Acta Biologica Hungarica

, Volume 69, Issue 4, pp 464–480 | Cite as

Comparison of the Responses to NaCl Stress of Three Tomato Introgression Lines

  • Fedia Rebah
  • Chayma OuhibiEmail author
  • K. H. Alamer
  • Najoua Msilini
  • Mouhiba Ben Nasri
  • Rebecca Stevens
  • Houneida Attia


We aimed to examine the response of three tomato introgression lines (IL925.3, IL925.5 and IL925.6) to NaCl stress. These lines originated from a cross between M82 (Solarium lycopersicum) and the wild salt-tolerant tomato Solarium permellii, each line containing a different fragment of the S.pennellii genome. Salt-sensitive phenotypes related to plant growth and physiology, and the response of antioxidants, pig-ments and antioxidant enzymes were measured. In general, salt stress decreased the fresh weight of leaves, leaf area and leaf number and an increase of Na+ accumulation in aerial parts was observed, which caused a reduction in the absorption of K+ and Ca2+. Salt stress also induced a decrease in chlorophyll, carotenoids and lipid peroxidation (MDA) and an increase in anthocyanins and reduced ascorbate, although some differences were seen between the lines, for example for carotenoid levels. Guaiacol per-oxidase, catalase and glutathione reductase activity enhanced in aerial parts of the lines, but again some differences were seen between the three lines. It is concluded that IL925.5 might be the most sensitive line to salt stress as its dry weight loss was the greatest in response to salt and this line showed the high-est Na+ ion accumulation in leaves.


Antioxidant enzymes ascorbate introgression lines salinity tomatoes variability 


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  1. 1.
    Agarwal, S., Pandey, V. (2004) Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biol. Plant. 48, 555–560.CrossRefGoogle Scholar
  2. 2.
    Akinci, S., Yilmaz, K., Akinci, I. E. (2004) Response of tomato (Lycopersicon esculentum Mill.) to salinity in the early growth stages for agricultural cultivation in saline environments. J. Environ. Biol. 25, 351–357.PubMedGoogle Scholar
  3. 3.
    Aktas, H., Abak, K., Cakmak, I. (2006) Genotypic variation in the response of pepper to salinity. Sci. Hortte. 10, 260–266.CrossRefGoogle Scholar
  4. 4.
    Alfocea, P. F., Estan, M. T., Caro, M., Guerrier, G. (1993) Osmotic adjustment in Lycopersicon esculentum and L. Pennellii under NaCl and polyethylene glycol 6000 iso-osmotic stresses. Physiol. Plant 87, 493–198.CrossRefGoogle Scholar
  5. 5.
    Ashraf M., Harris, P. J. C. (2004) Potential biochemical indicators of salinity tolerance in plants. Plant. Sci. 116, 3–16.CrossRefGoogle Scholar
  6. 6.
    Attia, H., Nouaili, S., Soltani, A., Lachaal, M. (2009) Comparison of the responses to NaCl stress of two pea cultivars using split-root system. Sci. Hort. 123, 164–169.CrossRefGoogle Scholar
  7. 7.
    Attia, H., Karraya, N., Rabhi, M., Lachaal, M. (2008) Salt-imposed restrictions on the uptake of macro elements by roots of Arabidopsis thaliana. Act. Physiol. Plant. 30, 723–727.CrossRefGoogle Scholar
  8. 8.
    Attia, H., Arnaud, N., Karraya, N., Lachaal, M. (2008) Long-term effects of mild salt stress on growth, ion accumulation and superoxide dismutase expression of Arabidopsis rosette leaves. Physiol. Plant 132, 293–305.CrossRefPubMedGoogle Scholar
  9. 9.
    Beadle, C. L. (1993) Growth analysis. 36-16. In: Hall, D. C., Scurlock, J. M. O., Bolhar-Nordenkampf H. R., Leegod, R. C. Long, S. P. (eds) Photosynthesis and production in a changing environment, A. field and laboratory manual, London.Google Scholar
  10. 10.
    Bhardwaj, N. V., Sharma, M. K. (2005) Genetic parameters and character association in tomato. Bangladesh. J. Agric. Res. 30, 49–56.Google Scholar
  11. 11.
    Bolarin, M. C., Perez-Alfocea, E., Cano, E. A., Estan, M. T., Caro, M. (1993) Growth, fruit yield, and ion concentration in tomato genotypes after pre-emergence and post-emergence salt treatments. J. Am. Soc. Hortic. Sci. 118, 655–660.CrossRefGoogle Scholar
  12. 12.
    Bradford, M. M. (1976) Arapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.Google Scholar
  13. 13.
    Chance, B., Maehly, S. K. (1955) Assay of catalase and peroxidases. Meth. Enzymol. 2, 764–775.CrossRefGoogle Scholar
  14. 14.
    Cuartero, J., Bolarin, M. C., Asins, M. J., Moreno, V. (2006) Increasing salt tolerance in the tomato. J. Exp. Bot. 5, 1045–1058.CrossRefGoogle Scholar
  15. 15.
    Delf, E. M. (1912) Transpiration in succulent plants. Arm. Bot. 26, 409–140.Google Scholar
  16. 16.
    Demidchik, V., Maathuis, F. J. M. (2007) Physiological roles of non selective cation channels in plants: from salt stress to signaling and development. New Phytol. 175, 387–104.CrossRefPubMedGoogle Scholar
  17. 17.
    Ding, M., Hou, P., Shen, X., Wang, M., Deng, S., Sun, J., Xiao, E., Wang, R., Zhou, X., Lu, C., Zhang, D., Zheng, X., Hu, Z., Chen, S. (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant. Mol. Biol. 73, 251–269.CrossRefPubMedGoogle Scholar
  18. 18.
    Dionisio-Sese, M. L., Tolbita, S. (1999) Antioxidative responses of shoots and roots of wheat increasing NaCl concentration. J. Plant. Physiol. 155, 274–280.CrossRefGoogle Scholar
  19. 19.
    Eryilmaz, F. (2006) The relationships between salt stress and anthocyanin content in higher plants. Biotechnol. Biotechnol. Equip. 20, 47–52.CrossRefGoogle Scholar
  20. 20.
    Eshed, Y., Zamir, D. (1995) The introgression-line (IL) population of S. pennellii in a processing-tomato variety (M82) is an efficient tool for identification and mapping of QTL. Genetics 141, 1147–1162.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Eshed, Y., Zamir, D. (1994) Agenomic library of Lycopersicon pennellii ini. esculentum: Atool for fine mapping of genes. Euphytica 79, 175–179.CrossRefGoogle Scholar
  22. 22.
    Eshed, Y., Gera, G., Zamir, D. (1996) A. genome-wide search for wild-species alleles that increase horticultural yield of processing tomatoes. 3, 877–886.Google Scholar
  23. 23.
    Foolad, M. R. (2004) Recent advances in genetics of salt tolerance in tomato. Plant Cell. Tissue. Organ. Cult. 76, 101–119.CrossRefGoogle Scholar
  24. 24.
    Foolad, M. R. (2007) Genome mapping and molecular breeding of tomato. Int. J. Plant Genomics 2007, 52. pp.Google Scholar
  25. 25.
    Frary, A., Keles, D., Pinar, H., Gol, D., Doganlar, S. (2011) NaCl tolerance in Lycopersiconpennellii introgression lines: QTL related to physiological responses. Biol. Plant 55, 461–168.CrossRefGoogle Scholar
  26. 26.
    Frary, A., Göl, D., Keles, D., Ökmen, B., Pinar, H., Sigva, Ö. H., Yemenicioglu, A., Doganlar, S. (2010) Salt tolerance in Solanum pennellii: antioxidant response and related QTL. BMC Plant. Biol. 10, 58. pp.Google Scholar
  27. 27.
    Fridman, E., Liu, Y. S., Carmel-Goren, L., Gur, A., Shoresh, M., Pleban, T., Eshed, Y., Zamir, D. (2002) Two tightly linked QTLs modify tomato sugar content via different physiological pathways. Mol. Genet. Genomics 266, 821–826.CrossRefPubMedGoogle Scholar
  28. 28.
    Gomez-Mestre, I., Alexander, P. R., Wiens, J. J. (2012) Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66, 1558–5646.CrossRefGoogle Scholar
  29. 29.
    Haydar, A., Mandal, M. A., Ahmed, M. B., Hannan, M. M., Karim, R. (2007) Studies on genetic variability and interrelationship among different traits in tomato (Lycopesicon esculantum Mill.). MiddleEastJ. Sci. Res. 2, 139–142.Google Scholar
  30. 30.
    Heath, R. L., Packer, L. (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125, 189–198.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hoagland, D., Arnon, D. I. (1950) The water culture method for growing plants without soil. California. Agricultural Experiment Station.Google Scholar
  32. 32.
    Juan, M. M., Rivero, L. R., Juan, M. R. (2005) Evaluation of some nutritional and biochemical indicators in selecting salt-resistant tomato cultivars. Environ. Exp. Bot. 54, 193–201.CrossRefGoogle Scholar
  33. 33.
    Kennedy, B. F., De Fillippis, L. F. (1999) Physiological and oxidative response to NaCl of the salt tolerant Grevillea ilicifolia and the salt sensitive Grevillea arenaria. J. Plant. Physiol. 155, 746–754.CrossRefGoogle Scholar
  34. 34.
    Koji, Y., Shiro, M., Michio, K., Mitsutaka, T., Hiroshi, M. (2009) Antioxidant capacity and damages caused by salinity stress in apical and basal regions of rice leaf. Plant Prod. Sci. 12, 319–326.CrossRefGoogle Scholar
  35. 35.
    Liang, Y. C. (1999) Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant. Soil. 209, 217–224.CrossRefGoogle Scholar
  36. 36.
    Lichtenthaler, H. K. (1988) In Vivo Chlorophyll Fluorescence as a Tool for Stress Detection in Plants. Applications of Chlorophyll Fluorescene in Photosynthesis Research, Stress Physiology Hydrobiology and Remote Sensing. 129–142.CrossRefGoogle Scholar
  37. 37.
    Lieberman, M., Segev, O., Gilboa, N., Lalazar, A., Levin, I. (2004) The tomato homolog of the gene encoding UV damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. Theor. Appl. Genet. 108, 1574–1581.CrossRefPubMedGoogle Scholar
  38. 38.
    Meloni, D. A., Oliva, M. A., Martinez, C. A., Cambraia, J. (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 49, 69–76.CrossRefGoogle Scholar
  39. 39.
    Mittova, V., Guy, M., Tal, M., Volokita, M. (2002) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: increased activities of antioxidant enzymes in root plastids. Free Radic. Res. 36, 195–202.CrossRefPubMedGoogle Scholar
  40. 40.
    Mittova, V., Tal, M., Volokita, M., Guy, M. (2002). Salt stress induces up-regulation of an efficiënt chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol. Plant. 115, 393–100.CrossRefPubMedGoogle Scholar
  41. 41.
    Munns, R., Termaat, A. (1986) Whole-plant responses to salinity. Aust. J. Plant Physiol. 13, 143–160.Google Scholar
  42. 42.
    Munns, R., Tester, M. (2008) Mechanisms of Salinity Tolerance. Plant. Biol. 59, 651–681.CrossRefGoogle Scholar
  43. 43.
    Murray, J. R., Hackett, W. P. (1998) Leaf anthocyanin content changes in Zea mays L. grown at low temperature: significance for the relationship between the quantum yield of PSII and the apparent quantum yield of C02 assimilation. Photosyn. Res. 58, 213–219.CrossRefGoogle Scholar
  44. 44.
    Nakano, Y., Asada, K. (1981) Hydrogen peroxide in scavenged by ascorbate-specific peroxidise in spinach chloroplast. Plant. Cell. Physiol. 22, 867–880.Google Scholar
  45. 45.
    Oztekin, G. B., Tuzel, Y. (2011) Comparative Salinity Responses Among Tomato Genotypes and Rootstocks. Pak. J. Bot. 43, 2665–2672.Google Scholar
  46. 46.
    Ozturk, L., Demir, Y., Unlukara, A., Karatas, I., Kurunc, A., Duzdemir, O. (2012) Effects of long-term salt stress on antioxidant system, chlorophyll and proline contents in pea leaves Rom. Biotechnol Lett. 17, 7227–7236.Google Scholar
  47. 47.
    Panda, S. K. (2001) Response of green gram seeds under salinity stress. IndianJ. Plant. Physiol. 6, 438–140.Google Scholar
  48. 48.
    Parida, A. K., Das, A. B. (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Sof. 60, 324–349.CrossRefGoogle Scholar
  49. 49.
    Peralta, I. E., Spooner, D. M. (2005). Morphological characterization and relationships of wild tomatoes (Solanum L. Section Lycopersicon): A Festschrift for William G., D’Arcy T. B., Croat V. C., Hollowell, R. C., Keating, M. Botanical Garden Press. 104, 227–257.Google Scholar
  50. 50.
    Perez-Alfocea, F., Estan, M. T., Caro, M., Bolarin, M. C. (1993) Response of tomato cultivars to salinity. Plant. Soil. 150, 203–211.CrossRefGoogle Scholar
  51. 51.
    Rajamane, N. N., Gaikwad, D. K. (2014) Effect of sodium chloride stress on polyphenol, flavonoid, anthocyanins contents and Lipid peroxidation of leaf Iets of Simarouba glauca. Indian J. Pharm. Educ.Res. 1, 2350–1138.Google Scholar
  52. 52.
    Rao, M. V. (1992) Cellular detoxifying mechanisms determine age dependent injury in tropical plants exposed to SO. J. Plant. Physiol. 140, 733–740.CrossRefGoogle Scholar
  53. 53.
    Rodriguez-Rosales, M. P., Kerkeb, L., Bueno, R., Donaire, J. P. (1999) Changes induced by NaCl in lipid content and composition, lipoxygenase, plasma membrane H+-ATPase and antioxidant enzyme activities of tomato (Lycopersicon esculentum Mill.) calli. Plant. Sci. 143, 143–150.CrossRefGoogle Scholar
  54. 54.
    Rus, A. M., Estan, M. T., Gisbert, C., Garcia-Sogo, B., Serrano, R., Caro, M., Moreno, V., Bolarin, M. C. (2001) Expressing the yeast HAL1 gene in tomato increases fruit yield and enhances K+/Na+ selectivity under salt stress. Plant. Cell. Environ. 24, 875–880.CrossRefGoogle Scholar
  55. 55.
    Saeed, M., Saleem, F., Zakria, M., Anjum, S. A., Shakeel, A., Saeed, N. (2011) Genetic variability of NaCl tolerance in tomato. Genet. Mol. Res. 10, 1371–1382.CrossRefPubMedGoogle Scholar
  56. 56.
    Sairam, R. K., Rao, K. V., Srivastava, G. C. (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant. Sci. 163, 1037–1046.CrossRefGoogle Scholar
  57. 57.
    Saranga, Y., Zamir, D., Marani, A., Rudich, J. (1991) Breeding tomatoes for salt tolerance - field-evaluation of Lycopersicon germplasm for yield and dry-matter production. J. Am. Soc. Hort. Sci. 116, 1067–1071.CrossRefGoogle Scholar
  58. 58.
    Savithri, H. S., Sudhakar, C. (1999) Total peroxidase activity and peroxidase isoforms as modified by salt stress in two cultivars of foxtail millet with differential salt resistance. Plant. Sci. 141, 1–9.CrossRefGoogle Scholar
  59. 59.
    Shalata, A., Tal, M. (1998) The effect of salt stress on lipid peroxidation and antioxidants in the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol. Plant. 104, 169–174.CrossRefGoogle Scholar
  60. 60.
    Sharifova, S., Mehdiyeva, S., Theodorikas, K., Roubos, K. (2013) Assessment of genetic diversity in cultivated tomato (Solanum lycopersicum L.) genotypes using raped primers. J. Hortte. Res. 21, 83–89.Google Scholar
  61. 61.
    Stevens, R., Buret, M., Duffé, P., Garchery, C., Baldet, P., Rothan, C., Causse, M. (2007) Candidate Genes and Quantitative Trait Loei Affecting Fruit Ascorbic Acid Content in Three Tomato Populations. Plant. Physiol. 143, 1943–1953.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Stevens, R., Buret, M., Garchery, C., Carretero, Y., Causse, M. (2007) Technique for rapid, small-scale analysis of vitamin C. levels in fruit and application to a tomato mutant collection. J. Agric. Food Chem. 54, 6159–6165.CrossRefGoogle Scholar
  63. 63.
    Stevens, R., Page, D., Gouble, B., Garchery, C., Zamir, D., Causse, M. (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant. Cell. Environ. 31, 1086–1096.CrossRefPubMedGoogle Scholar
  64. 64.
    Taha, R., Mills, D., Heimer, Y., Tal, M. (2000) The relation between low K+/Na+ ratio and salt-tolerance in the wild tomato species Lycopersiconpennellii. J. Plant Physiol. 157, 59–64.CrossRefGoogle Scholar
  65. 65.
    Tal, M., Shannon, M. C. (1983) Salt tolerance in the wild relatives of the cultivated tomato: Responses of Lycopersicon esculentum. L. cheesmanii, L. peruvianum, solanum pennellii and F1 hybrids to high salinity. Aust. J. Plant Physiol. 10, 109–117.Google Scholar
  66. 66.
    Turhan, A., Seniz, V. (2010) Salt tolerance of some tomato genotypes grown in Turkey. J. Food. Agri. Environ. 8, 332–339.Google Scholar
  67. 67.
    Wang, W., Vinocur, B., Altman, A. (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Witkoswski, E. T. F., Lamont, B. B. (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 84, 362–370.Google Scholar
  69. 69.
    Xiong, L., Zhu, J. K. (2002) Salt tolerance. The Arabidopsis Book. American Society of Plant Biologists. Rockville.Google Scholar
  70. 70.
    Yagi, K. (1976) A. simple fluorometric assay for lipoperoxide in blood plasma. Biochem. Med. 15, 212–216.CrossRefPubMedGoogle Scholar
  71. 71.
    Yokas, I., Tuna, A. L., Bürün, B., Altunlu, H., Altan, F., Kaya, C. (2008) Response of the tomato (Lycopersicon esculentum Mill.) plant to exposure to different salt forms and rates. Turk. J. Agric. For. 32, 319–329.Google Scholar

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© Akadémiai Kiadó Zrt. 2018

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Authors and Affiliations

  • Fedia Rebah
    • 1
    • 2
  • Chayma Ouhibi
    • 1
    Email author
  • K. H. Alamer
    • 3
  • Najoua Msilini
    • 1
  • Mouhiba Ben Nasri
    • 1
  • Rebecca Stevens
    • 2
  • Houneida Attia
    • 1
    • 3
  1. 1.Unité de Physiologie et Biochimie de la Réponse des Plantes aux Contraintes Abiotiques, Département de Biologie, Faculté des Sciences de TunisUniversité Tunis El ManarTunisTunisie
  2. 2.INRA, UR1052Génétique et Amélioration des Fruits et LégumesMontfavetFrance
  3. 3.Biology Department, Faculty of ScienceTaif UniversityKingdom of Saudi Arabia

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