow. M: PageRuler Prestained Protein Ladder.

https://doi.org/10.1371/journal.pone.0197971.s002

S3 Fig. Indirect competitive ELISA and protein extraction.

(A) Standard curve of indirect competitive ELISA to quantify Sola l 4 in tomato and (B) reproducibility of the protein extraction method exemplarily shown for cultivars Farbini, Gardenberry and Orama.

https://doi.org/10.1371/journal.pone.0197971.s003

S1 Table. Tomato cultivars.

Sola l 4 content (mean values) in μg/g fresh weight (FW), total soluble protein in μg/g FW and percentage of Sola l 4/total soluble protein of different tomatoes. Plants were grown at garden center Böck (Neufahrn, Munich).

https://doi.org/10.1371/journal.pone.0197971.s004

Acknowledgments

We thank garden center Böck for providing the tomato samples.

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Review article, tomato responses to salinity stress: from morphological traits to genetic changes.

tomato research papers pdf

  • Department of Horticultural Technologies, Faculty of Horticulture, “Ion Ionescu de la Brad” Iasi University of Life Sciences, Iasi, Romania

Tomato is an essential annual crop providing human food worldwide. It is estimated that by the year 2050 more than 50% of the arable land will become saline and, in this respect, in recent years, researchers have focused their attention on studying how tomato plants behave under various saline conditions. Plenty of research papers are available regarding the effects of salinity on tomato plant growth and development, that provide information on the behavior of different cultivars under various salt concentrations, or experimental protocols analyzing various parameters. This review gives a synthetic insight of the recent scientific advances relevant into the effects of salinity on the morphological, physiological, biochemical, yield, fruit quality parameters, and on gene expression of tomato plants. Notably, the works that assessed the salinity effects on tomatoes were firstly identified in Scopus, PubMed, and Web of Science databases, followed by their sifter according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline and with an emphasis on their results. The assessment of the selected studies pointed out that salinity is one of the factors significantly affecting tomato growth in all stages of plant development. Therefore, more research to find solutions to increase the tolerance of tomato plants to salinity stress is needed. Furthermore, the findings reported in this review are helpful to select, and apply appropriate cropping practices to sustain tomato market demand in a scenario of increasing salinity in arable lands due to soil water deficit, use of low-quality water in farming and intensive agronomic practices.

Introduction

Tomatoes ( Solanum lycopersicum L.) are widely consumed worldwide as fresh or processed food products (e.g. canned tomatoes, sauce, juice, ketchup, soup, etc.) ( Campestrini et al., 2019 ; Li et al., 2021 ) ranking second in the top of the most consumed vegetables in the United States of America, after potatoes ( Reimers and Keast, 2016 ). These fruits have a high content of nutrients and bioactive substances ( De Sio et al., 2021 ; Ali et al., 2021a ) that are beneficial for a healthy body, a healthy skin, and weight loss, and which may ameliorate or prevent various human chronic degenerative diseases ( Ali et al., 2021a ). Tomato fruits are rich in carotenoids (e.g. β-carotenoids and lycopene), ascorbic acid (vitamin C), tocopherol (vitamin E), and bioactive phenolic compounds such as quercetin, kaempferol, naringenin and lutein, caffeic, ferulic and chlorogenic acids ( Dasgupta and Klein, 2014 ; Mihalache et al., 2020 ; Stoleru et al., 2020 ; Murariu et al., 2021 ). The carotenoids from tomatoes are known to display anticancer properties and to be excellent deactivators of reactive oxygen species (ROS) (e.g. for singlet oxygen ( 1 O 2 ) and peroxyl radical (ROO•)) ( Campestrini et al., 2019 ; Stoleru et al., 2020 ). Lycopene, which is an antioxidant, might protect the cells against oxidative damage and prevent cardiovascular disease and various types of cancer (e.g. prostate, breast, lung, bladder, ovaries, colon, as well as pancreas cancer) ( Dasgupta and Klein, 2014 ). Li et al. (2021) ascertained in their study that the consumption of tomatoes provides about 85% of the daily dose of lycopene required by the population of North America and 56–97% in five European countries.

According to FAOSTAT database, in 2020 about 251,687,023 tonnes of tomatoes were harvested from 6,163,463 hectares worldwide, with a yield average of 40.84 tonnes/ha ( FAOSTAT, 2022 ). In 2020, the European Community reported a production of 16,657,000 tonnes, of which 9,801,000 tonnes were processed and 6,856,000 tonnes were consumed fresh. Compared to the previous year, EU production increased by almost 1%. In the last 10 years, the average annual tomato production in the EU was 16,474,000 tonnes, with the lowest value recorded in 2012 and 2013 (15,082,000 tonnes) and the highest in 2016 (17,862,000 tonnes) ( European Commission, 2021 ).

Annually, a wide variety of factors can affect tomato yield and fruit nutritional quality ( Inculet et al., 2019 ). Among these factors, the salt content in soil and water used in irrigation stands out. According to Shrivastava and Kumar (2015) “ worldwide 20% of total cultivated and 33% of irrigated agricultural lands are afflicted by high salinity ”. Furthermore, by the year 2050 more than 50% of the arable land will probably become saline soils as a consequence of weathering of native rocks, irrigation with saline water, climate change projections predicting increasing drought events forcing farmers to make use of salty water, and intensive agronomic practices. The Food and Agriculture Organization of the United Nations ascertained that every year soil salinization takes 1.5 million ha of farmland out of production and annually decreases the production potential by up to 46 million ha per year. In sum, soil salinization has been causing annual losses in agricultural productivity estimated to be US $ 31 million ( FAO, 2022 ).

Tanji ( 2002 ) defined the salinity as “ concentration of dissolved mineral salts present in soils (soil solution) and waters ”. In small amounts, the dissolved salts are vital for the normal plant growth and development, but at high levels, they become harmful and often cause the death of plants ( Nebauer et al., 2013 ). Sodium chloride is the most common salt detected in salty soils and waters, along with the chloride, sulfate, and carbonate salts of calcium, magnesium, and sodium ( Nebauer et al., 2013 ; Riaz et al., 2019 ). Soil and water salinization generally occurs naturally, but the human factor via land clearing and inappropriate irrigation practices emphasizes this phenomenon. The soil is generally considered salt-affected when its electrical conductivity (EC) is above 4 dS·m -1 . The soil salinity can be also increased by rainwater, which according to Riaz et al. (2019) can contain even 650 mg·kg -1 NaCl.

Salinity induces various deleterious effects on plants which are forced to react. Depending on the post-exposure phase, plant responses induced by salinity can be grouped into ( Negrão et al., 2017 ; Isayenkov and Maathuis, 2019 ):

(I) the ion-independent response which occurs in the first hours-days after exposure and is characterized by stomatal closure and inhibition of cell expansion mainly in the shoot, and general plant growth;

(II) the ion-dependent response which takes place over days or even weeks and is characterized by the slowdown of the metabolic processes, premature senescence, and ultimately cell death.

Plant adaptation to saline stress depends significantly on a multitude of physiological and molecular mechanisms which are classified into three main categories: osmotic tolerance, ion exclusion, and tissue tolerance ( Munns and Tester, 2008 ; Roy et al., 2014 ; Isayenkov and Maathuis, 2019 ). Under salinity stress, the plants maintain their growth and development, by tolerating the water loss, preserving the leaf expansion and stomatal conductance (osmotic tolerance), avoiding the accumulation of Na + ions in the shoots and leaves at toxic concentrations (by ion exclusion) and protecting the plant cells against the toxic action of Na + through its removal from the cytosol and subsequent sequestration in vacuoles (tissue tolerance) ( Munns and Tester, 2008 ; Hasegawa, 2013 ; Roy et al., 2014 ). A range of transporters and their controllers at both plasma membrane and tonoplast levels are involved in ion exclusion and tissue tolerance. The ways of plants react to salinity stress at molecular, cellular, metabolic, and physiological levels, as well as the mechanisms involved in salinity tolerance are far from being completely understood ( Gupta and Huang, 2014 ; Maathuis, 2014 ). Under osmotic stress, the cell expansion in root tips and young leaves is immediately reduced and stomatal closure is induced. Plant tolerance to salt is mediated by various biochemical pathways that support water retention and/or acquisition, protection of chloroplast functions and the maintenance of ion homeostasis ( Ludwiczak et al., 2021 ). Proline, glycine-betaine and soluble sugars are the main osmoprotectants synthesized by plants to balance the osmotic difference between the cell's surroundings and the cytosol and to protect the cell structure ( Gupta and Huang, 2014 ; Sharma et al., 2019 ). According to Roy et al. (2014) , the action of the tolerance mechanisms is highly dependent on the salinity level. For example, the Na + exclusion is more effective in conditions of high salinity, while osmotic tolerance may be the most important tolerance mechanism at moderate salinity. In Figure 1 the possible adaptive responses of plants to salt stress is schematically shown ( Horie et al., 2012 ; de Oliveira et al., 2013 ).

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Figure 1 Plant adaptive responses to salt stress.

Plant exposure to salinity causes negative effects on their growth and development, even leading to their death. The first visible sign of salinity stress in plants is usually stunted growth, with plant leaves often colored in bluish-green ( Zahra et al., 2020 ). Toxicity of Na + occurs with time and after a great concentration increase of these ions in the older leaves which causes their premature death ( Hasegawa, 2013 ). Salinity induces osmotic stress, excessive uptake of sodium and chloride ions (cytotoxicity), and nutritional imbalance, impairing the plant growth and development ( Zahra et al., 2020 ; Ludwiczak et al., 2021 ). Plant exposure to saline stress also causes oxidative stress due to the generation of reactive oxygen species (ROS) ( Isayenkov and Maathuis, 2019 ). High levels of salt cause physiological dysfunctions, affect photosynthesis, respiration, starch metabolism, and nitrogen fixation, and lead to reduced crop yield ( Zahra et al., 2020 ). Salt accumulation inside the plant tissues above the tolerance limits leads to several negative changes in plant morphology, physiology, biochemistry and crop productivity. Salinity reduces water availability for plant use and due to unfavorable osmotic pressure, the roots are unable to absorb the water ( Shrivastava and Kumar, 2015 ). According to Hasegawa (2013) , Na + causes the destabilization of membranes and proteins and negatively affects the fundamental cellular and physiological processes, mainly the division and expansion, primary and secondary metabolism, and mineral nutrient homeostasis. In addition, Na + competes with K + uptake causing K + deficiency. The adverse effects of soil salinity on plants have been proven to be caused not only by Na + cations but also by Cl − anions ( Acosta-Motos et al., 2017 ). It has been reported in various studies that Cl − apart from having a toxic effect on plants, it also is a beneficial element for higher plants. As a micronutrient, Cl − regulates the leaf osmotic potential and turgor, stimulates growth in plants by increasing the leaf area and biomass, and improves the photosynthetic performance of plants ( Colmenero-Flores et al., 2019 ; Franco-Navarro et al., 2019 ; Wu and Li, 2019 ). Geilfus (2018) stated that 0.2–2 mg g –1 fresh weight of Cl − can act in stabilizing the oxygen-evolving complex of photosystem II, maintaining the electrical potential in cell membranes, regulating tonoplast H + -ATPase and enzyme activities. Na + cations are usually more toxic than chlorine anions in plants, but Wu and Li (2019) asserted that the salinity effects observed in soybeans and avocado were mainly due to Cl − toxicity. High concentrations of Cl – caused nitrogen or phosphorus deficiency, interfered with photosystem II (PSII) quantum yield and photosynthetic electron transport rate, and induced necrotic lesions, resulting in the symptom of leaf-tip burning and impairment of photosynthesis and growth ( Teakle and Tyerman, 2010 ; Wu and Li, 2019 ).

Due to both Na + and Cl − toxicity, high levels of salt can induce a large number of negative effects on tomato plants: alteration of phenological development, replacement of nutrients with sodium and chloride ions, osmotic inhibition, photosynthetic reduction, nutrient deficiencies or imbalances, changes in gene expression and protein synthesis, and negative effects on crop productivity ( Figure 2 ). Salinity affects almost all aspects of plant growth including germination, vegetative growth and reproductive development. Plants are generally more sensitive to salinity during germination and early growth, and excessive accumulation of sodium in cell can rapidly lead to osmotic stress and cell death ( Shrivastava and Kumar, 2015 ).

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Figure 2 Salinity effects on tomato plants.

According to Ibrahim (2018 ) and Zaki and Yokoi (2016) , tomato is a moderately tolerant species to salinity, and seed germination, plant growth and fruit development are just affected by high salinity levels. The response to salinity depends mainly on the tomato genotype ( Zaki and Yokoi, 2016 ) and it has been demonstrated that salt tolerance is controlled by several gene families ( Ali et al., 2021a ). Studies conducted so far have highlighted that the different levels of salts in soil or in the irrigation water can induce changes in plant morphology, physiology, and biochemistry, with particular consequences on yield and fruit quality.

The knowledge of the salinity effects on tomato plants and fruits is an asset in the selection and application of the appropriate crop practices to fulfill tomato market demand. The assessment of the tomato responses to salinity stress is the main focus of this review, which was achieved through: (i) identification in Scopus, PubMed, and Web of Science databases of research works that assessed the effects induced by salinity on tomatoes, followed by (ii) their sifter according to PRISMA guideline and (iii) emphasis of the salinity effects on morphology, physiology, biochemistry, yield, fruit quality and gene expression of tomato plants induced by different levels of salts in water and soil.

Bibliographic research and data collection

The problem of plant salinity stress has attracted the attention of many researchers who have been focusing on this topic. The main research approaches refer both to the effects of salinity on plant growth and development and to the possible strategies to increase plant tolerance to salinity. In this study, only original scientific papers which were published in the last 10 years, in peer-reviewed journals, and underlying the individual salinity effects on morphology, physiology, biochemistry, yield, fruit quality, and gene expression of tomato plants induced by different levels of Na, K and Mg salts in water and soil were included. PRISMA guideline ( Page et al., 2021 ) was used in this review to extract from Scopus, Web of Knowledge and PubMed databases the scientific papers focused on the assessment of the effects induced by salinity on tomato plants.

The key expression “tomato salinity effects” was used to identify the scientific papers and the search returned 529, 751, and 178 articles in Scopus, Web of Science, and PubMed databases respectively, published in the last 10 years. According to the PRISMA flow diagram ( Figure 3 ) after repetitive publications removal, 964 scientific papers were considered in the screening step. Following a careful reading of titles and abstracts, 435 articles were identified as incompatible with the search topic. Subsequently, the full texts of the left papers were downloaded and assessed to identify the works eligible with the established criteria. After an extensive screening, 11 papers in another language than English, 23 articles without full text, 250 articles focused on the methods and practices that could increase the tomato tolerance to saline stress, and 99 items for other reasons (e.g., reviews, inadequate experimental criteria data, book chapters, conference papers, are not highlighted the salinity effects, etc.) were removed.

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Figure 3 Preferred Reporting Items for Systematic Reviews and Meta-Analyses PRISMA flow diagram for the targeted systematic review.

Finally, only 146 original articles were eligible based on the inclusion criteria. The detailed analysis of these articles led to the following results ( Figure 4A ):

● 14 articles focused on salinity’s impact on seed germination;

● in 92 articles the plant/parts of the plant height, fresh/dry weight, leaf area, and/or flower/ branch number depending on salinity level in the soil or water were measured;

● in 87 articles the physiological parameters related to photosynthesis, osmosis, nutrients uptake, and water content in plant parts were evaluated;

● in 81 articles the biochemical activity of tomato plants under saline stress was assessed. The main parameters analyzed were enzymatic activity, proteins, sugars and other compound synthesis, hormonal levels, and/or molecular biology analyses.

● and only in 51 scientific papers, the impact of saline stress on yield and/or fruit quality was studied.

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Figure 4 The number of relevant articles (A) which underline the salinity impact on tomato morphology, physiology, biochemistry or/and yield and fruits and (B) published annually starting from 2012.

Out of the 146 full articles assessed for eligibility, only 98 studies were included in the reference list, following the evaluation of the information reported by the proposed objectives. In the last 10 years, at least 12 articles focusing on the impact of salinity on tomato morphology, physiology, biochemistry, and yield have been published annually in Scopus, Web of Science, and PubMed databases, respectively ( Figure 4B ).

Morphological changes of tomato plants under salinity stress

Salinity strongly influences all the aspects of a tomato plant’s life, producing changes even in the morphological characteristics. In general, the morphology of a plant is a reflection of its environmental conditions, proving information about its metabolic function. Increases in salt content and in particular of sodium chloride in the growing environment can significantly affect the plant’s physical appearance, but also the germination traits of tomato seeds. In the study conducted by Sholi (2012) , it was reported that the increase of NaCl concentration in the 1/2 MS solidified medium delayed the seed germination of all four tomato cultivars: Jenin 1, Hebron, Ramallah and Maramand. The experiments were done in Petri dishes and incubated in the light at 23 ° C. The medium with the corresponding salt concentration was solidified with 8 g L -1 agar. At 0 mM NaCl the time required for germination of 50 % of ‘Jenin 1’ seeds was 2.45 days, but at 100 mM NaCl the same germination rate was reached in 8.51 days. At 150 mM NaCl the germination of ‘Jenin 1’, ‘Hebron’ and ‘Maramand’ cultivar seeds were completely inhibited. Similar results were obtained by Abdel-Farid et al. (2020) , who observed that a salinity level of 50, 100 and 200 mM, NaCl reduced significantly the germination rate of tomato seeds, while at 100 and 200 mM NaCl the germination of tomato seeds was completely inhibited. The authors explained that the delay in seed germination may be due to the impairment of enzyme activity by the partially osmotic or ion toxicity. González-Grande et al. (2020) found that 85 mM NaCl reduced the seed germination rate of tomato cultivar Río Grande by 6.4% compared with the control (0 mM). At 171 and 257 mM NaCl the germination was severely affected, the rate being lower than 2.8%. The experiments were done in sterile Petri dishes on filter papers. Paradoxically, at 100 mM NaCl, Tanveer et al. (2020) reported a germination rate of 80% for tomato seeds. In the study of Adilu and Gebre (2021) , a delay in seed germination with salinity increase was observed, the mean germination times (days) for the four selected tomato varieties (Sirinka, Weyno, ARP D2, and Roma VF) were 10.70, 8.72, 7.31, and 6.85 days respectively at 4 dS m -1 and 5.79, 5.69, 4.68, 5.09 days respectively at 0 dS m -1 . According to Adilu and Gebre (2021) a low level of NaCl induces seed dormancy while a high level inhibits seed germination. González-Grande et al. (2020) ; Abdel-Farid et al. (2020) and Adilu and Gebre (2021) explained that the reduction in germination rate and percentage under salt stress can be linked to a decrease in water potential gradient among seeds and their surrounding medium. Furthermore, the osmotic and toxic effects of NaCl affect the enzyme activation during seed germination and the gibberellin acid content.

Regarding the salinity effects on plant morphology, changes can appear in all stages of plant development, affecting the plant height, root/shoot ratio, leaf area, number of branches, or the number of leaves/flowers per plant. The studies focusing on the salinity effects on tomato plants showed that the intensity of plant morphology changes depends on the salt level in the growing environment. In addition, each cultivar/hybrid responds differently to saline stress. Assimakopoulou et al. (2015) assessed the responses of three cultivars (Santorini Authentic, Santorini Kaisia and Chios) and four hybrids of cherry tomato (Cherelino F 1 , Scintilla F 1 , Delicassi F 1 , and Zucchero F 1 ) at 0, 75 and 150 mM NaCl in a mix of loamy soil and perlite (3:1 v/v). The results of this study showed that cultivar Chios was the most affected at 150 mM and its total plant dry weight decreased by 65.37% and the root/upper plant part ratio in terms of fresh weight from 0.09 to 0.03. The total plant dry weight of the other cherry tomato cultivars was reduced by 52.52-56.52% at the highest salinity level compared to the lowest level. Assimakopoulou et al. (2015) stated that the growth inhibition was due to the toxicity of Cl - and Na + ions and to the nutritional imbalance induced by salinity. Samarah et al. (2021) assessed the tomato seedling growth in response to four saline water solutions of NaCl (0, 5, 10, and 15 dS m -1 ). The seedlings at 15 dS m -1 had a mean length of 3.8 cm and a dry weight of 9 mg, showing a longer length and weight at 0 dS m -1 (16.2 cm and 45 mg/seedling, respectively).

The harmful effects of salinity on leaf area, leaf number, and leaf length also increase with the salt concentration rise, according to the studies performed by Babu et al. (2012) ; De Pascale et al. (2012) ; Hossain et al. (2012) ; Lovelli et al. (2012) ; Sánchez et al. (2012) ; Martínez et al. (2014) ; Al Hassan et al. (2015) ; Abouelsaad et al. (2016) ; Parvin et al. (2016) ; Chaichi et al. (2017) ; Rahman et al. (2018) ; Abdelaziz and Abdeldaym, (2019) ; Maeda et al. (2020) . The cultivar Raf exposed at a salinity level of 5.5 dS m -1 had 2708 cm 2 for the leaf area, but at 11 dS m -1 the leaves were smaller, and their leaf area decreased to 1815 cm 2 ( Sánchez et al., 2012 ). According to De Pascale et al. (2012) , the saline water with an electrical conductivity of 4.4 dS m -1 used in tomato irrigation reduced the leaf number per plant from 82.6 at 48.9 and their leaf area with 47.55%, compared to the control. In their study, Babu et al. (2012) assessed the morphological changes induced by salinity on tomato cultivar PKM 1 based on leaf area, dry matter weight percentage, plant height and number of fruits per plant. Irrigation during 90 days with water containing NaCl at the concentrations of 0, 25, 50, 100,150, and 200 mM immediately after sowing caused negative changes in tomato plants. For example, it was found that the treatment with 200 mM NaCl reduced the plant leaf area by 43.91% and the fruit number per plant to 4 compared to 15 in the control. In addition, at this concentration, the plant height was 76.17 cm shorter compared to the control. In another study, irrigation with water having EC between 1.75 and 10.02 dS m -1 produced significant effects on specific leaf area, number of nodes per stem, fresh weight of roots/shoots/leaves, and length of primary roots/stem of the tomato cultivars Roma and Rio Grande ( Prazeres et al., 2013 ). Increasing the NaCl concentration, in the irrigation water up to 3.22 dS m -1 led to an increase in the fresh weight of cultivar Roma leaves (by 84.7 g per plant), but at a higher NaCl concentration the leaf weight was reduced by 2.98-31.33 g. At 5.02 dS m -1 the leaf weight per plant was 157.80 g, with a non-significant reduction induced by salinity compared to the control whose leaf weight was 160.78 g per plant. In contrast, the fresh weight of the stems and roots decreased with the NaCl content increase in irrigation water. For cultivar Rio Grande the water EC higher than 1.75 dS m -1 had a positive effect on the fresh weight of roots, shoots and leaves, on specific leaf areas, number of nodes per stem and length of primary roots and stem ( Prazeres et al., 2013 ). Several other studies have shown that the salt variation in the growing medium caused negative or positive changes in fresh biomass, plant height, root/shoot ratio, leaf areas, number of branches, and number of leaves/flowers per plant. In this respect, the results of some studies which assessed the morphological changes in tomato plants under salinity stress have been reported in Table 1 . Reducing plant height, leaf area, leaf number, and leaf length under salt stress conditions may be an adaptive morphological strategy to limit the water loss through transpiration. However, it could also be the result of the toxicity of Na + and Cl - ions accumulated in cells, which slow the cell growth of young leaves ( Negrão et al., 2017 ).

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Table 1 Morphological changes in tomato plants under salinity stress.

The same authors interestingly focused on tissue and cellular levels to assess the morphological alterations caused by salinity in tomato plants. In this respect, Bogoutdinova et al. (2016) investigated the cell organization of the epidermis and parenchyma cortical tissues of tomato hypocotyl under different levels of NaCl in vitro . The size of the intercellular spaces in the cortical parenchyma as well as the average cross-sectional areas and shape of epidermal and cortical parenchyma hypocotyl cells of tomato line YaLF and cultivar Rekordsmen were significantly affected by the addition of NaCl to the culture medium. At 250 mM NaCl, the highest increase in the cell areas of tomato line YaLF was observed and the epidermal cell became angular in contours.

Physiological changes under salinity stress

Plant physiological processes are very sensitive to all environmental changes. Variations in NaCl and other salt levels in soil or hydroponic cultivation have a strong impact on the physiology of plants. Depending on the stress duration and severity, changes that can occur in the physiological processes affect plant growth, development, and productivity. The studies done on tomatoes in the last 10 years highlighted a negative influence of salinity stress on the physiological parameters such as photosynthetic rate, transpiration, stomatal conductance, chlorophyll content and mineral uptake ( Hossain et al., 2012 ; Lovelli et al., 2012 ; Giannakoula and Ilias, 2013 ; Maeda et al., 2020 ; Yang et al., 2021 ). For instance, Maeda et al. (2020) reported that the increase of Enshi nutrient solution EC from 1.2 to 6 dS m -1 caused the reduction of: photosynthetic rate by 10.2 % and 12.4 %, respectively, in tomato leaves of cultivars CF Momotaro York and Endeavour; transpiration rate and stomatal conductance by 26.9% and 23.4%, respectively, in the cultivar CF Momotaro York, and by 24.6% and 24.1%, respectively, in the cultivar Endeavour. At 6 dS m -1 , the stomatal conductance of tomato leaves grown in silt loam soil was 0.03 mol m -2 s -1 , i.e., 0.05 mol m -2 s -1 lower than in control (EC= 0 dS m -1 Na) ( Parvin et al., 2016 ). Marsic et al. (2018) reported that the photosynthetic and transpiration rates as well as stomatal conductance were lower in the leaves of tomato cultivars Belle and Gardel raised in hydroponics with electrical conductivity of 6 dS m -1 , compared to 2 dS m -1 . The photosynthetic and transpiration rates and stomatal conductance of cultivar Belle leaves were lower by 44.1%, 52.9% and 90%, respectively, than the control, and by 40.3%, 48.6% and 91.3%, respectively compared to cultivar Gardel. According to Marsic et al. (2018) , the decreased values of these parameters could be due to the stomatal closure induced by water deficit.

Like the photosynthesis rate, the chlorophyll synthesis in tomato plant leaves can be negatively affected by the exposure to high salt levels ( Giannakoula and Ilias, 2013 ; Taheri et al., 2020 ). This may happen due to metabolic disorders which result in decreased chloroplast activity and photosynthesis, increased chlorophyllase enzyme activity, and respiration, followed by reduced chlorophyll contents ( Taheri et al., 2020 ). Singh et al. (2016) found in their study that the chlorophyll content in ‘Lakshmi’ tomato leaves was reduced from 0.996 mg g -1 to 0.751 mg g -1 when the NaCl level increased from 0 to 0.5 g kg -1 in soilless cultivation. The same trend was observed in chlorophyll b synthesis, whose content decreased by 27.73% compared to the control. In another study carried out on the tomato cultivar Super Chef grown in hydroponics, the total chlorophyll content decreased by 40.93% at 120 mM NaCl compared to the control (0 mM NaCl) ( Taheri et al., 2020 ).

The effects of salinity on photosynthesis processes in tomatowere evaluated in various studies by chlorophyll fluorescence. This type of analysis offers information on energy transfer in the photosynthetic apparatus and the related photosynthetic processes, mainly about the activity of photosystem II (PSII). PSII is a membrane protein complex whose active centers exist as dimers in the thylakoid membranes of grana stacks. It is known that PSII has the function to catalyze light-induced water oxidation in oxygenic photosynthesis and in this way light energy is converted into biologically useful chemical energy ( Khorobrykh, 2019 ; Rantala et al., 2021 ). Shin et al. (2020) used chlorophyll fluorescence to assess the PSII activity in the leaves of cultivars ‘Dafnis’, ‘Maxifort’, ‘BKO’ and ‘B-blocking’ irrigated with saline water. At 400 mM (the maximum concentration of NaCl in saline water) the chlorophyll fluorescence decrease ratio (Rfd) was the parameter whose levels were most negatively affected, followed by the maximum quantum yield of PSII photochemistry (Fv/Fm). The chlorophyll fluorescence parameters, such as the coefficient of photochemical quenching of variable fluorescence based on the puddle model of PSII (qP) and coefficient of nonphotochemical quenching of variable fluorescence (qN) showed moderate negativechanges due to the salt level increase in irrigation water, whereas the quantum yield of nonregulated energy dissipation in PSII Y(NPQ) showed a significant increment at the higher salt concentration compared to control. Gong et al. (2013) reported that the values of Fv/Fm parameter and the actual quantum efficiency of photosynthetic system II (ФPSII) in cv. ‘Jinpeng No. 1’ decreased with increasing levels of salt in the hydroponic media. For the non-photochemical quenching (NPQ) parameter was noticed that an increase in salt level led to an increase in its value, the highest being recorded at 100 mM. According to Zhao et al. (2019) the qP parameter measures the openness of PSII centers and reflects the conversion efficiency of the captured light quantum into chemical energy, while qN assesses the rate constant for heat loss from PSII. Fv/Fm parameters give information about the maximum light energy conversion efficiency of PSII after adaptation to darkness and NPQ reflects the level of excess energy dissipation as heat. Using the ФPSII parameter of chlorophyll fluorescence is assessed the actual photochemical efficiency when the PSII reaction center is partly shut down under light. Thereby, as Tsai et al. (2019) and Zhao et al. (2019) stated, the changes observed in the chlorophyll fluorescence parameters under salt stress are the results of the membrane system stability disturbance (especially the damage of thylakoid membrane), the aggravation of the PSII reaction center and disturbances in PSII performance, which diminished the photosynthesis.

More results on the changes induced by saline stress on photosynthetic rate, transpiration, stomatal conductance and chlorophyll content in tomato leaves have been included in Table 2 .

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Table 2 Photosynthetic rate, transpiration, stomatal conductance and chlorophyll content in tomato leaves under salinity stress.

Frequently, salinity increase can lead to a reduction in the essential minerals content such as calcium, potassium or magnesium and, consequently, to a nutritional imbalance. Calcium is one of the structural components of cell walls and membranes and serves as a second messenger in a variety of processes ( Thor, 2019 ; Bang et al., 2021 ). By transduction, integration and incoming signals multiplication, the calcium links the environmental stimuli with the physiological responses of plants ( Bang et al., 2021 ). Potassium ensures optimal plant growth, acts as an activator of dozens of important enzymes and enhances plant yield. For example, potassium plays an important role in protein synthesis, sugar transport, N (nitrogen) and C (carbon) metabolism, photosynthesis, cell osmotic pressure regulation and maintaining the balance between cations and anions in the cytoplasm ( Xu et al., 2020 ). Magnesium in plant tissue is the central element of the tetrapyrrole ring of the chlorophyll molecule and, therefore, its deficiency leads to a chlorophyll synthesis decrease and to the impairment of normal plant growth and development. Magnesium also acts as an activator or cofactor of enzymes involved in carbohydrate metabolism ( Guo et al., 2015 ; Bang et al., 2021 ). Therefore, a deficiency of these minerals in the plant tissues can cause negative effects on growth and development ( Bang et al., 2021 ).

In tomato plants, the essential mineral uptake in soil or hydroponic cultivation can be significantly affected by saline stress ( Sánchez et al., 2012 ; Nebauer et al., 2013 ; Assimakopoulou et al., 2015 ; Javeed et al., 2021 ). The results of studies presented in Table 3 show that high salt levels in the growing culture can cause a lower uptake of calcium, potassium and sometimes of magnesium ions ( Sánchez et al., 2012 ; Nebauer et al., 2013 ; Assimakopoulou et al., 2015 ; Parvin et al., 2016 ). Nebauer et al. (2013) reported in their study that regardless of the salt applied (NaCl, Na 2 SO 4 , MgCl 2 or MgSO 4 ), a level of 100 mM in soil reduced the Ca uptake by 48.75 to 71.26% in tomato cultivar Marmande RAF and by 12.28 to 38.60% in cultivar Daniela. Moreover, the amount of K in plants was lower by up to 68.05% at 100 mM MgSO 4 in cv. Marmande RAF leaves and by up to 42.67% at 100 mM MgCl 2 or 100 mM MgSO 4 in cv. Daniela leaves. Decreases in the content of aforementioned minerals were also reported by Manan et al. (2016) ; Gharbi et al. (2017a) ; Rodríguez-Ortega et al. (2019) or Borbély et al. (2020) . Therefore, it can be stated that salinity limits the assimilation of essential minerals in the tomato plant tissue and the physiological processes are adversely affected by these deficiencies. However, there are studies that showed that potassium, calcium and magnesium content in tomato leaves increased under salt stress ( Costan et al., 2020 ; Javeed et al., 2021 ). For example, the content of calcium increased from 6.66 mg g -1 to 11.03 mg g -1 and of potassium from 36.68 mg g -1 to 71.51 mg g -1 in the fresh leaves of cultivar Rio Grande, grown in hydroponics with nutrients solution and seawater (5%, 10 % and 20%), and an EC of the growing media between 0.41 and 8.14 dS m -1 ( Javeed et al., 2021 ). The high content of calcium and magnesium ions in tomato leaves under saline stress could be due to the higher uptake affinity for these ions rather than for Na + or Cl - ( Al-Ghumaiz et al., 2017 ). According to Al-Ghumaiz et al. (2017) , the tolerant plants under salinity stress can exclude the Na + ions from their shoots or blades while maintaining high levels of K + .

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Table 3 Mineral accumulation in tomato leaves under salinity stress.

Salinity effects on the biochemical parameters of tomato plants and fruits

Besides affecting the morphological and physiological status, saline stress can also influence the biochemical reactions of plants. Many studies have shown that high salt concentrations cause biochemical imbalances resulting in low plant productivity ( Kusvuran et al., 2016 ). Tomato plants, though considered moderately sensitive to saline stress, show many changes at the biochemical level such as increases or decreases in the accumulation of hormones, reactive oxygen species (ROS) or antioxidants. These changes have been mainly recorded when NaCl has been used as a salt stressor, in concentrations varying between 25 and 600 mM ( Table 4 ).

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Table 4 Salinity impact on the biochemical parameters in tomato plants and fruits.

In general, the plants respond to the salinity stress in two phases: in the first, which lasts for days or weeks, the effect of osmotic stress is predominant; in the second, of weeks to months duration, the ionic toxicity effect of leaf salt accumulation affects plant growth. In the first phase, the phytohormones play an important role in regulating plant growth. For instance, abscisic acid (ABA) under saline conditions can accumulate in tomato leaves and/or roots, as a response to the low soil water potential, causing stomatal closure, thus affecting the photosynthesis or enhancing the root growth ( Babu et al., 2012 ; Lovelli et al., 2012 ; Gharbi et al., 2017a ; de la Torre-González et al., 2017b ). Indole acetic acid (IAA) is another hormone that is usually highly synthesized under saline stress, alleviating the negative effects of osmotic and oxidative stress, being involved in all aspects of the plant, from germination to vegetative growth and flowering. The accumulation of IAA was recorded in tomato leaves exposed to salt concentrations varying from 25 mM NaCl to 100 mM NaCl ( Babu et al., 2012 ; de la Torre-González et al., 2017b ). However, decreases or no change in the total auxins were found by Gharbi et al. (2017a) , in S. chilense and cultivar Ailsa Craig at 125 mM NaCl or by de la Torre-González et al. (2017b) in cultivar Marmande at 100 mM NaCl. Other phytohormones studied in relation to saline stress in tomato are salicylic acid, polyamines (Put, Spd and Spm), ethylene, benzoic acid, total jasmonates, total gibberellins, cytokinins or aminocyclopropane-1-carboxylic acid (ACC, the ethylene precursor), whose content has shown very changeable responses to salinity. The content of phytohormones has been found highly dependent on the cultivar, salt concentration or plant part. For instance, the bioactive gibberellin GA4 accumulated in the cultivar Grand Brix, but not in Marmande; the total jasmonates increased in the leaves of cultivar Ailsa Craig, but remained unchanged in the roots ( Table 4 ) ( de la Torre-González et al., 2017b ; Gharbi et al., 2017b , 2017a ).

Under salinity stress, but not only, plants increased the content of ROS, causing oxidative damages. Regarding tomato, the studies have mainly focused on the activity of malondialdehyde (MDA, a lipid peroxidation marker), carbonyl groups, H 2 O 2 , O 2 − or lipoxygenase (LOX). Their accumulation can lead to the inhibition of plant growth and development, and plant death. Increases in ROS content in tomato plants were reported at low levels of salinity (25 mM NaCl), in cultivar Ciettaicale, for hydrogen peroxide, but also at high levels of salinity (450 mM NaCl) in the variety cerasiforme for MDA ( Al Hassan et al., 2015 ; Moles et al., 2019 ). The duration of exposure to salinity is an important factor in ROS accumulation, as suggested by Al Hassan et al. (2015) , who recorded a significant increase in MDA content 33 days after starting the treatment but not after 25 days. Cultivar also plays a key role: the exposure of tomato cultivar Micro-Tom to NaCl (120 mM) or of Marmande and Grand Brix (100 mM NaCl) led to an increase in MDA and carbonyl groups or H 2 O 2 and LOX contents, while at 40, 80 and 160 mM NaCl the MDA content in S. chilense Dun. and variety cerasiforme was not affected ( Manai et al., 2014 ; Martínez et al., 2014 ; de la Torre-González et al., 2017b ).

In order to prevent the negative effects of ROS, plants produce enzymatic and non-enzymatic compounds such as: ascorbic acid, phenols, ascorbate peroxidase (APX), superoxide dismutase (SOD), glutathione reductase (GR), catalase (CAT), peroxidase (POD), glutathione peroxidase (GPx), plasma glutathione peroxidase (GSHPx) etc., which play a key role in cell protection against the oxidative stress ( Kusvuran et al., 2016 ). In tomato subjected to saline stress, the antioxidant production can vary depending on cultivar, salt concentration, plant age or part. For instance, in a study done on cerasiforme variety subjected to 40, 80 and 160 mM NaCl, the enzymatic activity of SOD increased at 40 and 80 mM NaCl, then decreased at 160 mM, while the APX activity decreased regardless of the salt concentration ( Martinez et al., 2012 ). In another study, where tomato cultivar Micro-Tom was subjected to 120 mM NaCl, the activity/content of ascorbate, glutathione (GSH), NADP-isocitrate dehydrogenase (NADP-ICDH), glucose-6-phosphate dehydrogenase (G6PDH), 6-phosphogluconate dehydrogenase (6PGDH), S-nitrosoglutathione (GSNO) reductase and CAT decreased, while the activity of GR and GPx increased, suggesting a negative impact of the salinity stress on the redox status and NO metabolism ( Manai et al., 2014 ). Interesting findings were made by Srineing et al. (2015) , in a study in vitro on the cultivar Puangphaka treated with NaCl at concentrations ranging between 5 – 100 mM. The authors analyzed the activity of SOD, CAT and GPx (roots and stem) at different time intervals: 7, 14, 21 days after incubation. The results showed differences in enzyme activity depending on plant age and part (roots or stems) ( Table 4 ). The influence of the salt and the exposure time on total carotenoids, total phenolics, total flavonoids and TSS was also analyzed by Al Hassan et al. (2015) in cerasiforme variety exposed to 150, 300 and 450 mM NaCl. The results showed that regardless of the time of treatment (25 or 33 days) the content of total carotenoids significantly decreased at all the concentrations, except for 150 and 300 mM, 25 days after treatment, while the content of the total phenolics and flavonoids significantly increased at all the salt concentrations, except for 150 mM, 25 days after treatment, in the case of phenolics. In another study, where the tomato plants of cultivar Microtom were exposed shorter to NaCl stress (14 days) the phenols increased to 150 mM NaCl ( Bacha et al., 2017 ). Changes in the antioxidant activity were also reported by Martínez et al. (2014) ; Manan et al. (2016) and de la Torre-González et al. (2017b) , included in Table 4 .

Salinity stress is known to produce a C shortage in plants, stimulating the synthesis of C-rich compounds such as trehalose, mannitol, sorbitol or proline, involved in the osmotic adjustment mechanism to stressful conditions. Moreover, the N status is affected because of the influence on NO 3 − and NO 4 + uptake.

Hossain et al. (2012) and Manai et al. (2014) reported that the activity of enzymes involved in the N absorption was affected by saline stress: a decrease was recorded for nitrate and nitrite reductase or nitric oxide (NO), suggesting a negative impact on the NO metabolism under salinity stress, while an increase was recorded for protease, glutamate synthase and Fd-dependent glutamate synthase, NADP-dependent isocitrate dehydrogenase, and glutamate dehydrogenase. No change was observed for NADH-dependent glutamate synthase. Most of the studies carried out on different tomato cultivars, varieties or genotypes (e.g. BINATomato-5, PKM1, Cerasiforme, Rio grande, Savera, Ciettaicale or San Marzano) reported increases in the proline, glycine betaine, serine, alanine, or total soluble sugars contents under different NaCl concentrations, as a result of osmotic adjustments ( Babu et al., 2012 ; Hossain et al., 2012 ; Al Hassan et al., 2015 ; Manan et al., 2016 ; Moles et al., 2016 ). Increases in the proline content in the roots, stems and leaves of tomato plants, but not of the total soluble sugars, were also recorded in the case of combined salt stress, consisting of NaCl:Na 2 SO 4 in a molar ratio of 9:1 ( Wang et al., 2015 ). By contrast, a decrease in the proline content was reported by Abdel-Farid et al. (2020) , in a pot experiment, where tomato plants were treated with 25, 50, 100, 200 mM NaCl. The decrease was explained by taking into consideration the replacement of the proline by another osmoprotectant under saline conditions.

The salinity stress can also affect the protein content of plants. A study performed on two tomato cultivars (Castle rock and Edkawi) with different tolerance to salinity showed an accumulation of proteins (the large chloroplast subunit (RbcL), structural maintenance of chromosomes (SMC) protein, a protein from the plasma membrane, and transcription factors) at 50 mM NaCl in both cultivars, a gradual decrease at higher salt concentration for Castle rock and an approximately constant accumulation for Edkawi at 100, 150, 200 mM NaCl, followed by a decrease to 300 mM NaCl. According to the authors, the accumulation of RbcL at 50 mM NaCl in the cultivar Castle rock might be the result of Rubisco degradation under saline stress, as this cultivar is more sensitive to salinity. The better tolerance to salt stress of cultivar Edkawi is demonstrated by better retention of Rubisco content, chromosome segregation and up-regulation of ion pump proteins ( Khalifa, 2012 ). In another study carried out on the cultivar BINATomato-5 the soluble protein content decreased by 25.64% at 60 mM NaCl and by 42.75% at 120 mM NaCl ( Hossain et al., 2012 ). A decrease in protein content was also observed by Manaa et al. (2013a) in the leaves of two tomato cultivars (Roma – salt tolerant, SuperMarmande – salt sensitive), at 100 and 200 mM NaCl. The same author conducted leaf proteomic analysis, identifying 26 proteins involved in energy and carbon metabolism, photosynthesis, ROS scavenging and detoxification, stress defense and heat shock proteins, amino acid metabolism and electron transport. The majority of the proteins identified were upregulated as a consequence of saline stress. Variations in protein abundance were also reported in the fruits of two tomato cultivars (Cervil and Levovil), which were correlated to the salt treatments and the fruit ripening stage. Most of the proteins identified were associated with carbon and energy metabolism, salt stress, oxidative stress, and the ripening process ( Manaa et al., 2013b ). In general, the content of soluble proteins represents an indicator of plant physiological status under stress, having an important role in osmotic adjustments, and providing storage for different forms of nitrogen. Depending on the cultivar, the soluble proteins can decrease as a result of protein synthesis inhibition and/or protein hydrolysis or can increase through the production of new stress-related proteins ( Ahmad et al., 2016 ).

Salinity stress can also have no impact on the protein content, as recorded by Martínez et al. (2014) , in a study done on S. chilense Dun. and variety cerasiforme at 40, 80, or 160 mM NaCl.

Salinity can also affect the carboxylate metabolism and organic acid production, depending on the cultivar as demonstrated by ( de la Torre-González et al., 2017a ) ( Table 4 ). High activity of the enzymes involved in the carboxylate metabolism enhances tomato resistance to salinity due to the activation of osmotic adjustments mechanism of response which helps the plant to adapt to stressful conditions. Also, high organic acid concentrations are necessary for enhancing the plant’s tolerance to salinity, taking into account their important role in different biochemical pathways, such as energy production or amino-acid biosynthesis. In addition, Moles et al. (2019) showed that NaCl can influence the activity of the cell wall enzymes (endo-β-mannanase, β-mannosidase, α-galactosidase) involved in seed germination. Under 25 mM NaCl, the concentration of endo-β-mannanase and β-mannosidase increased in cultivar Ciettaicale, and decreased in cultivar San Marzano affecting the seed germination. Reyes-Pérez et al. (2019) stated that acid and alkali phosphatase, trypsin, lipase, β-galactosidase, and esterase can be used as biomarkers for NaCl-stress tolerance in tomato.

Salinity effects on tomato gene expression

In general, salinity stress, like other abiotic stresses, determines changes in the gene expression of plants. The knowledge of the gene expression as a result of salt stress is still limited, but mostly refers to changes in transcription factors ( Devkar et al., 2020 ).

Tomato research regarding the effect of salinity on gene expression has been carried out on different cultivars and focused mostly on the effect of NaCl applied at the concentration range between 50 and 500 mM ( Table 5 ). The results suggested changes in the expressions of genes involved in cell wall construction, biosynthesis of volatiles and secondary metabolites, protein synthesis, transport activity, etc. for the plants subjected to salinity stress.

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Table 5 Salinity stress-related genes in tomato plants.

In a study with the cultivar Micro-Tom subjected to NaCl at 100, 200 and 400 mM, the genes responsible for the phenylpropanoid pathway ( 4CL3 = 4-coumarate-CoA ligase, PAL6 = phenylalanine ammonia lyase, CHI1 and CHI2 = chalcone isomerase, HQT = hydroxycinnamoyl-CoA quinate transferase), xyloglucan endo-transglucosylase or hydrolase ( XTH4 ,  XTH20 ,  XTH16 ) activities, or enzymatic response to reactive oxygen species ( ROS , SOD genes), were up-regulated in the top younger leaflets as compared to the older ones situated at the bottom of tomato plants, indicating an increase in the lignification process and flavonoid synthesis, a strengthening in the mechanical cell wall properties and an intensification in SOD production, an enzyme involved in the response to ROS as a result of the salinity stress. Furthermore, in the top leaflets of stressed plants, the expression of expansins ( EXPA4 , EXPA5 , EXPA18 ), genes involved in cell wall reshaping, fasciclin-like arabinogalactan proteins ( FLA 2, FLA10, FLA11 ) involved in keeping the plasma membrane and cell wall in close contact, and volatile organic compounds’ synthesis ( TPS ,  FPS ) were down-regulated, suggesting an increase in the salt sensitivity, as plant growth was stopped, as well as the production of terpene synthase ( TPS ) or farnesyl pyrophosphate synthase ( FPS ). Changes in the gene expression were also recorded in the bottom leaflets, with the LEA and LOX genes up-regulated, indicating an accumulation in late embryogenesis abundant (LEA) proteins responsible for membrane maintenance and ion-sequestering properties, as well as in lipoxygenases, markers for cell membrane damage.

Other up-regulated genes in the salt-stressed tomato plants were those coding for heat shock transcription factor  HSF30 ( Hoffmann et al., 2021 ). In another experiment, in which tomato cultivar Yanfen 210 was treated with seawater at different concentrations (10%, 20% and 30%), a significant differential change was recorded in the expression of 509 genes, 40.67% of which were up-regulated, while 59.33% down-regulated. The highlighted genes were responsible for biological processes (i.e. metabolic process, cellular process or single organism process), cellular components (i.e. cell, cell part, membrane, organelle, etc.) or molecular functions (i.e. catalytic activity, binding, transporter activity, etc.). Notably, the SlGA20OX1 gene expression was down-regulated, thus affecting the production of gibberellin and plant growth. Down-regulations were also observed for SlMYB13 , part of MYB family transcription factors involved in biological and developmental processes, cell morphology, biological stress response, primary and secondary metabolism adjustment, SlCI-2 gene involved in the inhibition of proteinase activity or SlHYD gene responsible for the activity of cell membrane. On the other hand, over-expressions were observed for SlPCC27-04 gene coding for plant desiccation-related proteins, SlMYB48 gene responsible for ABA signaling, SlAPRR5 gene known to control the time of the flowering process, the circadian rhythms or the photomorphogenesis, or SlMFS  gene involved in the membrane activity ( Mu et al., 2021 ). Zhang et al. (2018) , investigating the effect of NaCl on the volatile compound emission of tomato plants, found the expression of 18 genes down-regulated, thus affecting the biosynthesis of isopentenyl diphosphate isomerase, geranyl pyrophosphate synthase, sesquiterpene synthase, β-phellandrene synthase, terpene synthase 1, 28, 38 or farnesyl pyrophosphate synthase 1. Out of a total 7210 differentially expressed after NaCl exposure, of which 1208 were over-expressed and 6200 were down-expressed, other 3454 genes were related to plant-pathogen interaction, RNA-transport or hormone signal transduction. Changes in the expression of hormone-related genes were also recorded by Pye et al. (2018) in the roots of the cultivar New Yorker. The treatment with NaCl and CaCl 2 led to an increased expression of two ABA-related genes: NCED and  TAS14 .

An interesting finding was made by Coyne et al. (2019) , who observed a correlation between the expression of some genes and the circadian rhythms. The gene coding for sodium or hydrogen antiporter and an enzyme for proline synthesis, SlSOS2 and P5CS , were expressed only in the morning, while SlDREB2 encoding a transcription factor responsible for the response of tomatoes to salinity was expressed only in the evening. Due to this behavior, tomato, but also other species, might be able to keep the balance of the endogenous systems to circadian rhythms. Almeida et al. (2014b) also reported an overexpression of P5CS gene which led to an accumulation of proline and Na + in the leaves of five weeks old tomato plants, but not in the roots. The same authors observed a higher expression of NHX1 and NHX3 genes correlated with a lower Na + accumulation in leaves, and a higher Na + accumulation in roots; the expression of HKT1;2 gene in the roots was positively correlated with the amount of Na + in leaves and stems, but not in the roots, where other genes were responsible for the accumulation of Na + ( HKT1;1 ). Changes in the expression of HKT1;2  gene due to salinity stress was also recorded in the cultivar Arbasson where an increase in the gene expression in stems and roots was recorded along with increased salinity stress. In leaves, the accumulation of Na + was correlated with a low expression of HKT1;2  genes ( Almeida et al., 2014a ). The role of HKT1;1  and  HKT1;2 in the ion homeostasis in tomato leaves and stems was also confirmed by Asins et al. (2013) . Jaime-Pérez et al. (2017) demonstrated in transgenic tomato plants the importance of HKT1 ; 2 gene in Na +  homeostasis and salinity tolerance. The same genes ( HKT1;1  and  HKT1;2 ) along with LeNHX1 ,  LeNHX3 ,  LeNHX4 , SIWRKY8, SIWRKY31 ,  SIWRKY 39 ( WRKY  gene family) and ERF transcription factors were reported to be highly expressed in a study carried out by Gharsallah et al. (2016) on three tomato genotypes.

The salinity stress can also affect the expression of genes related to nitrogen uptake and transport. In this respect, Abouelsaad et al. (2016) demonstrated a decrease in the expression of mRNA of nitrate transporters NRT1.1  and  NRT1.2 in both cultivars Manitoba and S. pennellii . The same authors observed a higher expression of remarkable affinity ammonium transporters ( AMT1.1  and  AMT1.2 ) in Manitoba and a down-regulation of the Gs1 gene (cytosolic glutamine synthetase) in S. pennellii .

Other genes whose expression was changed by salt stress are: SlERF5 gene, part of ERF family gene, which has an important role in the ethylene and abscisic acid signaling pathway ( Pan et al., 2012 ); SlGSTU23 ,  SlGSTU26, SlGSTL3, SlGSTT2, SlDHAR5, SlGSTZ2 involved in primary metabolism, regulation of plant growth and development, anthocyanin’s absorption, detoxification of toxic compounds (xenobiotic, lipid peroxides), etc. ( Csiszár et al., 2014 ); LeHAK5 gene whose expression was significantly decreased when the Na + concentration was increased ( Bacha et al., 2015 ); SlARF1 , SlARF4 , SlARF8A , SlARF19 and SlARF24 which were upregulated in response to salinity stress ( Bouzroud et al., 2018 ).

The gene RBCL (large subunit RUBISCO) whose level of expression was not different as a result of salinity stress, in the presence or absence of ABA synthesis, but whose protein it encodes, showed a significant decrease ( Poór et al., 2019 ).

Salinity impact on yield and fruit quality

High levels of sodium chloride in soil or in nutritional medium highly affect plant physiological and biochemical processes as well as gene expression, with effects on plant morphology, but also on yield and fruit quality. Most of the research carried out with tomato suggested a positive or no impact of salinity on fruit quality ( Table 6 ). Therefore, increases are reported in the lycopene content ( De Pascale et al., 2012 ; Islam et al., 2018 ; Sellitto et al., 2019 ), sugar ( De Pascale et al., 2012 ; Islam et al., 2018 ; Marsic et al., 2018 ; Botella et al., 2021 ), total soluble solids (TSS), titratable acidity (TA), organic acids (OA), fruit firmness ( Cantore et al., 2012 ; De Pascale et al., 2012 ; Martínez et al., 2012 ; Liu et al., 2014 ; Zhai et al., 2015 ; Pengfei et al., 2017 ; Islam et al., 2018 ; Rodríguez-Ortega et al., 2019 ; Maeda et al., 2020 ; Botella et al., 2021 ) or cuticle thickness ( Agius et al., 2022 ). According to Agius et al. (2022) a salinity level of up to 5 dS m −1 in nutrient solutions may enhance the fruit quality. In a study conducted by Cantore et al. (2012) on two tomato cultivars, salinity increased the content of TSS and had no significant effect on the ascorbic acid content or the TA. Martínez et al. (2012) showed no change in the TSS and TA content at 40 or 80 mM NaCl. At a salinity level of 6.8 dS m -1 in soil, the TSS and TA contents in fruits of Buran F 1 grafted on Maxifort are higher compared to the values determined in fruits grown in soil with the EC of 1.7 dS m -1 ( Pašalić et al., 2016 ). Zhang et al. (2016) reported that the salt enrichment in nutrient solution also leads to an increase in the acidity of the tomato fruit. Islam et al. (2018) ; Costan et al. (2020) and De Pascale et al. (2012) found in their studies that the total soluble solids (Brix index) and citric acid content increased in tomato fruits with salinity increase. In the fruits of tomato cultivar Unicorn the total soluble solids (Brix index) and citric acid content increased by 22% and 20% per dS m -1 ( Islam et al., 2018 ). Improvement of fruit quality as a result of salinity was also reported by: Ahmed et al. (2017) ; Pengfei et al. (2017) in cultivar Pepe; Rodríguez-Ortega et al. (2019) in tomato cultivar Optima; Maeda et al. (2020) in the two tomato cultivars CF Momotaro York and Endeavour. The main factors influencing the fruit quality under salinity stress are harvest day, salinity distribution in the soil or the growth stage ( Iglesias et al., 2015 ; Chen et al., 2016 ; Zhang et al., 2017 ). In a study conducted with 4 tomato varieties (Raf, Delizia, Conquista, Tigre) subjected to salinity stress, the content of TSS was significantly decreased when the fruits were harvested 136 days after transplant for cultivar Raf and 90 and 104 days for Delizia; a significant increase of TSS was recorded for Conquista 150 days after transplant and Tigre 136 days ( Iglesias et al., 2015 ). By testing the effect of the uneven vertical distribution of soil salinity on the tomato quality of cultivar Yazhoufenwang, Chen et al. (2016) showed that the content of TSS, OA and vitamin C increased with the soil salt concentration in the upper layer. Zhang et al. (2017) , demonstrated that the salinity stress applied from flowering until the fruiting stage improves the TSS content. However, negative effects of high salt levels can be found in the mineral content of tomato fruits. Studies conducted by De Pascale et al. (2012) ; Hernández-Hernández et al. (2018) ; Islam et al. (2018) ; Costan et al. (2020) showed that under salinity stress, the mineral content in tomato fruits ( Table 7 ), especially of calcium and potassium, can decrease.

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Table 6 Salinity impact on yield and citric acid, lycopene, soluble solids contents in tomato fruits.

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Table 7 Salinity impact on mineral content in tomato fruit.

Regarding tomato yield under saline stress, the Division of Agriculture and Natural Resources of University of California specifies that a soil salinity of 7.6 dS m -1 may reduce both tomato plant emergence and crop yield by 50% ( Division of Agriculture and Natural Resources, 2022 ), but these effects are closely related to the tomato cultivar. The study performed by De Pascale et al. (2012) showed that at 4.4 dS m -1 the mean fruit weight, the number of fruits per plant and the total yield of tomato decreased compared to the control (0.5 dS m -1 ) by 19.68%, 20.74%, and 23.07%, respectively. According to Islam et al. (2018) an increase in soil salinity from 2.5 at 7.5 dS m -1 causes a 14.81% reduction in the mean fruit weight of the cultivar Unicorn. In addition, Liu et al. (2014) reported that the yield of three cherry tomato cultivars grown inpeat moss, perlite and sand mix (2:1:1) was affected differently by the same levels of salinity. At 150 mM NaCl the mean fruit weight of Tainan ASVEG No. 19, Hualien ASVEG No. 21 and Taiwan Seed ASVEG No. 22 was reduced by 26.03%, 47.13%, and 55.56% respectively, compared to the control, and the total yield decreased from 243.9, 78.7 and 155.5 g/plant to 48.8, 6.9, and 19.3 g/plant, respectively. Costan et al. (2020) reported that, although the number of fruits per plant increased with the salinity rises in the hydroponic system (from 0 at 50 mM), the yield of the tomato cultivar Belladonna was reduced by more than 36%. Noshadi et al. (2013) found the highest yield (47.15 t·ha -1 ) was recorded when the irrigation water EC was of 2 dS m -1 . At 0.6 dS m -1 , 38.02 t·ha -1 were harvested and at 4 dS m -1 about 31.57 t·ha -1 , whereas the lowest yield was at 8 dS m -1 EC (21.20 t·ha -1 ). Therefore, according to the results of the latter study, a slightly saline soil or hydroponic cultivation can enhance tomato yield.

Recommendations for alleviating the effects of salinity on tomato

The negative effects of salinity on tomato plants can be alleviated by using different strategies like plant priming or genetic modification.

Plant priming represents a promising method to reduce the time required for a plant exposed to abiotic stress to respond efficiently to the stressor and, thereby, to increase the tolerance to stress conditions ( Aranega-Bou et al., 2014 ). Effective priming agents against salt stress in tomato, which have been studied over years are elements (Fe, Si, K, N), plant growth regulators (ACC, IAA, SA, melatonin), reactive species (S-nitrosoglutathione, sodium hydrosulfide, sodium nitroprusside), vitamins (ascorbic acid - AsA), aminoacids, natural extracts (seaweed), polymers (chitosan), osmoprotectants (glycine betaine, proline), polyamines (spermidine) or plant growth promoting microorganisms (bacteria, fungi or arbuscular mycorrhizal fungi) ( Choudhary et al., 2022 ; Gedeon et al., 2022 ; Zulfiqar et al., 2022 ). The results showed in most of the cases an enhancement of the tolerance of plants to various concentrations of salt, by decreasing the osmotic stress, enhancing the activity of the antioxidant system, increasing the growth and yield or by improving the fruit quality. For instance, the application of Fe increased the ascorbic acid content in the fruits of tomato along with the increment in salinity level; the Si addition stimulated an early accumulation of TSS in the fruits of tomatoes, but did not influence the quality of the taste; in another study, the presence of Si decreased the SOD activity, suggesting a reduction in ROS production; also, the treatment with Si increased the β-carotene and vitamin C content; the addition of 5 mM K + regulated the ascorbate–glutathione cycle, the activity of antioxidant enzymes, the carbohydrate metabolism and increased the proline content; nitrogen applied at different concentrations (25, 75, 150 kg N ha −1 ) had a positive impact on the proline content and on the activity of P5CS enzyme, also affected the activity of various enzymes: proline dehydrogenase, nitrate reductase, nitrite reductase, glutamine synthetase and glutamate synthase, glutamate dehydrogenase under NaCl stress ( Tantawy et al., 2013 ; Iglesias et al., 2015 ; Muneer and Jeong, 2015 ; Singh et al., 2016 ; Costan et al., 2020 ; Khan et al., 2021 ). The application of plant growth regulators such as ACC decreased the osmotic stress in ‘Ailsa Craig’ tomato cultivar; spraying the tomato plants with IAA (100 and 200 ppm) increased the TSS content of fruit juice and the chlorophyll content of the leaves; the exogenous application of salicylic acid decreased the ethylene synthesis and increased the polyamine endogenous concentration; in another study, salicylic acid applied foliar increased the TSS and the vitamin C content; the treatment of the seeds with salicylic acid (1 mM) and H 2 O 2 (50 mM) increased the TSS, proteins, POD, CAT, SOD and MDA content; the treatment with 20 and 50 µM melatonin improved the activity of the antioxidant system, the proline and carbohydrate metabolism, also the ascorbate/reduced glutathione cycle in ‘Five Start’ tomato cultivar; in another studies, melatonin improved the root architecture, reduced the production of reactive oxygen species, enhanced the activity of enzymatic antioxidants and the photosynthesis ( Gharbi et al., 2016 ; Gaba et al., 2018 ; Siddiqui et al., 2019 ; Alam et al., 2020 ; Altaf et al., 2020 , 2021 ; 2022b ; Borbély et al., 2020 ; Naeem et al., 2020 ; Hu et al., 2021 ; Ali et al., 2021b ). The application of S-nitrosoglutathione and NaHS promoted the accumulation of NO and H 2 S, alleviating the deleterious effects of oxidative stress; the use of sodium nitroprusside increased the content of non-enzymatic and enzymatic antioxidants, up-regulated the NO level in leaves, enhanced the activity of Calvin cycle, overcame the stomatal limitations and protected the photosystem II from damages ( da-Silva et al., 2018 ; Taheri et al., 2020 ; Li et al., 2022 ). Alves et al. (2021) by soaking the tomato ‘Micro-Tom’ seeds for one hour in 100 mM AsA, observed that the tolerance of plants to salt stress was enhanced by modulating the antioxidant mechanisms. The content of CAT, APX, POX, GPX, GR, GSH, SOD, chlorophyll, and carotenoids in the leaves of primed plants was higher than in the control. Chen et al. (2021) by spraying 0.5 mmol/L AsA solution on the leaves of cv. ‘Ligeer87-5’ exposed at 100 mmol/L NaCl reported an attenuation of the photoinhibition and oxidative stress damage in chloroplasts, dissipation of excitation energy in PSII antennae, stimulation of chlorophyll synthesis and reduction of damaging effects on photosynthesis in tomato leaves. The foliar application of an aminoacid (Botamisol as free L-amino acids) at different concentrations (0, 2, 4 g·L -1 ) increased the proline level in the leaves of tomato plants exposed to salinity (8 and 10 dS·m -1 ) ( Jannesari et al., 2016 ). The application of a seaweed extract (100 mL of P. gymnospora 0.2% w/v) improved the growth, yield and quality of ‘Rio Fuego’ tomato cultivar ( Hernández-Herrera et al., 2022 ). The use of chitosan solution at different concentrations (0.03% and 0.05% or 50, 100 and 150 mg/L) for spraying the tomato leaves, enhanced the salt tolerance of tomato at 100 mM NaCl applied as a root drench, promoted the growth and development of plants and increased the chlorophyll contents ( Ullah et al., 2020 ; Özkurt and Bektaş, 2022 ). The exogenous application of spermidine (Spd) on tomato cv. ‘Ailsa Craig’ seedlings grown under salt stress resulted in higher photosynthesis and biomass, better ionic and osmotic homeostasis, and enhanced ROS scavenging capacity ( Raziq et al., 2022 ). Siddiqui et al. (2017) found that the chlorophyll a and b contents, proline, activity of CAT, SOD, POD, GR and APX were increased and H 2 O 2 and MDA production in tomato var. Five Star was reduced as a result of exogenous spermidine application on seedlings. The foliar application of 10 and 20 mg/L proline during the flowering stage of cultivars ‘Rio Grande’ and ‘Heinz-227’ led to an increase in the dry mass of leaves, stems and roots, improved various chlorophyll fluorescence parameters, increased the potassium and phosphorous content and reduced the accumulation of Na + in different organs, compared with control ( Kahlaoui et al., 2014 ). The effects of the exogenous application of glycine betaine (GB) on different tomato cultivars have been assessed in a few studies and both positive and negative correlations were found between GB exogenous application and salt tolerance in tomato. Chen et al. (2009) found that the exogenous use of 5 mM GB in half-strength Hoagland could alleviate the salt stress effects in tomato cv. ‘F144’ and cv. ‘Patio’ through changing the expression abundance of some proteins. Sajyan et al. (2019) irrigated the tomato ‘Sila’ plants with saline water (with EC between 2 and 10 dS m -1 ) and exogenous GB in various doses (4.5, 6 and 7.5 g/L) and observed a positive effects on leaf number, stem diameter, number of flowers, number of fruits, no evident effects on the number of clusters, fruit set, the weight of individual fruit, yield and fruit diameter were observed and a reduction in the fruit ripening process at 7.5 g/L GB.

Plant growth-promoting rhizosphere bacteria (PGPB) can alleviate the effects induced by salt stress by production of phytohormone (e.g. auxin, cytokinin, and abscisic acid), ACC-deaminase, ammonia, IAA, extracellular polymeric substance (EPS), induction of synthesis of plant osmolytes and antioxidant activity, increasing the essential nutrient uptake or/and by reducing ethylene production ( Kumar et al., 2020 ). Sphingobacterium BHU-AV3 ( Vaishnav et al., 2020 ), Bacillus megaterium strain A12 ( Akram et al., 2019 ), Enterobacter 64S1 and Pseudomonas 42P4 ( Pérez-Rodriguez et al., 2022 ), Bacillus aryabhattai H19-1 and Bacillus mesonae H20-5 ( Yoo et al., 2019 ) are some of the PGPB that have been proved to increase tomato tolerance to salt stress. For example, inoculation of tomato cv. ‘Kashi amrit’ plants with Sphingobacterium BHU-AV3 exhibited a less senescence in plants exposed to 200 mM NaCl, being determined that the proline content was increased, ion balance was maintained and the ROS was lower compared to the non-inoculated plants. In BHU-AV3-inoculated plant leaves superoxide content, cell death and lipid peroxidation were significantly reduced ( Vaishnav et al., 2020 ). Enterobacter 64S1 and Pseudomonas 42P4 under salt stress reduced electrolyte leakage and lipid peroxidation and increased chlorophyll quantum efficiency (Fv/Fm), proline and antioxidant nonenzymatic compounds (carotenes and total phenolic compounds) contents in tomato leaves ( Pérez-Rodriguez et al., 2022 ). A combination of arbuscular mycorrhizal fungi ( Claroideoglomus etunicatum , Funneliformis mosseae , Glomus aggregatum , Rhizophagus intraradices ), bacteria and fungi ( Trichoderma , Streptomyces , Bacillus , Pseudomonas ) improved the tomato fruit quality and the antioxidant content of ‘Pixel F1’ tomato cultivar exposed to soils electrical conductivity of 1.5, 3.0, 4.5, and 6.0 ( Sellitto et al., 2019 ).

Some researchers have focused not only on assessing the individual effects of a potential priming agent against salt stress in tomato plants, but also their combined effect. For example, Attia et al. (2021) studied the effects of foliar application of chitosan dissolved in acetic acid (Ch ACE), ascorbic acid (Ch ASC), citric acid (Ch CIT) and malic acid chitosan (Ch MAL) on tomato cultivar 023 irrigated with saline water (100 mM NaCl). These treatments alleviated the negative effects of salinity on tomato plants by increasing the photosynthetic pigments, osmoprotective compounds, and potassium content and lowering MDA, H 2 O 2 and Na + levels in leaves. Chanratana et al. (2019) used as a bioinoculant chitosan-immobilized aggregated Methylobacterium oryzae CBMB20 to improve the salt tolerance of cv. ‘Yeoreum Mujeok Heukchima’ and the results showed that plant dry weight, nutrient uptake, photosynthetic efficiency, and the accumulation of proline have been enhanced. Furthermore, the oxidative stress exerted by salt stress was alleviated and the electrolyte leakage and the excess Na + influx into the plant cell were reduced.

Tomato genetic modification techniques have already proven their efficiency and accuracy in protecting plants against salinity stress by improving their genome. Gene transformation, gene editing, quantitative trait loci (QTLs) analysis, gene-pyramiding, and genetic engineering (overexpression) are some examples of molecular genetic tools that have helped in the development of salt-tolerant tomato plants.

Gene transformation has mainly focused on transferring genes of various origins, which can be good candidates to increase the tolerance to salinity stress, into tomato plants. Salt tolerant tomato plants were successfully obtained by Gilbert et al. by transferring the gene HAL1 from Saccharomyces cerevisiae , involved in Na + transport and K + regulation, which improved the in vivo and in vitro salt tolerance of transgenic tomato plants, by promoting the retention of K + and the growth of the plants ( Gisbert et al., 2000 ); by Goel et al., who demonstrated that by transforming the tomato cultivar ‘Pusa Ruby’ with the bacterial codA gene from Arthrobacter globiformis encoding for choline oxidase, the production of glycine betaine was induced, the content of relative water, chlorophyll and proline increased, also the overall tolerance of the plants under saline stress was improved ( Goel et al., 2011 ); by Jia et al., who transferred the BADH gene from Atriplex hortensis in ‘Bailichun’ tomato cultivar, obtaining a normal growth and development of the plants treated with 120 mM NaCl ( Jia et al., 2002 ); by Li et al., who isolated the SpPKE1 a lysine-, glutamic- and proline-rich type gene from the abiotic resistant Solanum pennellii  LA0716 and transferred it to S. lycopersicum  cv. M82 or by transferring the Osmotin gene from tobacco into tomato plants, an increased tolerance to salt stress was obtained, highlighted by better cell signaling, ROS scavenging, the content of carbohydrates, amino acids, polyols and performance of the antioxidant and photosynthetic systems ( Goel et al., 2011 ; Li et al., 2019a ; Rao et al., 2020 ).

The only genetic editing technique that has been reported to be used in improving the tomato tolerance to salinity is clustered regularly interspaced short palindromic repeat (CRISPR)-Cas9 (CRISPR-associated nuclease 9) a modern, easy and very effective genome editing tool ( Salava et al., 2021 ; Altaf et al., 2022a ). However, the researches on increasing tomato tolerance to salt stress by using CRISPR/Cas9 are still limited. So far, this tool was used to precisely edit the hybrid proline-rich proteins domain ( HyPRP1 ) involved in different biotic and abiotic responses. The deletion of the SlHyPRP1 negative-response domain led to salt tolerance as high as 150 mM NaCl, improving the germination and the growth of the plants ( Tran et al., 2021 ). The same results were obtained earlier by Li et al., who also observed that by silencing the negative regulator HyPRP1 the expression of the genes responsible for the production of SOD and CAT was enhanced ( Li et al., 2016 ). In addition, CRISPR/Cas9 technology was used to knock out the SlABIG1 gene in tomato exposed to salinity, resulting plants with improved chlorophyll and proline content, photosynthetic system, root dry weight and decreased concentrations of ROS, MDA and Na + ( Ding et al., 2022 ). By using the same tool, Wang et al., demonstrated the importance of the plasma membrane Na + /H + antiporter SlSOS1 in the salt tolerance of tomato, by creating two mutant alleles ( Slsos1-1  and  Slsos1-2 ) which showed a significant increase in the Na + /K +  ratio and the salt sensitivity, as compared with the wild type ( Wang et al., 2021 ). Bouzroud et al., by generating tomato SlARF4 -crispr ( arf4-cr ) plants showed the importance of Auxin Response Factor 4 (ARF4) in the tolerance of tomato plants to salinity ( Bouzroud et al., 2020 ). Regarding the other two known genetic editing techniques (zinc finger nucleases - ZFNs and Transcription Activator-Like Effector Nucleases - TALENs) no reports are available on tomato tolerance ( Salava et al., 2021 ; Altaf et al., 2022a ).

Due to the QTLs mapping, different loci related to the oxidative defence system, Na + /K +  homeostasis, or developmental stages were identified in playing an important role in increasing the tomato tolerance to salinity. Therefore, Frary et al., identified 125 QTLs for antioxidant compounds under saline and non-saline conditions in S. pennellii tomato introgression lines, and their parental lines, salt-resistant wild tomato ( S. pennellii LA716) and the salt sensitive cultivated S. lycopersicum Mill. cv. M82 that could be beneficial in developing salt-tolerant cultivars. Under the salt stress (150 mM NaCl), the wild tomato and different introgression lines accumulated more antioxidant compounds (phenolics, flavonoids, SOD, CAT, APX) than the cultivated tomato ( Frary et al., 2010 ). The same wild tomato ascension, the wild S. lycopersicoides  LA2951 and two introgression lines derived from them were used to identify QTLs for tolerance to salinity in the seedling stage by Li et al. Four major QTLs were detected on chromosomes 6, 7 and 11 in S. pennellii  IL library, while in S. lycopersicoides  IL library, six major QTLs were found on chromosomes 4, 6, 9 and 12. The authors concluded the possibility to create hybrids with QTLs coming from these two ascensions ( Li et al., 2011 ). Foolad et al., detected and validated a number of five QTLs for tomato salt tolerance during vegetative growth in a population (BC 1 ) resulted from the crosses between the breeding line NC84173 ( Lycopersicon esculentum Mill.) and L. pimpinellifolium (Jusl.) Mill. accession LA722. One minor QTLs was identified on chromosome 3 in the interval CT82–TG515, two major QTLs on chromosomes 1 and 5, and the other two on chromosomes 6 and 11 ( Foolad et al., 2001 ). Villalta el al., found QTLs for salt tolerance during reproductive stage in two populations of F7 tomato lines (P and C) resulted from ‘cerasiforme’ variety (salt sensitive genotype), as female parent, and two lines tolerant to salt tolerant, as male parents: S. pimpinellifolium , the P population (142 lines), and S. cheesmaniae , the C population (116 lines). The authors suggested that the QTLs detected by them can be used to increase the fruit yield of tomato plants under salt stress, being good candidates for increasing the tomato tolerance to salinity. The QTLs for fruit yield were detected in chromosome 5, the specific loci being fn5.2 and tw8.1 found in C population and fn10.1 which overlaps  tw10.1 and fw8.1 loci in P population. Under saline conditions the fruits set percentage per truss, fruit number per plant and the total fruit weight per plant increased ( Villalta et al., 2007 ). Other candidates for QTL can be those associated with Na + /K +  homeostasis are the genes encoding HKT1-like transporters ( SlHKT1;1  and  SlHKT1;2 ), with tonoplast NHX Na + /H + -antiporters ( SlNHX3  and  SlNHX4 ), with the content of α-tocopherol in tomato fruits (chromosomes 6 and 9), or with tocopherol biosynthesis (chromosomes 7, 8, and 9) ( Egea et al., 2022 ).

Gene pyramiding, which consists in combining multiple traits in a single genotype, represents another method that can help to obtain tomato plants tolerant to salinity stress, but the researches are still limited. Some strategies that have been proposed refer to pyramiding the ascorbic acid (AsA) biosynthetic pathway, the ascorbate–glutathione pathway, or different QTLs. For improving the AsA content in tomato, Li et al. pyramided the biosynthetic genes involved in the D-Man/L-Gal pathway of ascorbate, resulting the pyramiding lines GDP-Mannose 3′,5′-epimerase ( GME ) × GDP-d-mannose pyrophosphorylase ( GMP ), GDP-l-Gal phosphorylase ( GGP ) × l-Gal-1-P phosphatase ( GPP ) and  GME  ×  GMP ×  GGP  ×  GPP . The results showed increased concentrations of total ascorbate in leaves and fruits and improved AsA transport capacity, light response and salinity stress tolerance. In addition, the fruit weight (significantly decreased in GGP × GPP  lines), fruit size (significantly decreased in GMP × GME and GGP × GPP  lines), and soluble solid (significantly increased in GMP × GME  and  GMP × GME × GGP × GPP  lines) were affected by pyramiding maybe because of the influence of different primary metabolism pathways (sugar, acid, and cell wall metabolism) as stated by the authors ( Li et al., 2019b ). By pyramiding the genes of ascorbate-glutathione pathway, isolated from Pennisetum glaucoma (Pg) ( PgSOD, PgAPX, PgGR, PgDHAR  and  PgMDHAR ) Raja et al., obtained tomato lines with better germination rate, survival rate, photosynthetic and antioxidant activity, reduced ROS production, and membrane disruption, under 200 mM NaCl ( Raja et al., 2022 ). Pyramiding QTLs can be an effective method to improve the tomato salt tolerance. The pyramiding of QTLs takes place by using a marker assisted selection (MAS). Some authors proposed the use of different QTLs associated with salt tolerance during seed germination or vegetative growth in tomato ( Foolad, 2004 ).

Another way to enhance the tomato salt tolerance is to overexpress specific genes that can increase the tomato tolerance to salt stress. Some authors highlighted the importance of various genes in the salt stress in transgenic plants and, in this respect, Hu et al. (2014) demonstrated that the overexpression of LeERF1  and  LeERF2 genes have a positive impact on tomato plants exposed to salinity stress. Good results regarding different physiological and biochemical parameters (i.e. root length, chlorophyll, proline and antioxidant enzymes contents) were obtained in the transgenic tomato, where the expression of other genes related to salinity stress was up-regulated ( RBOHC, TAS14 ,  HVA22 ,  PR5  and  LHA1 ). The overexpression of SlERF5 gene (ethylene response factor) in transgenic tomato led to an increased tolerance to salinity by improving the relative water content ( Rao et al., 2020 ). Albacete et al. (2014) recorded improved fruit yield, hormone concentrations, and sugar content in transgenic tomato due to the overexpression of a gene coding for isopentenyl transferase, an enzyme involved in cytokines biosynthesis – IPT gene and a cell wall invertase gene – CIN1 . Cai et al., 2016 showed the importance of SlDof22 gene, coding for Dof proteins responsible for abiotic stress response, gibberellins regulation, and evolution of cell cycle, in improving the tomato tolerance to salinity stress. Other genes whose expression increased the tomato plant biomass production and yield under salinity stress were CDF3 , which regulated important genes for redox homeostasis, photosynthesis process or primary metabolism ( Renau-Morata et al., 2017 ). NAC transcription factor SlTAF1 is another gene described as a good candidate for increasing the salinity tolerance of tomato and other species. It’s silencing in transgenic plants increased the damages related to salinity ( Devkar et al., 2020 ).

Conclusions and future perspectives

Soil salinity represents one of the main causes of agricultural yield losses worldwide. Natural factors such as topography, and type of geological material, but especially anthropogenic activities like inappropriate agricultural practices (i.e. excessive fertilization, irrigation without proper drainage, and leaching) intensify the soil salinization process. Plants are directly impacted by the increases in soil salt concentration through reduced water and nutrient uptake by roots. In tomato plants, salinity stress affects positively ornegatively the germination process, the morphological traits, the physiological features, the biochemical and molecular parameters, and also the yield. Usually, the germination, morphology and physiology of tomato plants are negatively influenced by the saline stress. When the soil salinity increases, its water potential drops to a point close to the root water potential, slowing down the process of water uptake by roots, thus causing drought stress-related symptoms. Also, in saline soils, nutrients in the form of cations (Mg + , Ca + , K + , NH 4 + ) and anions ( NO 3 − , PO 4 3 − ) compete with Na + and Cl − to be transported inside the plant. Na + competes with NH 4 + and K + cations decreasing their absorption, while Cl − competes with NO 3 − anions decreasing its uptake. Therefore, along with a deficiency in the nutrient uptake, ion toxicity takes place due to excessive concentrations of Na + and Cl − , consequently affecting plant growth and development. Regarding the effects on gene expression, the salinity stress can down-regulate or up-regulate the expression of genes in tomato plants. A similar situation also occurs with regard to the biochemical parameters which can either be enhanced by the saline stress or can be decreased. Generally, most of the increases and the decreases recorded for the biochemical parameters and the up- or down-regulation of genes represent adaptive responses to stress by plants that try to improve their homeostasis and resistance. However, the decreases can also be the result of biochemical pathways dysregulations. The quality of tomato fruit benefits from saline conditions in most cases, maybe due to lower water content and accumulation of biomolecules such as sugars, amino acids, and inorganic solutes that contribute to osmotic adjustments.

The results of the studies carried out over the last 10 years have shed more light on the impact that saline stress can have on tomato plants. However, for a clearer image of the effects of salinity on tomato plants, more studies should be carried out in the field, in salt-affected soils, taking into account the individual and cumulative interactions of the factors involved.

The deleterious effects of salinity on tomato plants can be alleviated by using different strategies like plant priming or genetic modification techniques. The results are very promising, but at this moment, they are relatively limited and at their beginnings. In addition, most of the research has focused on developing salt-resistant tomato plants and testing them for the needed characters, but to develop commercial lines, research carried out in saline fields are needed.

Considering the FAO predictions that by 2050 more than 50% of arable land will become saline, urgent measures should also be taken to reduce the salinization process such as better water drainage and leaching of salts; a decrease in the quantity and number of fertilizers applied and water used in irrigation; proper crop selection or reduction of the degree of tillage systems. Therefore, researchers should focus more their attention on methods to desalinate the soils, on studies regarding the development of fertigation schemes that promote a better management of water and fertilizers applied according to the plant requirements, on the production of new varieties resistant to salinity, or in improving the existing species.

Author contributions

VS, GM and MR: Conceptualization. MR and GM: Formal analysis. MR and GM: Investigation. MR and GM: Writing—original draft preparation. VS: Supervision and validation. VS, GM and MR: Writing - review & editing. MR and GM contributed equally to this work and share first authorship. All authors have read and agreed to this version of the manuscript. All authors contributed to the article and approved the submitted version.

Acknowledgments

The authors are grateful to prof. Gianluca Caruso for his time and efforts in assisting with the proofreading of the manuscript.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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Keywords: abiotic stress, PRISMA, salt stress, screening of salinity effects, tomato, alleviation of salinity effects

Citation: Roșca M, Mihalache G and Stoleru V (2023) Tomato responses to salinity stress: From morphological traits to genetic changes. Front. Plant Sci. 14:1118383. doi: 10.3389/fpls.2023.1118383

Received: 07 December 2022; Accepted: 26 January 2023; Published: 10 February 2023.

Reviewed by:

Copyright © 2023 Roșca, Mihalache and Stoleru. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Vasile Stoleru, [email protected]

† These authors have contributed equally to this work and share first authorship

This article is part of the Research Topic

Gene Regulatory Networks involved in the Molecular Response to Drought, Salt and Osmotic Stresses in Crops

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Best Agronomic Practices of Tomato Cultivation

by M. Darthiya

2021, www.justagriculture.in

Tomato is the most important vegetable crop in India. Due to climate change, tomato growing farmers are facing some problems like drought and ground water depletion and labour scarcity. The wages for labours have also increased which leads to increase in cost of cultivation. Weeds are another major problem in tomato crop due to labour shortage and with increase in labour wages it is even more difficult to manage weeds in tomato crop. Now- a - days farmers are adopting plastic mulching in tomato. Plastic mulching reduces the evaporation losses and prevents the weed seed germination. By adopting technologies like drip fertigation, staking, timely plant protection measures, plastic mulching and best time of transplanting the yield and quality of tomato is increased.

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Mulching methods and their effects on the yield of tomato (Lycopersicon esculentum, Mill.) in the Zeta plain

Scientific Reports

India produces around 19.0 million tonnes of tomatoes annually, which is insufficient to meet the ever-increasing demand. A big gap of tomato productivity (72.14 t ha–1) between India (24.66 t ha–1) and the USA (96.8 t ha–1) exist, which can be bridged by integrating trellis system of shoot training, shoot pruning, liquid fertilizers, farmyard manure, and mulching technologies. Therefore, the present experiment was conducted on tomato (cv. Himsona) during 2019–2020 at farmers' fields to improve tomato productivity and quality. There were five treatments laid in a randomized block design (RBD) with three replications; T1 [Farmer practice on the flatbed with RDF @ N120:P60:K60 + FYM @6.0 t ha−1 without mulch], T2 [T1 + Polythene mulch (50 microns)], T3 [Tomato plants grown on the raised bed with polythene mulch + FYM @ 8.0 t ha−1 + Single shoot trellis system + Side shoot pruning + Liquid Fertilizer (LF1—N19:P19:K19) @ 2.0 g l–1 for vegetative growth + Liquid Fertilizer (LF2—N0: P...

Modified plant architecture integrated with liquid fertilizers improves fruit productivity and quality of tomato in North West Himalaya, India

Arnold Bray Mashingaidze

An experiment was carried out from 30 March to 24 August 1994 to compare the effects of clear and black plastic mulch against an uncovered control on soil temperature, weed seed viability and weed seedling emergence and height and yield of tomatoes (Lycopersicon lycopersicum L. cultivar Moneymaker). Mean weekly soil temperatures at 2 cm depth at 1400 hrs were highest under the clear plastic and were generally lowest under the black plastic covers. The plastic covers did not affect the viability of weed seeds in soil samples collected from 0-3 and 0-5 cm depths at 6 and 10 weeks after transplanting (WAT) respectively. When the plastic mulch was removed at the end of the experiment, significantly more weeds (P<0,05) had emerged under the clear plastic (324 weeds per m2;) than in the uncovered control (99 weeds per m2) and under the black plastic (6 weeds per m2). Plant height at 12 WAT, number of plants with flowers and fruits at 7 WAT and 10 WAT respectively, were similar in the black and clear plastic treatments, but were lower (P<0,05) in the uncovered control. Yield was similar among the three treatments during the first four weekly harvests but plastic mulching resulted in significantly higher yields (P<0,05) than the control in the last three weeks of harvesting. Cumulative yield over the 7-week harvesting period significantly differed (P<0,01) among the three treatments being 18,6; 14,8 and 7,82 tonnes per ha for the clear plastic, black plastic and uncovered control respectively. The plastic mulching treatments enhanced tomato plant growth and yield by changing the temperature and light micro-environment around the plants.

The effects of clear and black plastic mulch on soil temperature, weed seed viability and seedling emergence, growth and yield of tomatoes

Yigzaw Dessalegn

2016, Journal of Horticulture and Forestry

The experiment was conducted to study the effect of mulch on growth and yield of tomato varieties under polyhouse condition at Bahir Dar, Ethiopia in 2012 and 2013. The treatments were 4 × 2 factorial combinations of mulching material (Black plastic mulch (BPM), White plastic mulch (WPM), Grass mulch (GM) and no mulch with two varieties (Cochoro and Miya). White plastic mulch recorded significantly tallest plant height followed by black plastic mulch. Significantly highest number of primary and secondary branches per plant were recorded for un-mulched Cochoro variety and mulched with grass, respectively in 2013. Cochoro variety mulched with grass produced significantly highest number of flowers per cluster in 2013. Significantly highest number of fruits per cluster and percent fruit set was registered when Miya variety was grown on grass and black plastic mulch, respectively. Earlier flower, fruit set and maturity of fruits were recorded from plants mulched with white plastic. Signi...

Influence of mulching and varieties on growth and yield of tomato under polyhouse

Shah Zareen

2017, JOURNAL OF WEED SCIENCE RESEARCH

Yield and yield attributes of tomato (Lycopersicon esculentum Mill) cultivars influenced by weed management techniques

jitender bhatia

2016, Indian Journal of Economics and Development

Knowledge of Farmers Regarding Tomato Crop Production in Karnal District of Haryana

Savita Bhoutekar

2007, Agricultural Water Management

Experiments were conducted in summer of 2003 and 2004 to study the effect of withholding irrigation on tomato growth and yield in a drip irrigated, plasticulture system. Irrigation treatments were initiated at tomato planting (S0), after transplant establishment (S1), at first flower (S2), at first fruit (S3), or at fruit ripening (S4). An additional treatment received only enough water to apply fertigation (FT). Withholding drip irrigation for a short period (S2–S3) increased tomato marketable yield by 8–15%, fruit number by 12–14% while reducing amount of irrigation water by 20% compared to the S0 treatment. Withholding drip irrigation also increased irrigation water use efficiency (IWUE). Similar trends were observed in 2003 and 2004 despite large differences in rainfall, heat units, and tomato yield between years. This suggests that if soil moisture is adequate at transplanting, subsequent withholding of irrigation for 1–2 weeks after tomato transplanting may increase yield while reducing the amount of irrigation water.

Withholding of drip irrigation between transplanting and flowering increases the yield of field-grown tomato under plastic mulch

rajnish prasad rajesh

Journal of Agrometeorology

Microclimatic alteration produced by mulching with different coloured plastic sheets, inside and outside the polyhouse and its effect on yield of tomato was studied during 2012-13 at Birsa Agricultural University, Ranchi. The mean weekly minimum and maximum air temperature during last week of December to 1st week of March were found to be higher by 2 to 9 0C inside the polyhouse than open field. Relative humidity was always higher in the open field during January to February by 2 to 7 % but it was higher inside the polyhouse in the months of March to May by 4 % at 7.00 AM. Almost a similar trend at 2.00 PM was also observed but during March to April relative humidity was higher by 10 % in polyhouse condition. The maximum available light intensity inside the polyhouse was about 30 to 40 % lower than that of the open field irrespective of growth stages. Average soil temperature was found to be higher by 2 to 5 0C under open field condition than inside the polyhouse. Leaf temperature o...

Microclimatic alteration through protective cultivation and its effect on tomato yield

namita raut

Field experiment was conducted at Vegetable block of College of Horticulture, Bagalkote, University of Horticultural Sciences, Bagalkote to study the effect of different levels of irrigation and mulches on growth and yield of tomato. The experiment with 12 treatment combinations was laid out in split plot design with three replications. Main plot constitutes four irrigation levels (I1: 100%, I2: 80%, I3: 60% and I4: 40% cumulative pan evapotranspiration) and subplot comprised of three levels of mulches (M1: Without mulch, M2: Sugarcane mulch and M3: Polythene mulch). Irrigation was given based on cumulative pan evapotranspiration following alternate day irrigation schedule using drip irrigation. The treatment combination receiving drip irrigation at 80 per cent CPE along with polythene mulch (I2M3) was recorded with highest fruit yield per plant (2.74 kg), yield per plot (60.90 kg) and yield per hectare (51.83 t/ha). The same treatment combination was noticed with highest benefit co...

Impact of different levels of irrigation and mulches on yield of tomato, water use efficiency, weed density and soil moisture percentage in Northern dry zone of Karnataka

Priyanka Bijalwan

2020, Journal of Experimental Agriculture International

In this study we evaluated the effects of two different types of mulches (black mulch, silver/black) on weed control and yield in tomato (Solanum lycopersicum L.) production. Field studies were carried out during 2017-2018 and 2018-2019. The treatments consisted in the study were planting methods (raised bed/flat bed), polythene mulching applications (black mulch, silver/black and unmulched plots) and training systems (two stem and three stem). Tomato seedlings were transplanted in the plots, where mulch application had already been done prior transplanting.The results indicated thatmarketable tomato yield from the treatments consisting of black mulch, was higher compared to the other unmulched plots for both the years of study. In unmulched plots there was reduction of tomato yield. Mulch treatments reduced the number of weeds, weed intensity, and above ground biomass (fresh weight and dry weight of weeds) as compared to control plots. At tomato harvest weeds were well suppressed b...

Mulch Cover Management for Improving Weed Control in Tomato (Solanum lycopersicum L.) Production

Rehmat Karim

The primary data used for the investigation were obtained through a questionnaire. One hundred and twenty (120) farmers were randomly selected; their education level, area of cultivation, time of planting, intercropping, varieties grown, fertilizer used, time of picking, packing, transportation and processing were looked at. It was found that out of 120 respondents, 52% were literate, and 48% were illiterate. 90% land holders were owners while remaining were tenants. Roma variety (46%) was preferred variety followed by Rio-Grind (38%) and Heirloom variety (16%). In terms of picking time, majority of farmers picked tomatoes in the afternoon (38%) or evenings (34%) and rest picked them in the mornings (28%). All the farmers transported tomatoes to local market either in wooden boxes (76%) or traditional baskets (24%). Majority of the farmers responded positively to drying tomato, but (27%) were unaware of processing procedures. Over all loss of tomato crop to fungal and viral diseases...

Assessment of production practices of small scale farm holders of tomato in Bagrote Valley, CKNP region of Gilgit-Baltistan, Pakistan

Murali Arthanari

Tomato (Solanum lycopersicum) is a popular vegetable belongs to Solanaceae family, which is considered as most important vegetable crop and known as poor man’s orange due to its specific nutritive values. Naturally tomato receives high amount of inputs viz., inorganic fertilizers and plant protection chemicals leads to the more toxic accumulation and is consumed as horticultural maturity. Concerning the ill effects of chemical farming, now the trend have changed to organic farming and there is an emerging awareness among public on consuming organic produces.

Effect of Weed Management Practices on Tomato Yield Parameters, Yield and Soil Microbial Population

Bhuvnesh Kumar

The influence of black polyethylene mulch (BPM) on growth and yield of tomato was investigated under a low-input cultivation system in arid high altitude (elevation 3344 m) in trans-Himalaya. The mean marketable yield varied from 27.8±2.5 t.ha-1 in open-pollinated varieties with no mulch treatment to 81.2±11.9 t.ha-1 in hybrid tomatoes with BPM. The yield of hybrid tomatoes with BPM is similar or greater than those reported in high-input systems. With BPM, total marketable yield in hybrid varieties increased by 102 per cent and 107 per cent in 2014 and 2015, respectively. Yield increase due to mulching in open-pollinated varieties was 86 per cent and 80 per cent in 2014 and 2015, respectively. Increase in early fruiting under BPM was observed in all the five varieties studied. Difference in soil temperature between mulch and unmulch was significantly higher at early growth stage than during later stages. BPM reduced 57 per cent weed and save 74 per cent time in manual weeding. Incid...

Black Polyethylene Mulch Doubled Tomato Yield in a Low-input System in Arid Trans-Himalayan Ladakh Region

SVU-International Journal of Agricultural Sciences

Mulching strategy provides higher healthier, and cleaner tomato (Solanum lycopersicum) crop in a profitable way

Amar sawant

Tomato Cultivation Guide 2018 agricultureguruji.com/tomato-cultivation

Kenneth Mutoro

2021, Academia Letters

Effect of organic and inorganic mulching materials on tomato growth and development in Western Kenya

anurag malik

The Indian Journal of Agricultural Sciences

The field experiment was conducted during two consecutive years 2016-17 and 2017-18 to find out the influence of weed management practices and dates of transplanting on weed, fruit yield and profitability of tomato (Solanum lycopersicum L.) at Vegetable Research Farm of Chandra Shekhar Azad University of Agricultural and Technology, Kanpur. The experiment was laid out in factorial randomized block design (FRBD) with four different dates of transplanting, viz. 15 October, 31 October, 15 November and 30 November and four type of mulches, viz. black polyethylene, white polyethylene, bio-mulch (paddy straw) and control (without mulch) replicated thrice. Tomato cultivar Azad T-6 was used in experiment. Results of the experiment revealed that the minimum weed population (4.43 and 4.26/m2) and weeds fresh weight (9.52 and 9.15 g/m2) and significantly highest marketable yield (30610 and 31418 kg/ha) and net returns (` 241460.50 and 249538.00/ha) were recorded in crop transplanted on 30 Octo...

Influence of weed management practices and dates of transplanting in tomato (Solanum lycopersicum)

sathish bollaveni

Ecology, Environment and Conservation

The present investigation was carried out to study the effect of integrated crop management practices on yield and economics of tomato at farmer’s field of Mancherial district, Telangana state during the year from 2019-20, 2020-21 and 2021-22. The farming area available for the production of tomato across India during the financial year 2022 is estimated to have amounted to 841 thousand hectares. The treatments consist of farmer practice (T1) with application of RDF (180: 100: 60 kg NPK ha-1) and direct sowing in the field and T2 consists of raising of seedlings by nursery, installation of yellow sticky traps @ 25 ha-1, staking of plants, marigold grown as trap crop (tomato 16 rows: marigold 1 row) and spraying of need-based chemicals along with application of RDF (180: 100: 60 kg NPK ha-1). The results revealed that the total percent yield gap between potential yield and actual yield of tomato was 52.94 percent, in which 10.38 percent of yield gap between demonstration plot and act...

Effect of ICM Practices on Yield and Economics in Tomato (Lycopersicon esculentum Mill.)

Luisa del Piano

2020, Acta Horticulturae

Plant growth, yield, fruit quality and residual biomass composition of tomato as affected by mulch type

John Cardina

Journal of the American Society for Horticultural Science

Four tomato production systems were compared at Columbus and Fremont, Ohio: 1) a conventional system; 2) an integrated system [a fall-planted cover-crop mixture of hairy vetch (Vicia villosa Roth.), rye (Secale cereale L.), crimson clover (Trifolium incarnatum L.), and barley (Hordeum vulgare L.) killed before tomato planting and left as mulch, and reduced chemical inputs]; 3) an organic system (with cover-crop mixture and no synthetic chemical inputs); and (4) a no-input system (with cover-crop mixture and no additional management or inputs). Nitrogen in the cover-crop mixture above-ground biomass was 220 kg·ha-1 in Columbus and 360 kg·ha-1 in Fremont. Mulch systems (with cover-crop mixture on the bed surface) had higher soil moisture levels and reduced soil maximum temperatures relative to the conventional system. Overall, the cover-crop mulch suppressed weeds as well as herbicide plots, and no additional weed control was needed during the season. There were no differences in the ...

A Comparison of Four Processing Tomato Production Systems Differing in Cover Crop and Chemical Inputs

Arpna Bajpai

2015, Bhartiya Krishi Anusandhan Patrika

A field experiment was conducted on tomato (Lycopersicon esculentum L.) at during growing season (December-April) in 2013-14 and 2014-15, in a randomized complete block design with four replications. Treatments consisted of three colored polyethylene mulch (red, black and silver) with organic mulch and as controls. Results showed that the highest soil temperature was recorded under red plastic mulch. The highest plant height, number of flowers per cluster, SPAD value, fruit weight and yield also recorded in red mulch than black and silver plastic mulch as compared to least without mulch. The plants grown on red mulch produced maximum marketable yield.

Effect of different mulches on the growth, yield and economics of tomato (Lycopersicon esculentum L.)

Sharad Bisen

Yield Gap Analysis, Economics, Adoption and Horizontal Spread of Tomato Cultivation through Front Line Demonstration in Seoni District of Madhya Pradesh

Harish Chandra Raturi

2017, Annals of Horticulture

Effect of biofertilizer and mulch on yield, quality and nutrient content in tomato field grown under mid hills condtions of Himachal Pradesh

Amon Maerere

2015, African Journal of Food, Agriculture, Nutrition and Development

Effect of mulch and different fungicide spray regimes on yield of tomato (Solanum lycopersicum L.) in Tanzania

Deepak Chouhan

Effect of Green Shade Net on Yield and Quality of Tomato

vimal chaudhary

Different varieties of tomato trail were conducted as the on-farm tail (OFT) in Raisen district of Madhya Pradesh during 2018-19 and 2019-20 to compare the growth development and production potential of three (3) varieties of tomato viz. local check, Arka Rakshak, Arka Samratat farmers field under Krishi Vigyan Kendra, Raisen. Experimental data were collected, i.e. Plant height, total branch plant1, number of fruits plant1, average fruit weight, fruit length, fruit breath, Fruit yield Plant1 (Kg), fruit yield q/ha, production efficiency (Kg/ha/day), Economic efficiency (Rs/ha/day), Gross returns (Rs/ha), Net Returns (Rs/ha). The experiment was laid out in Complete Randomized Block Design. The mean data of all the observations over two years were pooled and statistically analyzed. The result revealed that a maximum number of fruit/plant (26.648), average fruit weight (90.634 gm), Fruit yield/Plant, (2.425kg/ha), fruit yield per hectare (471.5182 q/ha), production efficiency (589.397 ...

Evaluation of Tomato varieties for growth and yield components in Madhya Pradesh

Jayson K. Harper

1995, Journal of the American Society for Horticultural Science

During the initial season of implementation, four tomato production systems differing in soil management, pest control practices, and level of inputs, such as labor, materials, and management intensity were evaluated. These systems were CON, a low input (no mulch, no trellising, overhead irrigation, preplant fertilization, scheduled pest control), conventional agrichemical system; BLD, a high input [straw mulch, trellising, trickle irrigation, compost fertility amendment, integrated pest management (IPM)], ecologically-oriented system that emphasized the building up of soil organic matter levels and used no agrichemicals to supply fertility or for pest control; BLD+, a system similar to BLD, except that agrichemical pesticides were used; and ICM, a high input system (black polyethylene mulch, trellising, trickle irrigation, fertigation, IPM pest control) that used agrichemicals to supply fertility and for pest control. Soil characteristics and fertility levels in the BLD and BLD+ sy...

Evaluation of the Initial Season for Implementation of Four Tomato Production Systems

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    PDF | The continued importance of tomato (Lycopersicon esculentum Mill.) as a vegetable and salad commodity is reflected by the large volume of research... | Find, read and cite all the...

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    2018:3 Online publication: https://pub.epsilon.slu.se Bibliographic reference: Villanueva, EE (2018). An overview of recent studies of tomato (Solanum lycopersicum spp ) from a social, biochemical and genetic perspective on quality parameters Alnarp-Sweden: Sveriges lantbruksuniversitet. (Introductory Paper, 2018:3). Keywords:

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    1. Introduction. Tomato (Lycopersicon esculentum Mill.) belongs to the family of Solanaceae.It is the second most important economically important vegetable in the World (Ibitoye et al. Citation 2009; Muriel et al., Citation 2019).In Ethiopia tomato is one of the most important and widely grown vegetable crops, both during the rainy and dry seasons for its fruit by smallholder farmers ...

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