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

Abstract

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.

References

  1. 1.

    Agarwal, S., Pandey, V. (2004) Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biol. Plant. 48, 555–560.

    CAS  Article  Google 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.

    PubMed  Google Scholar 

  3. 3.

    Aktas, H., Abak, K., Cakmak, I. (2006) Genotypic variation in the response of pepper to salinity. Sci. Hortte. 10, 260–266.

    Article  CAS  Google 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.

    Article  Google Scholar 

  5. 5.

    Ashraf M., Harris, P. J. C. (2004) Potential biochemical indicators of salinity tolerance in plants. Plant. Sci. 116, 3–16.

    Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  Google 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.

    CAS  Google Scholar 

  13. 13.

    Chance, B., Maehly, S. K. (1955) Assay of catalase and peroxidases. Meth. Enzymol. 2, 764–775.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  Google Scholar 

  19. 19.

    Eryilmaz, F. (2006) The relationships between salt stress and anthocyanin content in higher plants. Biotechnol. Biotechnol. Equip. 20, 47–52.

    Article  CAS  Google 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.

    CAS  PubMed  PubMed Central  Google 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.

    Article  CAS  Google 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.

    Article  CAS  Google Scholar 

  24. 24.

    Foolad, M. R. (2007) Genome mapping and molecular breeding of tomato. Int. J. Plant Genomics 2007, 52. pp.

  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.

    Article  CAS  Google 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.

  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.

    Article  CAS  PubMed  Google 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.

    Article  Google 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.

    Article  CAS  PubMed  PubMed Central  Google 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.

    Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  CAS  Google 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.

    Book  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  Google 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.

    Article  Google 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.

    CAS  Google Scholar 

  45. 45.

    Oztekin, G. B., Tuzel, Y. (2011) Comparative Salinity Responses Among Tomato Genotypes and Rootstocks. Pak. J. Bot. 43, 2665–2672.

    CAS  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.

    CAS  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.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  PubMed Central  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  PubMed Central  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  Google Scholar 

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Correspondence to Chayma Ouhibi.

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Rebah, F., Ouhibi, C., Alamer, K.H. et al. Comparison of the Responses to NaCl Stress of Three Tomato Introgression Lines. BIOLOGIA FUTURA 69, 464–480 (2018). https://doi.org/10.1556/018.69.2018.4.8

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Keywords

  • Antioxidant enzymes
  • ascorbate
  • introgression lines
  • salinity
  • tomatoes
  • variability