, Volume 56, Issue 4, pp 1313–1325 | Cite as

Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence, photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress

  • D. KhoshbakhtEmail author
  • M. R. Asghari
  • M. Haghighi
Original paper


The effects of exogenous sodium nitroprusside (SNP), as nitric oxide donor, and spermidine (Spd) on growth and photosynthetic characteristics of Bakraii seedlings (Citrus reticulata × Citrus limetta) were studied under NaCl stress. In citrus plants, SNP- and Spd-induced growth improvement was found to be associated with reduced electrolyte leakage, malondialdehyde, hydrogen peroxide content, and leaf Na+ and Cl concentration. However, we found increased leaf Ca2+, Mg2+, and K+ concentrations, relative water content, chlorophyll fluorescence parameters, antioxidant enzyme activities, such as ascorbate peroxidase, catalase, superoxide dismutase and peroxidase, as well as higher photosynthetic rate, intercellular CO2 concentration, stomatal conductance, and transpiration rate under saline regime. Foliar application of SNP and Spd alone mitigated the adverse effect of salinity, while the combined application proved to be even more effective.

Additional key words

abiotic stress biomass gas exchange oxidative stress photosystem II efficiency 



ascorbate peroxidase


atmospheric CO2 concentration


intercellular CO2 concentration






transpiration rate


electrolyte leakage


minimal fluorescence yield of the dark-adapted state


maximal fluorescence yield of the dark-adapted state


variable fluorescence


maximum photochemical efficiency of PSII


stomatal conductance


number of leaves per plant




nonphotochemical quenching








net photosynthetic rate


photochemical quenching


reactive oxygen species


relative water content


length of shoot


sodium nitroprusside


superoxide dismutase


salinity stress






total plant dry mass


total plant fresh mass


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aebi H.: Catalase in vitro.–Methods Enzymol. 105: 121–126, 1984.CrossRefPubMedGoogle Scholar
  2. Alcázar R., Altabella T., Marco F. et al.: Polyamines: molecules withregulatory functions in plant abiotic stress tolerance.–Planta 231: 1237–1249, 2010.CrossRefPubMedGoogle Scholar
  3. Almansa M.S., Hernandez J.A., Jimenez A. et al.: Effect of salt stress on the superoxide dismutase activity in leaves of Citrus limonum in different rootstock-scion combinations.–Biol. Plantarum 45: 545–549, 2002.CrossRefGoogle Scholar
  4. Anjum M.A.: Effect of exogenously applied spermidine on growth and physiology of citrus rootstock Troyer citrange under saline conditions.–Turk. J. Agric. For. 35: 43–55, 2009.Google Scholar
  5. Anjum M.A.: Effect of NaCl concentration in irrigation water on growth and polyamine metabolism in two citrus rootstocks with different levels of salinity tolerance.–Acta Physiol. Plant 30: 43–52, 2007.CrossRefGoogle Scholar
  6. Arasimowicz M., Floryszak-Wieczorek J.: Nitric oxide as a bioactive signaling molecule in plant stress responses.–Plant Sci. 172: 876–887, 2007.CrossRefGoogle Scholar
  7. Arbona V., Aurelio J., Domingo J.: Carbohydrate depletion in roots and leaves of salt-stressed potted Citrus clementina L.–Plant Growth Regul. 46: 153–160, 2005.CrossRefGoogle Scholar
  8. Barrs H.D., Weatherley P.E.: A re-examination of the relative turgidity technique for estimating water deficits in leaves.–Aust. J. Biol. Sci. 15: 413–428, 1962.CrossRefGoogle Scholar
  9. Bates L., Waldren P.P., Teare J.D.: Rapid determination of the free proline of water stress studies.–Plant Soil 39: 205–207, 1973.CrossRefGoogle Scholar
  10. Beauchamp C., Fridovich I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.–Anal. Biochem. 44: 276–287, 1971.CrossRefPubMedGoogle Scholar
  11. Behboudian M.H., Törökfalvy E., Walker R.R.: Effects of Salinity on ionic content, water relations and gas exchanges parameters in some citrus scion-rootstock combinations.–Sci. Hortic.-Amsterdam 28: 105–116, 1986.CrossRefGoogle Scholar
  12. Beligni M.V., Fath A., Bethke P.C. et al.: Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers.–Plant Physiol. 129: 1642–1650, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bethke P.C., Drew M.C.: Stomatal and nonstomatal components to inhibition of photosynthesis in leaves of Capsicum annum during progressive exposure to NaCl salinity.–Plant Physiol. 99: 219–226, 1992.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bilger W., Johnsen T., Schreiber U.: UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants.–J. Exp. Bot. 52: 2007–2014, 2001.CrossRefPubMedGoogle Scholar
  15. Björkman O., Demming B.: Photon yield of oxygen evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origin.–Planta 170: 489–504, 1987.CrossRefPubMedGoogle Scholar
  16. Blokhina O., Virolainen E., Fagerstedt K.V.: Antioxidants, oxidative damage and oxygen deprivation stress: a review.–Ann. Bot.-London 91:179–194, 2003.CrossRefGoogle Scholar
  17. Bors W., Langebartels C., Michel C. et al.: Polyamines as radical scavengers and protectants against ozone damage.–Phytochemistry 28: 1589–1595, 1989.CrossRefGoogle Scholar
  18. Bouchereau A., Aziz A., Larher F. et al.: Polyamines and environmental challenges: recent development.–Plant Sci. 140: 103–125, 1999.CrossRefGoogle Scholar
  19. Bradford M.N.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding.–Anal Biochem. 72: 248–254, 1976.CrossRefPubMedGoogle Scholar
  20. Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.–Ann. Bot.-London 103: 551–560, 2009.CrossRefGoogle Scholar
  21. Demetriou G., Neonaki C., Navakoudis E. et al.: Salt stress impact on the molecular structure and function of the photosynthetic apparatus-the protective role of polyamines.–BBABioenergetics 1767: 272–280, 2007.CrossRefGoogle Scholar
  22. Dhindsa R.S., Plumb-Dhindsa P., Thorpe T.A.: Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase.–J. Exp. Bot. 32: 93–101, 1981.CrossRefGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. Gadallah M.A.A.: Effects of indole-3-acetic acid and zinc on the growth, osmotic potential and soluble carbon and nitrogen components of soybean plants growing under water deficit.–J. Arid. Environ. 44: 451–467, 2000.CrossRefGoogle Scholar
  25. Galston A.W., Kaur-Sawhney R., Altabella T. et al.: Plant polyamines in reproductive activity and response to a biotic stress.–Bot. Acta 110: 197–207, 1997.CrossRefGoogle Scholar
  26. García-Mata C., Lamattina L.: Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress.–Plant Physiol. 126: 1196–1204, 2001.CrossRefPubMedGoogle Scholar
  27. García-Sánchez F., Jifon J.L., Carvajal M. et al.: Gas exchange, chlorophylle and nutrient content in relation to Na and Cl accumulation in sunburst mandarin grafted on different rootstock.–Plant Sci. 162: 705–712, 2002.CrossRefGoogle Scholar
  28. Genty B., Briantais J.M., Baker N.B.: The relationship between the quantum yield of photosynthetic electrontransport and quenching of chlorophyll fluorescence.–Biochim. Biophys. Acta 990: 87–92, 1989.CrossRefGoogle Scholar
  29. González L., González-Vilar M.: Determination of relative water content.–In: Reigosa M.J. (ed.): Handbook of Plant Ecophysiology Techniques. Pp. 207–212. Kluwer Academic, Dordrecht 2001.Google Scholar
  30. Hamdani S., Gauthier A., Msilini N. et al.: Positive charges of polyamines protect PSII in isolated thylakoid membranes during photoinhibitory conditions.–Plant Cell Physiol. 52: 866–873, 2011.CrossRefPubMedGoogle Scholar
  31. Hare P.D., Cress W.A.: Metabolic implications of stress-induced proline accumulation in plants.–Plant Growth Regul. 21: 79–102, 1997.CrossRefGoogle Scholar
  32. Hedge J.E., Hofreiter B.T.: Estimation of starch by anthrone reagent.–In: Whistler R.L., Be-Miller J.N. (ed.): Methods in Carbohydrate Chemistry. Pp. 420. Academic Press, New York 1962.Google Scholar
  33. Hernández J.A., Almansa M.S.: Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves.–Physiol. Plantarum 115: 251–257, 2002.CrossRefGoogle Scholar
  34. Hernández J.A., Campillo A., Jimenez A. et al.: Response of antioxidant systems and leaf water relations to NaCl stress in pea plants.–New Phytol. 141: 241–251, 1999.CrossRefGoogle Scholar
  35. Huaifu F., Shirong G., Yansheng J. et al.: Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings NaCl stress.–Front. Agric. China 1: 308–314, 2007.Google Scholar
  36. Jiang M.Y., Zhang J.H.: Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings.–Plant Cell. Physiol. 42: 1265–1273, 2001.CrossRefPubMedGoogle Scholar
  37. Jiménez-Bremont J.F., Becerra Flora A., Hernández-Lucero E. et al.: Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine.–Biol. Plantarum 50:763–766, 2006.CrossRefGoogle Scholar
  38. Katerji N., van Hoorn J.W., Hamdy A. et al.: Osmotic adjustment of sugarbeets in response to soil salinity and its influence on stomatal conductance, growth and yield.–Agr. Water Manage. 34: 57–69, 1997.CrossRefGoogle Scholar
  39. Khan N.M., Siddiqui M.H., Mohammad F. et al.: Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation.–Acta Physiol. Plant. 32: 121–132, 2010.CrossRefGoogle Scholar
  40. Khayyat M., Tehranifar T., Davarynejad G.H.: Effects of NaCl salinity on some leaf nutrient concentrations, non-photochemical quenching and the efficiency of the PSII photochemistry of two Iranian pomegranate varieties under greenhouse and field conditions: Preliminary results.–J. Plant Nutr. 39: 1752–1765, 2016.CrossRefGoogle Scholar
  41. Khoshbakht D., Ghorbani A., Baninasab B. et al.: Effects of supplementary potassium nitrate on growth and gas-exchange characteristics of salt-stressed citrus seedlings.–Photosynthetica 52: 589–596, 2014.CrossRefGoogle Scholar
  42. Khoshbakht D., Asgharei M.R.: Influence of foliar-applied salicylic acid on growth, gas-exchange characteristics, and chlorophyll fluorescence in citrus under saline conditions.–Photosynthetica 53: 410–418, 2015a.CrossRefGoogle Scholar
  43. Khoshbakht D., Ramin A.A., Baninasab B.: Effects of sodium chloride stress on gas exchange, chlorophyll content and nutrient concentrations of nine citrus rootstocks.–Photosynthetica 53: 241–249, 2015b.CrossRefGoogle Scholar
  44. Kusano T., Berberich T., Tateda C. et al.: Polyamines: essential factors for growth and survival.–Planta 228: 367–381, 2008.CrossRefPubMedGoogle Scholar
  45. Lamattina L., García-Mata C., Graziano M. et al.: Nitric oxide: the versatility of an extensive signal molecule.–Annu. Rev. Plant Biol. 54: 109–136, 2003.CrossRefPubMedGoogle Scholar
  46. Larsen M.H., Davis T.D., Evans R.P.: Modulation of protein expression in uniconazole treated soybean in relation to heat stress.–Proc. Plant Growth Reg. Soc. Am. 15: 177–182, 1988.Google Scholar
  47. Laspina N.V., Groppa M.D., Tomaro M.L., Benavides M.P.: Nitric oxide protects sunflower leaves against Cd-induced oxidative stress.–Plant Sci. 169: 323–330, 2005.CrossRefGoogle Scholar
  48. Leshem Y.Y., Wills R.B.H., Ku V.V.V.: Evidence for the function of the free radical gas-nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants.–Plant Physiol. Bioch. 36: 825–833, 1998.CrossRefGoogle Scholar
  49. Lichtenthaler H.K., Wellburn W.R.: Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.–Biochem. Soc. T. 11: 591–592, 1983.CrossRefGoogle Scholar
  50. Liu S., Dong Y., Xu L. et al.: Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings.–Plant Growth Regul. 73: 67–68, 2014.CrossRefGoogle Scholar
  51. Lopatin A.N., Makhina E.N., Nichols C.G.: Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification.–Nature 372: 366–369, 1994.CrossRefPubMedGoogle Scholar
  52. López-Carrión A.I., Castellano R., Rosales M.A. et al.: Role of nitric oxide under saline stress: implications on proline metabolism.–Biol. Plantarum 52: 587–591, 2008.CrossRefGoogle Scholar
  53. Lutts S., Kinet J.M., Bouharmont J.: Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance.–J. Exp. Bot. 46: 1843–1852, 1995.CrossRefGoogle Scholar
  54. Lütz C., Navakoudis E., Seidlitz H.K. et al.: Simulated solar irradiation with enhanced UV-B adjust plastid-and thylakoidassociated polyamine changes for UV-B protection.–BBABioenergetics 1710: 24–33, 2005.CrossRefGoogle Scholar
  55. Mapelli S., Brambilla I., Radyukina N. et al.: Free and bound polyamines changes in different plants as a consequence of UV–B light irradiation.–Gen. Appl. Plant Physiol. 34: 55–66, 2008.Google Scholar
  56. Maxwell K., Johnson G.N.: Chlorophyll fluorescence–a practical guide.–J. Exp. Bot. 51: 659–668, 2000.CrossRefPubMedGoogle Scholar
  57. Mittler R.: Oxidative stress, antioxidants and stress tolerance.–Trends Plant Sci. 7: 405–410, 2002.CrossRefPubMedGoogle Scholar
  58. Moya J.L., Primo-Millo E., Talon M.: Morphological factors determining salt tolerance in citrus seedlings: the shoot to root ratio modulates passive root uptake of chloride ions and their accumulation in leaves.–Plant Cell Environ. 22: 1425–1433, 1999.CrossRefGoogle Scholar
  59. Munns R., Tester M.: Mechanisms of salinity tolerance.–Annu. Rev. Plant Biol. 59: 651–681, 2008.CrossRefPubMedGoogle Scholar
  60. Munns R.: Genes and salt tolerance: bringing them together.–New Phytol. 167: 645–663, 2005.CrossRefPubMedGoogle Scholar
  61. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.–Plant Cell. Physiol. 22: 867–880, 1981.Google Scholar
  62. Nickel R.S., Cunningham B.A.: Improved peroxidase assay method using leuco-2,3,6-trichloroindophenol and application to comparative measurements of peroxidase catalysis.–Anal. Biochem. 27: 292–299, 1969.CrossRefPubMedGoogle Scholar
  63. Noreen Z., Ashraf M., Akram N.A.: Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.).–J. Agron. Crop Sci. 196: 273–285, 2010.Google Scholar
  64. Palma F., Lluch C., Iribarne C. et al.: Combined effect of salicylic acid and salinity on some antioxidant activities, oxidative stress and metabolite accumulation in Phaseolus vulgaris.–Plant Growth Regul. 58: 307–316, 2009.CrossRefGoogle Scholar
  65. Parida A.K., Das A.B.: Salt tolerance and salinity effects on plants: a review.–Ecotoxicol. Environ. Safe. 60: 324–349, 2005.CrossRefGoogle Scholar
  66. Parihar P., Singh S., Singh R. et al.: Effect of salinity stress on plants and its tolerance strategies: a review.–Environ. Sci.Pollut. R. 22: 4056–4075, 2015.CrossRefGoogle Scholar
  67. Parvin S., Lee O.R., Sathiyaraj G. et al.: Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system.–Gene 537: 70–78, 2014.CrossRefPubMedGoogle Scholar
  68. Peltzer D., Dreyer E., Polle A.: Differential temperature dependencies of antioxidative enzymes in two contrasting species.–Plant Physiol. Bioch. 40: 141–150, 2002.CrossRefGoogle Scholar
  69. Rao G.G., Rao G.R.: Pigment composition and chlorophyllase activity in pigeon pea (Cajanus indicus Spreng) and Gingelley (Sesamum indicum L.) under NaCl salinity.–Indian J. Exp. Biol. 19: 768–770, 1981.Google Scholar
  70. Ravindran K.C., Venkatesan K., Balakrishan V. et al.: Restoration of saline land by halophytes for Indian soils.–Soil Biol. Biochem. 39: 2661–2664, 2007.CrossRefGoogle Scholar
  71. Romero-Aranda R., Soria T., Cuartero J.: Tomato plant-water uptake and plant-water relationships under saline growth conditions.–Plant Sci. 160: 265–272, 2001.CrossRefPubMedGoogle Scholar
  72. Rosales M.A., Rios J.J., Castellano R. et al.: Proline metabolism in cherry tomato exocarp in relation to temperatura and solar radiation.–J. Hortic. Sci. Biotech. 82: 739–744, 2007.CrossRefGoogle Scholar
  73. Roy P., Niyogi K., SenGupta D.N. et al.: Spermidine treatment to rice seedlings recovers salinity stressinduced damage of plasma membrane and PM-bound H+ATPase in salt-tolerant and salt-sensitive rice cultivars.–Plant Sci. 168: 583–591, 2005.CrossRefGoogle Scholar
  74. Ruiz D., Martínez V., Ceradá A.: Citrus response to salinity: growth and nutrient uptake.–Tree Physiol. 17: 141–150, 1997.CrossRefPubMedGoogle Scholar
  75. Santa-Cruz A., Acosta M., Perez-Alfocea F. et al.: Changes in free polyamine levels induced by salt stress in leaves of cultivated and wild tomato species.–Physiol. Plantarum 101: 341–346, 1997.CrossRefGoogle Scholar
  76. Setlík S.I., Allakhveridiev L., Nedbal E. et al.: Three type of photosystem II photoinactivation. I. Damaging process on the acceptor side.–Photosynth. Res. 23: 39–48, 1990.CrossRefPubMedGoogle Scholar
  77. Sfakianaki M., Sfichi L., Kotzabasis K.: The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature.–J. Photoch. Photobio. B 84: 181–188, 2006.CrossRefGoogle Scholar
  78. Shalhevet J.: Plants under salt and water stress.–In: Fowden L., Mansfield T., Stoddart J (ed.): Plant Adaptation to Environmental Stress. Pp. 133–154. Chapman and Hall, London-Glasgow-New York-Tokyo-Melbourne-Madras. 1993.Google Scholar
  79. Sharma D., Dubey A., Srivastav M. et al.: Effect of putrescine and paclobutrazol on growth, physiochemical parameters., and nutrient acquisition of salt-sensitive citrus rootstock Karna khatta (Citrus karna Raf.) under NaCl Stress.–J. Plant Growth Regul. 30: 301–311, 2011.CrossRefGoogle Scholar
  80. Sheokand S., Kumari A., Sawhney V.: Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants.–Physiol. Mol. Biol. Plants 14: 355–362, 2008.CrossRefPubMedGoogle Scholar
  81. Singh A.K, Dubey R.S.: Changes in chlorophyll a and b contents and activities of photosystems I and II in rice seedlings induced by NaCl.–Photosynthetica 31: 489–499, 1995.Google Scholar
  82. Stevens J., Senaratna T., Sivasithamparam K.: Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. ‘Roma’): associated changes in gas exchange, water relations and membrane stabilisation.–Plant Growth Regul. 49: 77–83, 2006.Google Scholar
  83. Sudhir P., Murthy S.D.S.: Effects of salt stress on basic processes of photosynthesis.–Photosynthetica 42: 481–486, 2004.CrossRefGoogle Scholar
  84. Syeed S., Anjum N.A., Nazar R. et al.: Salicylic acid-mediated changes in photosynthesis, nutrients content and antioxidant metabolism in two mustard (Brassica junea L.) cultivars differing in salt tolerance.–Acta Physiol. Plant. 33: 877–886, 2011.CrossRefGoogle Scholar
  85. Takahama U., Oniki T.: A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells.–Physiol. Plantarum 101: 845–852, 1997.CrossRefGoogle Scholar
  86. Todorova D., Sergiev I., Alexieva V. et al.: Polyamine content in Arabidopsis thaliana (L.) Heynh during recovery after low and high temperature treatments.–Plant Growth Regul. 51: 185–191, 2007.CrossRefGoogle Scholar
  87. Torrecillas A., Guillaume C., Alarcon J.J. et al.: Water relations of two tomato species under water stress and recovery.–Plant Sci. 105: 169–176, 1995.CrossRefGoogle Scholar
  88. Upchurch R.G.: Fatty acid unsaturation, mobilization and regulation in response of stress to plants.–Biotechnol. Lett. 30: 967–977, 2008.CrossRefPubMedGoogle Scholar
  89. van Kooten O., Snel J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.–Photosynth. Res. 25: 147–150, 1990.CrossRefPubMedGoogle Scholar
  90. Velikova V., Yordanov I., Edreva A.: Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines.–Plant Sci. 151: 59–66, 2000.CrossRefGoogle Scholar
  91. Verma S., Mishra S.N.: Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system.–J. Plant Physiol. 162: 669–677, 2005.CrossRefPubMedGoogle Scholar
  92. Wang X., Shi G.X., Xu Q.S. et al.: Exogenous polyamines enhance copper tolerance of Nymphoides peltatum.–J. Plant Physiol. 164: 1062–1070, 2007.CrossRefPubMedGoogle Scholar
  93. Wi S.J., Kim W.T., Park K.Y.: Overexpression of carnation Sadenosylmethionine decarboxylase gene generates a broad spectrum tolerance to abiotic stresses in transgenic tobacco plants.–Plant Cell. Rep. 25: 1111–1121, 2006.CrossRefPubMedGoogle Scholar
  94. Wimalasekera R., Tebartz F., Scherer G. F.: Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses.–Plant Sci. 181: 593–603, 2011.CrossRefPubMedGoogle Scholar
  95. Wu X., Zhu W., Zhang H. et al.: Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill).–Acta Physiol. Plant. 33: 1199–1209, 2011.CrossRefGoogle Scholar
  96. 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.CrossRefGoogle Scholar
  97. Zhang L., Zhang Z., Gao H. et al.: Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves.–Physiol. Plantarum 143: 396–407, 2011.CrossRefGoogle Scholar
  98. Zhao L.Q., Zhang F., Guo J.K. et al.: Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed.–Plant Physiol. 134: 849–857, 2004.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Department of Horticultural Science, College of AgricultureUrmia UniversityWest AzarbaijanIran
  2. 2.Department of Horticulture Science, College of AgricultureIsfahan University of TechnologyIsfahanIran

Personalised recommendations