Photosynthetica 2018, 56(3):750-762 | DOI: 10.1007/s11099-017-0727-y

Ameliorative role of salicylic acid and spermidine in the presence of excess salt in Lycopersicon esculentum

Q. Fariduddin1,*, T. A. Khan1, M. Yusuf1, S. T. Aafaqee1, R. R. A. E. Khalil2
1 Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh, India
2 Department of Botany, Faculty of Science, Benha University, Benha, Egypt

Salicylic acid (SA) and polyamines (PA) are widely used to overcome various abiotic stresses including salt (NaCl) stress in plants. In the present investigation, co-application efficacies of SA and PA on the salt stress (200 mM NaCl) were evaluated in Lycopersicon esculentum. After transplantation, at 10-d stage, seedlings were exposed to NaCl through soil and then allowed to grow till 30-d stage. At 31-d stage of growth, plants were sprayed with double distilled water (control) or spermidine (1.0 mM) and/or SA (10-5 M). The salt stress significantly reduced the growth, gas-exchange parameters, but increased antioxidant enzymes and proline content in the leaves. Moreover, the loss caused by salt stress was successfully restored by the following treatment of spermidine and SA.

Additional key words: abiotic stress; antioxidant; photosynthesis; proline

Received: October 5, 2016; Accepted: March 6, 2017; Prepublished online: September 1, 2018; Published: August 1, 2018  Show citation

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Fariduddin, Q., Khan, T.A., Yusuf, M., Aafaqee, S.T., & Khalil, R.R.A.E. (2018). Ameliorative role of salicylic acid and spermidine in the presence of excess salt in Lycopersicon esculentum. Photosynthetica56(3), 750-762. doi: 10.1007/s11099-017-0727-y
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References

  1. Agarwal S., Sairam F.K., Srivastava G.C. et al.: Role of ABA, salicylic acid, calcium and hydrogen peroxide on antioxidant enzymes induction in wheat seedlings.-Plant Sci. 169: 559-570, 2005. Go to original source...
  2. Ahmad P., Azooz M.M., Prasad M.N.V.: Ecophysiology and Responses of Plants under Salt Stress. Pp. 149-168. Springer Science & Business Media, New York 2012b. Go to original source...
  3. Ahmad P., Hakeem K.U.R., Kumar A. et al.: Salt induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.).-Afr. J. Biotechnol. 11: 2694-2703, 2012a. Go to original source...
  4. Ahmad P., Jaleel C.A., Azooz M.M. et al.: Generation of ROS and non-enzymatic antioxidants during abiotic stress in plants.-Bot. Res. Intern. 2: 11-20, 2009.
  5. Alarcon J.J., Sanchez-Blanco M.J., Bolarin M.C. et al.: Water relation and osmotic adjustment in Lycopersicum esculentum and L. pinnelli during short-term of salt exposure and recovery.-Physiol. Plantarum 89: 441-447, 1993. Go to original source...
  6. Al-Hakimi A.M.A., Hamada A.M.: Counteraction of salinity stress on wheat plants by grain soaking in ascorbic acid, thiamin or sodium salicylate.-Biol. Plantarum 44: 253-261, 2001. Go to original source...
  7. Ali Q., Athar H.R., Ashraf M.: Modulation of growth, photosynthetic capacity and water relations in salt stressed wheat plants by exogenously applied 24-epibrassinolide.-Plant Growth Regul. 56: 107-116, 2008. Go to original source...
  8. Mohanty P., Saradhi P.P.: Effect of sodium chloride on primary photochemical activities in cotyledonary leaves of Brassica juncea.-Biochem. Physiol. 188: 1-12, 1992. Go to original source...
  9. Amor N.B., Jiménez A., Megdiche W. et al.: Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima.-Physiol. Plantarum 126: 446-457, 2006. Go to original source...
  10. Amri E., Shahsavar A.: Response of lime seedlings (Citrus aurantifolia L.) to exogenous spermidine treatments under drought stress.-Aust. J. Basic Appl. Sci. 4: 4483-4489, 2010.
  11. Arfan M., Athar H.R., Ashraf M.: Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress?-J. Plant Physiol. 164: 685-694, 2007. Go to original source...
  12. Ashraf M., Akram N.A., Arteca R.N. et al.: The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance.-Crit. Rev. Plant Sci. 29: 162-190, 2010. Go to original source...
  13. Ashraf M., Athar H.R., Harris P.J.C. et al.: Some prospective strategies for improving crop salt tolerance.-Adv. Agron. 97: 45-110, 2008. Go to original source...
  14. Athwal G.S., Huber S.C.: Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase.-Plant J. 29: 119-129, 2002. Go to original source...
  15. Bais H.P., Ravishankar G.A.: Role of polyamines in the ontogeny of plants and their biotechnological applications.-Plant Cell Tiss. Org. 69: 1-34, 2002. Go to original source...
  16. Bates L.S., Waldeen R.P., Teare I.D.: Rapid determination of free proline for water stress studies.-Plant Soil 39: 205-207, 1973. Go to original source...
  17. Beauchamp C.O., Fridovich I.: Superoxide dismutase: improved assays and assays applicable to acrylamide gels.-Anal. Biochem. 44: 276-287, 1971. Go to original source...
  18. Belkheiri O., Mulas M.: The effects of salt stress on growth, water relations and ion accumulation in two halophyte Atriplex species.-Environ. Exp. Bot. 86: 17-28, 2013. Go to original source...
  19. Benavides M.P., Aizencang G., Tomaro M.L.: Polyamines in Helianthus annuus L. during germination under salt stress.-J. Plant Growth Regul. 16: 205-211, 1997. Go to original source...
  20. Besford R.T., Richardson C.M., Campos J.L. et al.: Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves.-Planta 189: 201-206, 1993. Go to original source...
  21. Bethkey P.C., Drew M.C.: Stomatal and non-stomatal components to inhibition of photosynthesis in leaves of Capsicum annum during progressive exposure to NaCl salinity.-Plant Physiol. 99: 219-226, 1992. Go to original source...
  22. Bouchereau A., Azis A., Larher F. et al.: Polyamines and environmental challenges: recent development.-Plant Sci. 140: 103-125, 1999. Go to original source...
  23. Campbell H.W.: Nitrate reductase structure, function and regulation: Bridging the gap between biochemistry and physiology.-Annu. Rev. Plant Phys. 50: 277-303, 1999. Go to original source...
  24. Carswell G.K., Johnson C.M, Shillito R.D. et al.: O-acetylsalicylic acid promotes colony formation from protoplasts of an elite maize inbred.-Plant Cell Rep. 8: 282-284, 1989. Go to original source...
  25. Chance B., Maehly A.C.: Assay of catalase and peroxidases.-Method. Enzymol. 2: 764-775, 1955. Go to original source...
  26. Chandra A., Bhatt R.K.: Biochemical and physiological response to salicylic acid in relation to the systemic acquired resistance.-Photosynthetica 35: 255-258, 1998. Go to original source...
  27. Chen C., Dickman M.B.: Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii.-P. Natl. Acad. Sci. USA 102: 3459-3464, 2005. Go to original source...
  28. Childs A.C., Mehta D.J., Germer E.W.: Polyamine-dependent gene expression.-Cell Mol. Life. Sci. 60: 1394-1406, 2003. Go to original source...
  29. Cohen S., Frank E., Doyle W.J. et al.: Types of stressors that increase susceptibility to the common cold in healthy adults.-Health Psychol. 17: 214-223, 1998. Go to original source...
  30. DeLacerda C.F., Cambraia J., Oliva M.A. et al.: Changes in growth and in solute concentrations in sorghum leaves and roots during salt stress recovery.-Environ. Exp. Bot. 54: 69-76, 2005. Go to original source...
  31. Duan J.J., Li J., Guo S.R. et al.: Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance.-J. Plant Physiol. 165: 1620-1635, 2008. Go to original source...
  32. Dwivedi R.S., Randhawa N.S.: Evolution of a rapid test for the hidden hunger of zinc in plants.-Plant Soil 40: 445-451, 1974. Go to original source...
  33. Fariduddin Q., Hayat S., Ahmad A.: Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity and seed yield in Brassica juncea.-Photosynthetica 41: 281-284, 2003. Go to original source...
  34. Feng G., Zhang F.S., Li X.L. et al.: Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots.-Mycorrhiza 12: 185-190, 2002. Go to original source...
  35. Geissler N., Hussin S., Koyro H.W.: Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L.-J. Exp. Bot. 60: 137-151, 2009. Go to original source...
  36. Gil-Amado J.A., Gomez-Jimenez M.C.: Regulation of polyamine metabolism and biosynthetic gene expression during olive mature-fruit abscission.-Planta 235: 1221-1237, 2012. Go to original source...
  37. Groppa M.D., Benavides M.P., Tomaro M.L.: Polyamine metabolism in sunflower and wheat leaf discs under cadmium or copper stress.-Plant Sci. 164: 293-299, 2003. Go to original source...
  38. Groppa M.D., Benavides M.P.: Polyamines and abiotic stress: recent advances.-Amino Acids 34: 35-45, 2008. Go to original source...
  39. Hameed M., Nawaz T., Ashraf M. et al.: Physioanatomical adaptations in response to salt stress in Sporobolus arabicus (Poaceae) from the Salt Range, Pakistan.-Turk. J. Bot. 37: 715-724, 2013. Go to original source...
  40. Hayat S., Fariduddin Q., Ali B. et al.: Effect of salicylic acid on growth and enzyme activities of wheat seedlings.-Acta Agron. Hung. 53: 433-437, 2005. Go to original source...
  41. Hayat S., Hasan S.A., Yusuf M. et al.: Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata.-Environ. Exp. Bot. 69: 105-112, 2010. Go to original source...
  42. Hayat S., Maheshwari P., Wani A.S. et al.: Comparative effect of homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L.-Plant Physiol. Bioch. 53: 61-68, 2012. Go to original source...
  43. He Y.L., Liu Y., Chen Q. et al.: Thermotolerance related to antioxidation induced by salicylic acid and heat acclimation in tall fescue seedlings.-J. Plant Phys. 28: 89-95, 2002.
  44. Hopkins W.G., Hüner N.P.A.: Introduction to Plant Physiology. Pp. 503. John Wiley & Sons, Inc., Hoboken 2009.
  45. Hussain S.S., Ali M., Ahmad M. et al.: Polyamines: natural and engineered abiotic and biotic stress tolerance in plants.-Biotechnol. Adv. 29: 300-311, 2011. Go to original source...
  46. Hussein M.M., Balbaa L.K., Gaballah M.S.: Salicylic acid and salinity effects on growth of maize plants.-J. Agric. Biol. Sci. 3: 321-328, 2007.
  47. Idrees M., Naeem M., Khan M.N. et al.: Alleviation of salt stress in lemongrass by salicylic acid.-Protoplasma 249: 709-720, 2012. Go to original source...
  48. Iyengar E.R.R., Reddy M.P.: Photosynthesis in highly salt tolerant plants.-In: Pessarakli M. (ed.): Handbook of Photosynthesis. Pp. 897-909. Marcel Dekker, New York 1996.
  49. Jaworski E.G.: Nitrate reductase assay in intact plant tissues.-Biochem. Biophys. Res. Co. 43: 1274-1279, 1971. Go to original source...
  50. Jayakannan M., Bose J., Babourina O. et al.: Salicylic acid in plant salinity stress signalling and tolerance.-Plant Growth Regul. 76: 25-40, 2015. Go to original source...
  51. Karim M.A., Fracheboud Y., Stamp P.: Photosynthetic activity of developing leaves of Zea mays is less affected by heat stress than of developed leaves.-Physiol. Plantarum 105: 685-693, 1999. Go to original source...
  52. Kausar F., Shahbaz M., Ashraf M. et al.: Protective role of foliar applied nitric oxide in Triticum aestivum under saline stress.-Turk. J. Bot. 37: 1155-1165, 2013. Go to original source...
  53. Khan M.H., Panda S.K.: Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaClsalinity stress.-Acta Physiol. Plant. 30: 81-89, 2008. Go to original source...
  54. Khodary S.E.A.: Effect of salicylic acid on growth, photosynthesis and carbohydrate metabolism in salt stressed maize plants.-Int. J. Agric. Biol. 6: 5-8, 2004.
  55. Kim N.H., Kim B.S., Hwang B.K.: Pepper arginine decarboxylase is required for polyamine and gamma-aminobutyric acid signaling in cell death and defense response.-Plant Physiol. 162: 2067-2083, 2013. Go to original source...
  56. Koca M., Bor M., Özdemir F. et al.: The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of Sesame cultivars.-Environ. Exp. Bot. 60: 344-351, 2007. Go to original source...
  57. Krishnamurthy R.: Amelioration of salinity effect in salt tolerant rice (Oryza sativa L.) by foliar application of putrescine.-Plant Cell Physiol. 32: 699-703, 1991. Go to original source...
  58. Lakra N., Mishra S.N., Singh D.B. et al.: Exogenous putrescine effect on cation concentration in leaf of Brassica juncea seedlings subjected to Cd and Pb along with salinity stress.-J. Environ. Biol. 27: 263-269, 2006.
  59. Lee J., Sperandio V., Frantz D.E. et al.: An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae.-J. Biol. Chem. 284: 9899-9907, 2009. Go to original source...
  60. Li S., Jin H., Zhang Q.: The effect of exogenous spermidine concentration on polyamine metabolism and salt tolerance in Zoysiagrass (Zoysia japonica Steud) subjected to short-term salinity stress.-Front. Plant Sci. 7: 1221, 2016. Go to original source...
  61. Li T.X., Yue Z., Hua L. et al.: Stable expression of Arabidopsis vacuolar Na+ /H+ antiporter gene AtNHX1 and salt tolerance in transgenic soybean for over six generations.-Chinese Sci. Bull. 55: 1127-1134, 2010. Go to original source...
  62. Liu J., Zhou Y.F., Zhang W.H. et al.: Effects of exogenous polyamines on chloroplast-bound polymine content and photosynthesis of corn suffering salt stress.-Acta Bot. Boreal. 26: 254-258, 2006.
  63. Manaa A., Gharbi E., Mimouni H. et al.: Simultaneous application of salicylic acid and calcium improves salt tolerance in two contrasting tomato (Solanum lycopersicum) cultivars.-South Afr. J. Bot. 95: 32-39, 2014. Go to original source...
  64. Mateo A., Mühlenbock P., Rustérucci C. et al.: Lesion simulating disease 1 is required for acclimation to conditions that promote excess excitation energy.-Plant Physiol. 136: 2818-2830, 2004. Go to original source...
  65. Melotto M., Underwood W., Koczan J. et al.: Plant stomata function in innate immunity against bacterial invasion.-Cell 126: 969-980, 2006. Go to original source...
  66. Metwally A., Finkmemeier I., Georgi M. et al.: Salicylic acid alleviates the cadmium toxcity in barley seedlings.-Plant Physiol. 132: 272-281, 2003. Go to original source...
  67. Mimouni H., Wasti S., Manaa A. et al.: Does salicylic acid (SA) improve tolerance to salt stress in plants? a study of SA effects on tomato plant growth, water dynamics, photosynthesis, and biochemical parameters.-OMICS 20: 180-190, 2016. Go to original source...
  68. Mir B.A., Khan T.A., Fariduddin Q.: 24-epibrassinolide and spermidine modulate photosynthesis and antioxidant systems in Vigna radiata under salt and zinc stress.-Int. J. Adv. Res. 3: 592-608, 2015.
  69. Mittler R.: Oxidative stress, antioxidants and stress tolerance.-Trends Plant Sci. 7: 405-410, 2002. Go to original source...
  70. Moharekar S.T., Lokhande S.D., Hara T. et al.: Effect of salicylic acid on chlorophyll and carotenoid contents of wheat and moong seedlings.-Photosynthetica 41: 315-317, 2003. Go to original source...
  71. Munné-Bosch S.M., Peñuelas J., Llusià J.: A deficiency in salicylic acid alters isoprenoid accumulation in water stressed transgenic Arabidopsis plants.-Plant Sci. 172: 756-762, 2007. Go to original source...
  72. Munns R.: Genes and salt tolerance: bringing them together.-New Phytol. 167: 645-663, 2005. Go to original source...
  73. Murphy K.S.T., Kinsey S.T., Durako M.J.: Physiological effects of short term salinity changes on Ruppia maritima.-Aquat Bot. 75: 293-309, 2003. Go to original source...
  74. Mutlu F., Bozcuk S.: Effects of salinity on the contents of polyamines and some other compounds in sunflower plants differing in salt tolerance.-Russ. J. Plant Physl+ 52: 29-34, 2005. Go to original source...
  75. Najafian S., Khoshkhui M., Tavallali V. et al.: Effect of salicylic acid and salinity in thyme (Thymus vulgaris L.): Investigation on changes in gas exchange, water relations, and membrane stabilization and biomass accumulation.-Aust. J. Basic Appl. Sci. 3: 2620-2626, 2009.
  76. Ouerghi Z., Cornic G., Roudani M. et al.: Effect of NaCl on the photosynthesis of two wheat species differing in their sensitivity to salt stress.-J. Plant Physio. 156: 335-340, 2000. Go to original source...
  77. Pál M.E., Horváth T., Janda E. et al.: Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants.-Physiol. Plantarum 125: 356-364, 2005. Go to original source...
  78. Parashar A., Yusuf M., Fariduddin Q. et al.: Salicylic acid enhances antioxidant system in Brassica juncea grown under different levels of manganese.-Int. J. Biol. Macromol. 70: 551-558, 2014. Go to original source...
  79. Pirasteh-Anosheh H., Ranjbar G., Emam Y. et al.: Salicylic-acidinduced recovery ability in salt-stressed Hordeum vulgare plants.-Turk. J. Bot. 38: 112-121, 2014. Go to original source...
  80. Pothipongsa A., Jantaro S., Incharoensakdi A.: Polyamines induced by osmotic stress protect Synechocystis sp. PCC 6803 cells and arginine decarboxylase transcripts against UV-B radiation.-Appl. Biochem. Biotech. 168: 1476-1488, 2012. Go to original source...
  81. Qadir M., Quillé rou E., Nangia V. et al.: Economics of saltinduced land degradation and restoration.-Nat. Resour. Forum. 38: 282-295, 2014. Go to original source...
  82. Rady M.M.: Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress.-Sci. Hortic.-Amsterdam 129: 232-237, 2011. Go to original source...
  83. Rajjou L., Belghazi M., Huguet R. et al.: Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms.-Plant Physiol. 141: 910-923, 2006. Go to original source...
  84. Rider J.E., Hacker A., Mackintosh C.A et al.: Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide.-Amino Acids 33: 231-240, 2007. Go to original source...
  85. Rosales E.P., Iannone M.F., Groppa M.D. et al.: Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide.-Amino Acids 42: 857-865, 2012. Go to original source...
  86. Sekmen A.H., Turkan I, Tanyolac Z.O. et al.: Different antioxidant defense responses to salt stress during germination and vegetative stages of endemic halophyte Gypsophila oblanceolata Bark.-Environ. Exp. Bot. 77: 63-76, 2012. Go to original source...
  87. Sen G., Eryilmaz I.E., Ozakca D.: The effect of aluminium-stress and exogenous spermidine on chlorophyll degradation, glutathione reductase activity and the photosystem II D1 protein gene (psbA) transcript level in lichen Xanthoria parietina.-Phytochemistry 98: 54-59, 2014. Go to original source...
  88. Seneratna T., Touchell D., Bunn E. et al.: Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants.-Plant Growth Regul. 30: 157-161, 2000. Go to original source...
  89. Sheokand S., Kumari A., Sawhney V.: Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants.-Physiol. Mol. Biol. Plant. 14: 355-362, 2008. Go to original source...
  90. Silveira V., De Vita A.M., Macedo A.F. et al.: Morphological and polyamine content changes in embryogenic and nonembryogenic callus of sugarcane.-Plant Cell Tiss. Org. 114: 351-364, 2013. Go to original source...
  91. Singh B., Usha K.: Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress.-Plant Growth Regul. 39: 137-141, 2003. Go to original source...
  92. Slaymaker D.H., Navarre D.A., Clark D. et al.: The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response.-P. Natl. Acad. Sci. USA 99: 11640-11645, 2002. Go to original source...
  93. Soussi M., Ocañ a A., Lluch C.: Effect of salt stress growth, photosynthesis and nitrogen fixation in chick-(Cicer arietinum L.).-J. Exp. Bot. 49: 1329-1337, 1998. Go to original source...
  94. Strobel N.E., Kuc A.: Chemical and biological inducers of systemic acquired resistance to pathogens protect cucumber and tobacco from damage caused by paraquat and cupric chloride.-Phytopathology 85: 1306-1310, 1995. Go to original source...
  95. Sudhir P., Murthy S.D.S.: Effects of salt stress on basic processes of photosynthesis.-Photosynthetica 42: 481-486, 2004. Go to original source...
  96. Sullivan C.Y., Ross W.M.: Selecting the drought and heat resistance in grain sorghum.-In: Mussel H, Staples R.C. (ed.): Stress Physiology in Crop Plants. Pp. 263-281. John Wiley & Sons, Inc, New York 1979.
  97. Sung M.S., Chow T.J., Lee T.M.: Polyamine acclimation alleviates hypersalinity-induced oxidative stress in a marine green macroalga, Ulva fasciata, by modulation of antioxidative enzyme gene.-J. Phycol. 47: 538-547, 2011. Go to original source...
  98. Szabados L., Savouré A.: Proline: a multifunctional amino acid.-Trends Plant Sci. 15: 89-97, 2010. Go to original source...
  99. Szepesi A., Csiszár J., Bajkán S.Z. et al.: Role of salicylic acid pre-treatment on the acclimation of tomato plants to salt- and osmotic stress.-Acta Biol. Szeged 49: 123-125, 2005.
  100. Tabor C.W., Tabor H.: Polyamines.-Annu. Rev. Biochem. 5: 749-790, 1984. Go to original source...
  101. Tadayon M.R., Emam Y.: Physiological and morphological responses of two barley cultivars to salt stress and their correlation with grain yield.-Agric. Nat. Res. Sci. Tech. 11: 253-262, 2007.
  102. Tanou G., Filippou P., Belghazi M. et al.: Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress.-Plant J. 72: 585-599, 2012. Go to original source...
  103. Tanou G., Ziogas V., Belghazi M. et al.: Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress.-Plant Cell Environ. 37: 864-885, 2014. Go to original source...
  104. Tari I., Csiszár J., Szalai G. et al.: Acclimation of tomato plants to salinity stress after a salicylic acid pre-treatment.-Acta Biol. Szeged 46: 55-56, 2002.
  105. Tiburcio A.F., Kaur-Sawhney R., Galston A.W.: Polyamine metabolism.-In: Miflin B.J., Lea P.J. (ed.): Intermedatory Nitrogen Metabolism. The Biochem of Plants. Pp. 283-325. Academic Press, Cambridge 1990. Go to original source...
  106. Tisi A., Federico R., Moreno S. et al.: Perturbation of polyamine catabolism can strongly affect root development and xylem differentiation.-Plant Physiol. 157: 200-215, 2011. Go to original source...
  107. Unni S., Rao K.K.: Protein and lipopolysaccharide profiles of a salt-sensitive Rhizobium sp. and its exopolysaccharidedeficient mutant.-Soil Biol. Biochem. 33: 111-115, 2001. Go to original source...
  108. Uzunova A.N., Popova L.P.: Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants.-Photosynthetica 38: 243-250, 2000. Go to original source...
  109. Verslues P.E., Agarwal M., Katiyar-Agarwal S. et al.: Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.-Plant J. 45: 523-539, 2006. Go to original source...
  110. Wang M., Jiang W., Yu H.: Effects of exogenous epibrassinolide on photosynthetic characteristics in tomato (Lycopersicon esculentum Mill) seedlings under weak light stress.-J Agr. Food Chem. 8: 3642-3645, 2010. Go to original source...
  111. Wani A.S., Ahmad A., Hayat S. et al.: Is foliar spray of proline sufficient for mitigation of salt stress in Brassica juncea cultivars?-Environ. Sci. Pollut. R. 23: 13413-13423, 2016. Go to original source...
  112. Wani A.S., Ahmad A., Hayat S. et al.: Salt-induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea.-Saudi J. Biol. Sci. 20: 183-193, 2013. Go to original source...
  113. Wu X.X., Ding H.D., Zhu Z.W. et al.: Effects of 24-epibrassinolide on photosynthesis of eggplant (Solanum melongena L.) seedlings under salt stress.-Afr. J. Biotechnol. 11: 8665-8671, 2012. Go to original source...
  114. Xu G., Magen H., Tarchitzky J. et al.: Advances in chloride nutrition of plants.-Adv. Agr. 68: 97-150, 1999. Go to original source...
  115. Yamaguchi K., Takahashi Y., Berberich T. et al.: A protective role for the polyamine spermine against drought stress in Arabidopsis.-Biochem. Biophys. Res. Co. 352: 486-490, 2007. Go to original source...
  116. Yang W.J., Rich P.J., Axtell J.D. et al.: Genotypic variation for glycine betaine in Sorghum.-Crop Sci. 43: 162-169, 2003. Go to original source...
  117. Yusuf M., Hasan S.A., Ali B. et al.: Effect of salicylic acid on salinity induced changes in Brassica juncea.-J. Integr. Plant. Biol. 50: 1-4, 2008. Go to original source...
  118. Zheng C., Jiang D., Liu F. et al.: Effects of salt and water logging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat.-Plant Sci. 176: 575-582, 2009. Go to original source...