Effect of Salt Stress on the Growth and Fruit Quality of Tomato Plants

  • Takeshi Saito
  • Chiaki MatsukuraEmail author


During the past several decades, salt injury has arisen as one of the most serious problems in agriculture worldwide, especially in arid and semiarid areas. Generally, excessive exposure of crops to salinity stress leads to yield reduction and loss of quality. However, for tomato crops, moderate salt stress improves the fruit quality, increasing nutritional components but decreasing fruit yield. In the current Japanese market, such fruits are referred to as “fruit tomatoes” and are sold at a higher price compared with normally cultivated tomatoes because of their high Brix (sugar content) and excellent flavor. Previously, the mechanism underlying this phenomenon was referred to as a “concentration effect” because fruit enlargement was suppressed by limited water uptake as a result of salt stress. However, recent studies have suggested that, in addition to the “concentration effect,” certain metabolic and molecular genetic responses to salinity are also involved in the development of fruit tomatoes. Here, we introduce metabolic alterations in major fruit components such as sugars, amino acids, organic acids, and carotenoids in high-Brix fruit, and we describe the physiological changes observed in tomato plants exposed to salt stress. We also discuss possible molecular mechanisms underlying the production of fruit tomatoes.


ADP-glucose pyrophosphorylase Amino acid Assimilate transport Fruit quality GABA Invertase Organic acid Salt stress Starch Tomato 


  1. Adams P (1991) Effects of increasing the salinity of nutrient solution with major nutrients or sodium chloride on the yield, quality and composition of tomatoes grown in rockwool. J Hortic Sci 66:201–207Google Scholar
  2. Adams P, Ho LC (1992) The susceptibility of modern tomato cultivars to blossom-end rot in relation to salinity. J Hortic Sci 67:827–839Google Scholar
  3. Akihiro T, Koike S, Tani R, Tominaga T, Watanabe S, Iijima Y, Aoki K, Shibata D, Ashihara H, Matsukura C, Akama K, Fujimura T, Ezura H (2008) Biochemical mechanism on GABA accumulation during fruit development in tomato. Plant Cell Physiol 49:1378–1389PubMedCrossRefGoogle Scholar
  4. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  5. Ashton JD, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223CrossRefGoogle Scholar
  6. Aurisano N, Bertani A, Reggiani R (1995) Involvement of calcium and calmodulin in protein and amino acid metabolism in rice roots under anoxia. Plant Cell Physiol 36:1525–1529Google Scholar
  7. Balibrea ME, Santa Cruz AM, Bolarin MC, Perez-Alfocea F (1996) Sucrolytic activities in relation to sink strength and carbohydrate composition in tomato fruit growing under salinity. Plant Sci 118:47–55CrossRefGoogle Scholar
  8. Balibrea ME, Martinez-Andújar C, Cuartero J, Bolarín M, Pérez-Alfocea F (2006) The high fruit soluble sugar content in wild Lycopersicon species and their hybrids with cultivars depends on sucrose import during ripening rather than on sucrose metabolism. Funct Plant Biol 33:279–288CrossRefGoogle Scholar
  9. Baxter CJ, Carrari F, Bauke A, Overy S, Hill SA, Quick PW, Fernie AR, Sweetlove LJ (2005) Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant Cell Physiol 46:425–437PubMedCrossRefGoogle Scholar
  10. Belda RM, Fenlon JS, Ho LC (1996) Salinity effects on the xylem vessels in tomato fruit among cultivars with different susceptibilities to blossom-end rot. J Hortic Sci 71:173–179Google Scholar
  11. Bouchè N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115PubMedCrossRefGoogle Scholar
  12. Canene-Adams K, Campbell JK, Zaripheh S, Jeffery EH, Erdman JW (2005) The tomato as a functional food. Symposium: relative bioactivity of functional foods and related dietary supplements. J Nutr 135:1226–1230PubMedGoogle Scholar
  13. Carvajal M, Cerda A, Martinez V (2000) Modification of the response of saline stressed tomato plants by the correction of cation disorders. Plant Growth Regul 30:37–47CrossRefGoogle Scholar
  14. Chen BY, Janes HW, Gianfagna T (1998) PCR cloning and characterization of multiple ADP-glucose pyrophosphorylase cDNA from tomato. Plant Sci 6:59–67CrossRefGoogle Scholar
  15. Chengappa S, Guilleroux M, Wendy P, Shields R (1999) Transgenic tomato plants with decreased sucrose synthase are unaltered in starch and sugar accumulation in the fruit. Plant Mol Biol 40:213–221PubMedCrossRefGoogle Scholar
  16. Chretien S, Gosselin A, Dorais M (2000) High electrical conductivity and radiation-based water management improve fruit quality of greenhouse tomatoes grown in rockwool. HortScience 35:627–631Google Scholar
  17. Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248CrossRefGoogle Scholar
  18. Cuartero J, Fernandez-Munoz R (1999) Tomato and salinity. Sci Hortic 78:83–125CrossRefGoogle Scholar
  19. D’Aoust MA, Yelle S, Nguyen-Quoc B (1999) Antisense inhibition of tomato fruit sucrose synthase decrease fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11:2407–2418PubMedCentralPubMedCrossRefGoogle Scholar
  20. Davies JN (1964) Effects of nitrogen, phosphorus and potassium fertilizers on the non-volatile organic acids of tomato fruit. J Sci Food Agric 15:665–673CrossRefGoogle Scholar
  21. Davies JN, Hobson GE (1981) The constituents of tomato fruit: the influence of environment, nutrition, and genotype. CRC Crit Rev Food Sci Nutr 15:205–280CrossRefGoogle Scholar
  22. De Pascale S, Maggio A, Fogliano V, Ambrosino P, Ritieni A (2001) Irrigation with saline water improves carotenoids content and antioxidant activity of tomato. J Hortic Sci Biotechnol 76:447–453Google Scholar
  23. Dumas Y, Dadomo M, Di Lucca G, Grolier P (2003) Effects of environmental factors and agricultural techniques on antioxidant content of tomatoes. J Sci Food Agric 83:369–382CrossRefGoogle Scholar
  24. Ehret DL, Ho LC (1986) The effects of salinity on dry matter partitioning and fruit growth in tomatoes grown in nutrient film culture. J Hortic Sci 61:361–367Google Scholar
  25. Fanasca S, Martino A, Heuvelink E, Stanghellini C (2007) Effect of electrical conductivity, fruit pruning, and truss position on quality in greenhouse tomato fruit. J Hortic Sci Biotechnol 82:488–494Google Scholar
  26. Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Aust J Plant Physiol 22:875–884CrossRefGoogle Scholar
  27. Foolad MR (2004) Recent advances in genetics of salt tolerance in tomato. Plant Cell Tissue Organ Cult 76:101–119CrossRefGoogle Scholar
  28. Franco JA, Banon S, Madrid R (1994) Effects of protein hydrolysate applied by fertigation on the effectiveness of calcium as a corrector of blossom-end rot in tomato cultivated under saline condition. Sci Hortic 57:283–292CrossRefGoogle Scholar
  29. Fridman E, Liu YS, Carmel-Goren L, Shoresh AGM, Pleban T, Eshed Y, Zamir D (2002) Two tightly linked QTLs modify tomato sugar content via different physiological pathways. Mol Gen Genet 266:821–826CrossRefGoogle Scholar
  30. Fridman E, Carrari F, Liu YS, FernieAR ZD (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305:1786–1789PubMedCrossRefGoogle Scholar
  31. Gao Z, Sagi M, Lips SH (1998) Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum Mill.) as affected by salinity. Plant Sci 135:149–159CrossRefGoogle Scholar
  32. Godt D, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115:273–282PubMedCentralPubMedCrossRefGoogle Scholar
  33. Ho LC (1986) Metabolism and compartmentation of translocates in sink organs. In: Cronshaw J, Lucas WJ, Giaquinta RT (eds) Phloem transport. Liss, New York, pp 317–324Google Scholar
  34. Ho LC, Grange RI, Picken AJ (1987) An analysis of the accumulation of water and dry matter in tomato fruit. Plant Cell Environ 10:157–162Google Scholar
  35. Ho LC, Belda R, Brown M, Andrews J, Adams P (1993) Uptake and transport of calcium and the possible causes of blossom-end rot in tomato. J Hortic Sci 44:509–518Google Scholar
  36. Inaba A, Yamamoto T, Ito T, Nakamura R (1980) Changes in the concentrations of free amino acids and soluble nucleotide in attached and detached tomato fruits during ripening. J Jpn Soc Hortic Sci 49:435–441CrossRefGoogle Scholar
  37. Inoue K, Shirai T, Ochiai H, Kasao M, Hayakawa K, Kimura M, Sansawa H (2003) Blood-pressure-lowering effect of a novel fermented milk containing gamma-aminobutyric acid (GABA) in mild hypertensives. Eur J Clin Nutr 57:490–495PubMedCrossRefGoogle Scholar
  38. Johnson BS, Singh NK, Cherry JH, Locy RD (1997) Purification and characterization of glutamate decarboxylase from cowpea. Phytochemistry 46:39–44CrossRefGoogle Scholar
  39. Kader AA, Stevens MA, Albright M, Morris LL (1978) Amino acid composition and flavor of fresh market tomatoes as influenced by fruit ripeness when harvested. J Am Soc Hortic Sci 103:541–544Google Scholar
  40. Krauss S, Schnitzler WH, Grassmann J, Woitke M (2006) The influence of different electrical conductivity values in a simplified recalculating soilless system on inner and outer fruit quality characteristics of tomato. J Agric Food Chem 54:441–448PubMedCrossRefGoogle Scholar
  41. Li XY, Xing JP, Thomas JG, Harry JW (2002) Sucrose regulation of ADP-glucose pyrophosphorylase subunit genes transcript levels in leaves and fruits. Plant Sci 162:239–244PubMedCrossRefGoogle Scholar
  42. Li Z, Palmer WM, Martin AP, Wang R, Rainsford F, Jin Y, Patrick JW, Yang Y, Ruan YL (2012) High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J Exp Bot 63:1155–1166PubMedCentralPubMedCrossRefGoogle Scholar
  43. Lin TP, Caspar T, Somerville C, Preiss J (1988) A starch-deficient mutant of Arabidopsis thaliana with low ADP-glucose pyrophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiol 88:1175–1181PubMedCentralPubMedCrossRefGoogle Scholar
  44. Mae M, Makino Y, Oshita S, Kawagoe Y, Tanaka A, Aoki K, Kurabayashi A, Akihiro T, Akama K, Koike S, Takayama M, Matsukura C, Ezura H (2012) Accumulation mechanism of γ-aminobutyric acid in tomatoes (Solanum lycopersicum L.) under low O2 with and without CO2. J Agric Food Chem 60:1013–1019PubMedCrossRefGoogle Scholar
  45. Matsumoto Y, Ohno K, Hiraoka Y (1997) Studies on the utilization of functional food materials containing high levels of gamma-aminobutyric acid (part1). Ehime Kougi Kenkyu Houkoku 35:97–100 (in Japanese)Google Scholar
  46. Minoggio M, Bramati L, Simonetti P, Gardana C, Lemoli L, Santangelo E, Mauri PL, Spigno P, Soressi GP, Pietta PG (2003) Polyphenol pattern and antioxidant activity of different tomato lines and cultivars. Ann Nutr Metab 47:64–69PubMedCrossRefGoogle Scholar
  47. Morell MK, Bloom M, Knowles V, Preiss J (1987) Subunit structure of spinach leaf ADP glucose pyrophosphorylase. Plant Physiol 85:182–187PubMedCentralPubMedCrossRefGoogle Scholar
  48. Müller-Röber B, Kossamann J, Hannah LC, Willmitzer L, Sonnewald U (1990) One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet 224:136–146PubMedCrossRefGoogle Scholar
  49. N’tchobo H, Dali N, Nguyen-Quoc B, Foyer CH, Yelle S (1999) Starch synthesis in tomato remains constant throughout fruit development and is dependent on sucrose supply and sucrose synthase activity. J Exp Bot 50:1457–1463CrossRefGoogle Scholar
  50. Nielsen TH, Krapp A, Röper-Schwarz U, Stitt M (1998) The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP-glucose pyrophosphorylase is modified by nitrogen and phosphate. Plant Cell Environ 21:443–455CrossRefGoogle Scholar
  51. Ohyama A, Nishimura S, Hirai M (1998) Cloning of cDNA for a cell wall-bound acid invertase from tomato (Lycopersicon esculentum) and expression of soluble and cell wall-bound invertases in plants and wounded leaves of L. esculentum and L. peruvianum. Genes Genet Syst 73:149–157PubMedCrossRefGoogle Scholar
  52. Papadopoulos I, Rendig VV (1983) Tomato plant response to salinity. Agron J 75:696–700CrossRefGoogle Scholar
  53. Park SW, Chung WI (1998) Molecular cloning and organ-specific expression of three isoforms of tomato ADP-glucose pyrophosphorylase gene. Gene (Amst) 206:215–221CrossRefGoogle Scholar
  54. Petreikov M, Shen S, Yeselson Y, Levin I, Bar M, Schaffer AA (2006) Temporally extended gene expression of the ADP-Glc pyrophosphorylase large subunit (AgpL1) leads to increased enzyme activity in developing tomato fruit. Planta (Berl) 224:1465–1479CrossRefGoogle Scholar
  55. Robinson NL, Hewitt JD, Bennett AB (1988) Sink metabolism in tomato fruit. I. Developmental changes in carbohydrate metabolizing enzymes. Plant Physiol 87:727–730PubMedCentralPubMedCrossRefGoogle Scholar
  56. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613PubMedCrossRefGoogle Scholar
  57. Rolin D, Baldet P, Just D, Chevalier C, Biran M, Raymond P (2000) NMR study of low subcellular pH during the development of cherry tomato fruit. Aust J Plant Physiol 27:61–69Google Scholar
  58. Saito T, Fukuda N, Nishimura S (2006) Effects of salinity treatment duration and planting density on size and sugar content of hydroponically grown tomato fruits. J Jpn Soc Hortic Sci 75:392–398CrossRefGoogle Scholar
  59. Saito T, Matsukura C, Ban Y, Shoji K, Sugiyama M, Fukuda N, Nishimura S (2008a) Salinity stress affects assimilate metabolism at the gene-expression level during fruit development and improves fruit quality in tomato (Solanum lycopersicum L.). J Jpn Soc Hortic Sci 77:61–68CrossRefGoogle Scholar
  60. Saito T, Matsukura C, Sugiyama M, Watahiki A, Ohshima I, Iijima Y, Konishi C, Fujii T, Inai S, Nishimura S, Ezura H (2008b) Screening for γ-aminobutyric acid (GABA)-rich tomato varieties. J Jpn Soc Hortic Sci 77:242–250CrossRefGoogle Scholar
  61. Saito T, Fukuda N, Matsukura C, Nishimura S (2009) Effects of salinity on distribution of photosynthates and carbohydrate metabolism in tomato grown using nutrient film technique. J Jpn Soc Hortic Sci 78:90–96CrossRefGoogle Scholar
  62. Sakamoto Y, Watanabe S, Nakashima T, Okano K (1999) Effects of salinity at two ripening stages on the fruit quality of single-truss tomato grown in hydroponics. J Hortic Sci Biotechnol 74:690–693Google Scholar
  63. Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706PubMedCentralPubMedCrossRefGoogle Scholar
  64. Schaffer AA, Petreikov M (1997) Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol 113:739–746PubMedCentralPubMedGoogle Scholar
  65. Schaffer AA, Levin I, Ogus I, Petreikov M, Cincarevsky F, Yeselson E, Shen S, Gilboa N, Bar M (2000) ADP-glucose pyrophosphorylase activity and starch accumulation in immature tomato fruit: the effect of a Lycopersicon hirsutum-derived introgression encoding for the large subunit. Plant Sci 152:135–144CrossRefGoogle Scholar
  66. Scheible WR, Gonzàlez-Fontes A, Lauerer M, Müller-Röber B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798PubMedCentralPubMedCrossRefGoogle Scholar
  67. Shi J, Le Maguer M (2000) Lycopene in tomatoes: chemical and physical properties affected by food processing. Crit Rev Food Sci Nutr 40:1–42PubMedCrossRefGoogle Scholar
  68. Sinha AK, Hofmann MG, Römer U, Köckenberger W, Elling L, Roitsch T (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiol 128:1480–1489PubMedCentralPubMedCrossRefGoogle Scholar
  69. Snedden WA, Arazi T, Fromm H, Shelp BJ (1995) Calcium/calmodulin activation of soybean glutamate decarboxylase. Plant Physiol 108:543–549PubMedCentralPubMedGoogle Scholar
  70. Snedden WA, Koutsia N, Baum G, Fromm H (1996) Activation of a petunia glutamate decarboxylase by calcium/calmodulin or by a monoclonal antibody which recognizes the calmodulin binding domain. J Biol Chem 271:4148–4153PubMedCrossRefGoogle Scholar
  71. Sokolov LN, Dejardin A, Kleczkowski LA (1998) Sugars and light/dark exposure trigger differential regulation of ADP-glucose pyrophosphorylase genes in Arabidopsis thaliana (thale cress). Biochem J 336:681–687PubMedCentralPubMedGoogle Scholar
  72. Sorrequieta A, Ferraro G, Boggio SB, Valle EM (2010) Free amino acid production during tomato fruit ripening: a focus on l-glutamate. Amino Acids 38:1523–1532PubMedCrossRefGoogle Scholar
  73. Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM (1992) Regulation of the amount of starch in plant tissues by ADP-glucose pyrophosphorylase. Science 258:287–292PubMedCrossRefGoogle Scholar
  74. Stevens MA, Kader AA, Albright-Holton M, Algazi M (1977) Genotypic variation for flavour and composition in fresh market tomatoes. J Am Soc Hortic Sci 102:680–689Google Scholar
  75. Sturm A (1999) Invertases. primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7PubMedCentralPubMedCrossRefGoogle Scholar
  76. Tal M, Katz A, Heikin H, Dehan K (1979) Salt tolerance in the wild relatives of the cultivated tomato: proline accumulation in Lycopersicon esculentum Mill., L. peruvianum Mill. and Solanum pennellii Cor. treated with NaCl and polyethyleneglycol. New Phytol 82:349–355CrossRefGoogle Scholar
  77. Tsai CY, Neleson OE (1966) Starch-deficient maize mutant lacking adenosine diphosphate glucose pyrophosphorylase activity. Science 151:341–343PubMedCrossRefGoogle Scholar
  78. Turano FJ, Fang TK (1998) Characterization of two glutamate decarboxylase cDNA clones from Arabidopsis. Plant Physiol 117:1411–1421PubMedCentralPubMedCrossRefGoogle Scholar
  79. Van Ieperen W (1996) Effects of different day and night salinity levels on vegetative growth, yield and quality of tomato. J Hortic Sci 71:99–111Google Scholar
  80. Willumsen J, Petersen KK, Kaack K (1996) Yield and blossom-end rot of tomato affected by salinity and cation activity ratios in the root zone. J Hortic Sci 71:81–98Google Scholar
  81. Yamaki S (2010) Metabolism and accumulation of sugars translocated to fruit and their regulation. J Jpn Soc Hortic Sci 79:1–15CrossRefGoogle Scholar
  82. Yelle S, Hewitt JD, Nieder M, Robinson NL, Damon S, Bennett AB (1988) Sink metabolism in tomato fruit. III. Analysis of carbohydrate assimilation in a wild species. Plant Physiol 87:731–736CrossRefGoogle Scholar
  83. Yin YG, Tominaga T, Iijima Y, Aoki K, Shibata D, Ashihara H, Nishimura S, Ezura H, Matsukura C (2010a) Metabolic alterations in organic acids and γ-amino butyric acid in developing tomato (Solanum lycopersicum L.) fruits. Plant Cell Physiol 51:1300–1314PubMedCrossRefGoogle Scholar
  84. Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C (2010b) Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. ‘Micro-Tom’) fruits in an ABA- and osmotic stress-independent manner. J Exp Bot 61:563–574PubMedCentralPubMedCrossRefGoogle Scholar
  85. Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, Sulpice R, Zhou YH, Fernie AR (2009) RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol 150:1204–1218PubMedCentralPubMedCrossRefGoogle Scholar
  86. Zhang Y (2013) Regulation of ascorbate synthesis in plants. In: Zhang Y (ed) Ascorbic acid in plants. Biosynthesis, regulation and enhancement. Springer, New York, pp 87–99CrossRefGoogle Scholar
  87. Zhang SJ, Jackson MB (1993) GABA-activated chloride channels in secretory nerve endings. Science 259:531–534PubMedCrossRefGoogle Scholar
  88. Zushi K, Matsuzoe N (2006) Free amino acid contents of tomato fruit grown under water and salinity stresses. Acta Hortic 724:91–96Google Scholar
  89. Zushi K, Matsuzoe N (2009) Seasonal and cultivar differences in salt-induced changes in antioxidant system in tomato. Sci Hortic 120:181–187CrossRefGoogle Scholar
  90. Zushi K, Ono M, Matsuzoe N (2014) Light intensity modulates antioxidant systems in salt-stressed tomato (Solanum lycopersicum L. cv. Micro-Tom) fruits. Sci Hortic 165:384–391CrossRefGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  1. 1.Organization for the Strategic Coordination of Research and Intellectual PropertiesMeiji UniversityKanagawaJapan
  2. 2.Graduate School of Life and Environmental SciencesUniversity of TsukubaIbarakiJapan

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