Photosynthetica 2018, 56(4):1313-1325 | DOI: 10.1007/s11099-018-0839-z

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

D. Khoshbakht1,*, M. R. Asghari1, M. Haghighi2
1 Department of Horticultural Science, College of Agriculture, Urmia University, West Azarbaijan, Iran
2 Department of Horticulture Science, College of Agriculture, Isfahan University of Technology, Isfahan, Iran

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.

Keywords: abiotic stress; biomass; gas exchange; oxidative stress; photosystem II efficiency

Received: June 30, 2017; Accepted: January 3, 2018; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

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Khoshbakht, D., Asghari, M.R., & Haghighi, M. (2018). Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence, photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress. Photosynthetica, 56(4), 1313-1325. doi: 10.1007/s11099-018-0839-z.
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    References

    1. Aebi H.: Catalase in vitro.-Methods Enzymol. 105: 121-126, 1984. Go to original source...
    2. Alcázar R., Altabella T., Marco F. et al.: Polyamines: molecules withregulatory functions in plant abiotic stress tolerance.-Planta 231: 1237-1249, 2010. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    6. Arasimowicz M., Floryszak-Wieczorek J.: Nitric oxide as a bioactive signaling molecule in plant stress responses.-Plant Sci. 172: 876-887, 2007. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    10. Beauchamp C., Fridovich I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.-Anal. Biochem. 44: 276-287, 1971. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    16. Blokhina O., Virolainen E., Fagerstedt K.V.: Antioxidants, oxidative damage and oxygen deprivation stress: a review.-Ann. Bot.-London 91:179-194, 2003. Go to original source...
    17. Bors W., Langebartels C., Michel C. et al.: Polyamines as radical scavengers and protectants against ozone damage.-Phytochemistry 28: 1589-1595, 1989. Go to original source...
    18. Bouchereau A., Aziz A., Larher F. et al.: Polyamines and environmental challenges: recent development.-Plant Sci. 140: 103-125, 1999. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    31. Hare P.D., Cress W.A.: Metabolic implications of stress-induced proline accumulation in plants.-Plant Growth Regul. 21: 79-102, 1997. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    44. Kusano T., Berberich T., Tateda C. et al.: Polyamines: essential factors for growth and survival.-Planta 228: 367-381, 2008. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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.
    56. Maxwell K., Johnson G.N.: Chlorophyll fluorescence-a practical guide.-J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    57. Mittler R.: Oxidative stress, antioxidants and stress tolerance.-Trends Plant Sci. 7: 405-410, 2002. Go to original source...
    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. Go to original source...
    59. Munns R., Tester M.: Mechanisms of salinity tolerance.-Annu. Rev. Plant Biol. 59: 651-681, 2008. Go to original source...
    60. Munns R.: Genes and salt tolerance: bringing them together.-New Phytol. 167: 645-663, 2005. Go to original source...
    61. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.-Plant Cell. Physiol. 22: 867-880, 1981.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    65. Parida A.K., Das A.B.: Salt tolerance and salinity effects on plants: a review.-Ecotoxicol. Environ. Safe. 60: 324-349, 2005. Go to original source...
    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. Go to original source...
    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. Go to original source...
    68. Peltzer D., Dreyer E., Polle A.: Differential temperature dependencies of antioxidative enzymes in two contrasting species.-Plant Physiol. Bioch. 40: 141-150, 2002. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    74. Ruiz D., Martínez V., Ceradá A.: Citrus response to salinity: growth and nutrient uptake.-Tree Physiol. 17: 141-150, 1997. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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.
    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.
    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.
    83. Sudhir P., Murthy S.D.S.: Effects of salt stress on basic processes of photosynthesis.-Photosynthetica 42: 481-486, 2004. Go to original source...
    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.
    85. Takahama U., Oniki T.: A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells.-Physiol. Plantarum 101: 845-852, 1997. Go to original source...
    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. Go to original source...
    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. Go to original source...
    88. Upchurch R.G.: Fatty acid unsaturation, mobilization and regulation in response of stress to plants.-Biotechnol. Lett. 30: 967-977, 2008. Go to original source...
    89. van Kooten O., Snel J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147-150, 1990. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...

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