Document Type : Research paper

Author

Department of Biology, Faculty of Science, Payame Noor University, Tehran 19395-3697, Iran

10.22059/ijhst.2021.312776.407

Abstract

Soil salinity is one of the critical challenges for development of culture area of agricultural crops. In the present study a pot experiment was conducted in factorial based on completely randomized design aimed to investigate the impact of exogenous application of salicylic acid (SA 0, 0.75 and 1.5 mM) and calcium chloride (CaCl2 0, 50 and 100 mM), solely or in combination, on plant growth, photosynthetic pigments (total chlorophyll (Chl), carotenoids, anthocyanin), and some metabolic parameters (reducing sugars, proline, lipid peroxidation and scavenging ability on DPPH (2,2-diphenyl-1-picrylhydrazyl) radical) of red bean exposed to salt stress (0, 25 and 75 mM NaCl). Results showed that exogenous application of SA or calcium (Ca) alone improved plant performance under NaCl stress. Growth slowed down under salinity. Malondialdehyde (MDA), DPPH radical, anthocyanin, and proline content were increased under salinity stress. However, application of SA and Ca enhanced the growth parameters, improved the Chl, carotenoids, and reducing sugars content, and significantly reduced MDA and DPPH radical in plants. Therefore, induced tolerance to salinity as the result of SA and Ca application may be related to the regulation of antioxidative responses. Furthermore, the beneficial effect of SA and Ca were achieved by applications of 0.75 mM SA and 50 mM CaCl2, which are recommended to improve red bean performance under saline conditions. In conclusion, exogenous application of SA and Ca improved salinity stress tolerance through the regulation of antioxidant system.

Keywords

Abd El-Hameid Asmaa R, Ahmed M.A, Gamal El-Din Karima M, Shalaby Magda A.F, Elnaggar Hoda M.H. 2017. Role of salicylic acid to improve physiological characters and bio-Chemical markers of soybean (Glycine max L.) under sea salt stress. International Journal of Environmental Research 11, 547-556.
Abdel Latef A.A.H. 2011. Ameliorative effect of calcium chloride on growth, antioxidant enzymes, protein patterns and some metabolic activities of canola (Brassica napus L.) under sea water stress. Journal of Plant Nutrrition 34(9), 1303–1320.
Acosta-Motos J.R, Ortuño M.F.A, Bernal-Vicente P, Diaz-Vivancos M.J, Hernandez JA. 2017. Plant responses to salt stress: Adaptive mechanisms. Agronomy 7 (1), 18–38.
Aghaei H, Ehsanpour A.A, Shah A.H.S, Komatsu S. 2009. Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids 36, 91–98.
Ahmad P, Abd-Allah E.F, Alyemeni M.N, Wijaya L, Alam P, Bhardwaj R, Siddique K.H.M. 2018. Exogenous application of calcium to 24-epibrassinosteroid pre-treated tomato seedlings mitigates NaCl toxicity by modifying ascorbate–glutathione cycle and secondary metabolites. Scientific Reports 8 (1), 13515.
Ahmad S, Wahid A, Rasul E, Wahid A. 2005. Comparative morphological and physiological responses of green gram genotypes to salinity applied at different growth stages. Botanical Bulletin Academia Sinica 6, 35–42.
Akhtar J, Ahmad R, Ashraf M.Y, Tanveer A, Warrich E.A, Oraby H. 2013. Influence of exogenous application of salicylic acid on saltstressed mungbean (Vigna radiata): Growth and nitrogen metabolism. Pakistan Journal of Botany 45, 119–25.
Aliniaeifard S, Hajilou J, Tabatabaei S.J. 2016a. Photosynthetic and growth responses of olive to proline and salicylic acid under salinity condition. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 44(2), 579-585.
Aliniaeifard S, Hajilou J, Tabatabaei S.J, Sifi-Kalhor M. 2016b. Effects of ascorbic acid and reduced glutathione on the alleviation of salinity stress in olive plants. International Journal of Fruit Science 16, 395–409.
Al-Whaibi M, Siddiqui M, Basalah M. 2012. Salicylic acid and calcium-induced protection of wheat against salinity. Protoplasma 249, 769–778.
Ananieva K, Malbeck J, Kamı´nek J, van Staden J. 2004. Methyl jasmonate down-regulates endogenous cytokinin levels in cotyledons of Cucurbita pepo (zucchini) seedlings. Physiologia Plantarum 122(4), 496–503.
Arfan M, Athar H.R, Ashraf M. 2007. 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? Journal of Plant Physiology 6, 685–694.
Arshi A, Abdin M.Z, Iqbal M. 2006. Sennoside content and yield attributes of Cassia angustifolia Vahl. as affected by NaCl and CaCl2. Scientia Horticulturae 111, 84–90.
Ashraf M, Ali Q. 2008. Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). Environmental and Experimental Botany 63 (1–3), 266–73.
Ashraf MY, Ashraf M, Mehmood K, Akhtar J, Hussain F, Arshad M. 2010. Phytoremediation of saline soils for sustainable agricultural productivity. In: Plant adaptation and phytoremediation, eds. M. Ashraf, M. Ozturk, and M. S. A., Ahmad, 335–355. Dordrecht, The Netherland: Springer.
Azevedo Neto A.D, Gomes-Filho E, Prisco J.T. 2008. Salinity and oxidative stress. In: Khan NA, Singh S (eds) Abiotic stress and plant responses. IK International Group, Aligarh, pp 58–82.
Azevedo Neto A.D, Prisco J.T, Ene´as-Filho J, Abreu C.E.B, Gomes- Filho E. 2006. Effect of salt stress on antioxidative enzymes and lipids peroxidation in leaves and roots of salt-tolerant and salt sensitive maize genotypes. Environmental and Experimental Botany 56, 87–94.
Bartels D, Sunkar R. 2005. Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23–58.
Bates L,Waldren R, Teare I. 1973. Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Blokhina O, Virolainen E, Fagerstedt K.V. 2003. Antioxidants, oxidative damage and oxygen deprivations stress. Annals of Botany 91, 179–194.
Bor M.O, Zdemir F, Turkan I. 2003. The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science 164, 77–84.
Cavalcanti F.R, Oliveira J.T.A, Miranda A.S.M, Vie´gas R.A, Silveira J.A.G. 2004. Superoxide dismutase, catalase and peroxidase activities do not confer protection against oxidative damage in salt-stressed cowpea leaves. New Phytologist 163, 563–571.
De Pascale S, Maggio A, Fogliano V, Ambrosino P, Ritieni A. 2001. Irrigation with saline water improves carotenoids content and antioxidant activity of tomato. The Journal of Horticultural Science and Biotechnology 76, 447–453.
Delavari PM, Baghizadeh A, Enteshari SH, Kalantari K.H.M, Yazdanpanah A, Mousavi E.A. 2010. The effect of salicylic acid on some of biochemical and morphological characteristic of Ocimum Basilicum under salinity stress. Australian Journal of Basic Applied Sciences 4(10), 4832–4845.
Demiral T, Turkan I. 2006. Exogenous glycinebetaine affects growth and proline accumulation and retards senescence in two rice cultivars under NaCl stress. Environmental and Experimental Botany 56, 72–79.
El-Khallal S.M, Hathout T.M, Abdel Raheim A, Ashour A, Kerrit A.A. 2009. Brassinolide and salicylic acid induced growth, biochemical activities and productivity of maize plant growth under salt stress. Research Journal of Agricultural and Biological Sciences 5(4), 380–390.
Erasalan F, Inal A, Gunes A, Alpaslan M. 2007. Impact of exogenous salicylic acid on the growth, antioxidant activity and physiology of carrot plants subjected to combined salinity and boron toxicity. Scientia Horticulturae 113, 120–128.
Fallon K.M, Phillips R. 1989. Responses to water stress in adapted and unadapted carrot cell suspension cultures. Journal of Experimental Botany 40, 681–687.
Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci E.G, Cicek N. 2007. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology 164, 728–736.
Heath R.L, Packer L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189– 198.
Hernández J.A. 2019. Salinity tolerance in plants: trends and perspectives international Journal of Molecular Sciences 20, 2408.
Heidarian F, Roshandel P. 2021. Salicylic acid improves tolerance against salt stress through boosting antioxidant defense system in Black Bean. International Journal of Horticultural Science and Technology 8(2), 175-189.
Hiratsuka S, Onodera H, Kawai Y, Kubo T, Itoh H, Wada R. 2001. ABA and sugar effects on anthocyanin formation in grape berry cultured in vitro. Scientia Horticulturae 90, 121–130.
Janda T, Horvath E, Szalai C, Paldi E. 2007. Role of salicylic acid in the induction of abiotic stress tolerance. In: Hayat S, Ahmad A (eds) Salicylic acid: a plant hormone. Springer, Dordrecht, pp 91–154.
Jeffries T.W, Yang V.W, Davis M.W. 1988. Comparative study of xylanase kinetics using dinitrosalicylic, arsenomolybdate, and ion chromatographic assays. Applied Biochemistry and Biotechnology 70–72, 257–265.
Katsuhara M, Otsuka T, Ezaki B. 2005. Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Science 169, 369–373.
Kaya C, Ak B.E, Higgs D, Murillo-Amador B. 2002. Influence of foliar-applied calcium nitrate on strawberry plants grown under salt stress conditions. Australian Journal of Experimental Agriculture 42, 631-636.
Kudla J, Batistic O, Hashimoto K. 2010. Calcium signals: the lead currency of plant information processing. Plant Cell 22, 541–563.
Larbi A, Kchaou H, Gaaliche B, Gargouri K, Boulal H, Morales F. 2020. Supplementary potassium and calcium improves salt tolerance in olive plants. Scientia Horticulturae 260.
Lastochkina O, Garshina D, Allagulova C, Pusenkova L, Garipova S, Maslennikova D, Fedorova K, Shpirnaya I, Ibragimov A, Koryakov I, Sakhapova A. 2021. Potential Aspects of Plant Growth Promoting Bacteria to Improve Horticultural Crop Production. International Journal of Horticultural Science and Technology 1, 8(2):103-122.
Lee D.H, Kim T.S, Lee C.B. 2001. The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). Journal of Plant Physiology 158, 737-745.
Lichtenthaler HK. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Magda A.F.S, Ahmed M.A, Abdallah M.S.A, Ebtesam A. 2013. Physiological role of salicylic acid in improving growth and productivity of barley (Hordeum vulgare L.) under sandy soil conditions. Middle East Journal of Agriculture Research 2(2), 68–75.
Martinez C.A, Maestri M, Lani E.G. 1996. In vitro salt tolerance and proline accumulation in Andean potato (Solanum spp.) differing in frost resistance. Plant Science 116, 177–184.
Meirs S, Philosoph hadas S, Aharoni N. 1992. Ethylene increased accumulation of fluorescent lipid peroxidation products detected during senescence of parsley by a newly developed method. Journal of the American Society for Horticultural Science 117, 128–132.
Meloni DA, Oliva MA, Martinez CA, Cambraia J. 2003: Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany 49, 69–76.
Michailidis M, Karagiannis E, Tanou G, Karamanoli K, Lazaridou A, Matsi T, Molassiotis A. 2017: Metabolomic and physico-chemical approach unravel dynamic regulation of calcium in sweet cherry fruit physiology. Plant Physiology and Biochemistry 116, 68–79.
Misra N, Saxena P. 2009. Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Science 177, 181–189.
Mohammad M, Shibli R, Ajlouni M, Nimri L. 1998. Tomato root and shoot responses to salt stress under different levels of phosphorus nutrition. Journal of Plant Nutrition 21(8), 1667–1680.
Mukhtar I, Shahid M.A, Khan M.W, Balal R.M, Iqbal M.M, Naz T, Zubair M, Ali H.H. 2016. Improving salinity tolerance in chili by exogenous application of calcium and sulphur. Soil and Environment 35 (1), 56–64.
Munns R, Tester M. 2008. Mechanisms of salinity tolerance. ‎Annual Review of Plant Biology 59 (1), 651–81.
Naeem M, Naeem M.S, Ahmad R, Ihsan M.Z, Ashraf M.Y, Hussain Y, Fahad S. 2018. Foliar calcium spray confers drought stress tolerance in maize via modulation of plant growth, water relations, proline content and hydrogen peroxide activity. Archives of Agronomy and Soil Science 64 (1), 116–31.
Navarro J.M, Martinez V, Carvajal M. 2000. Ammonium bicarbonate and calcium effects on tomato plants grown under saline conditions. Plant Science 157, 89–96.
Radi A.A, Farghaly F.A, Hamada A.M. 2013. Physiological and biochemical responses of salt-tolerant and salt-sensitive wheat and bean cultivars to salinity. Journal of Biology and Earth Sciences 3, 72–88.
Rejšková A.B, Lenka P, Eva S, Helena L. 2007. The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions. Journal of Plant Physiology 164, 174–184.
Rouholamin S, Zahedi B, Nazarian-Firouzabadi F, Saei A. 2015. Expression analysis of anthocyanin biosynthesis key regulatory genes involved in pomegranate (punica granatum l.). Scientia Horticulturae 186, 84–88.
Sahu G.K. 2013. Salicylic acid: Role in plant physiology and stress tolerance. In: G.R. Rout, A.B. Das (Eds.) Molecular stress physiology of plants. Springer, India, 217–239.
Seifikalhor M, Aliniaeifard S, Shomali A, Azad N, Hassani B, Lastochkina O, Li T. 2019. Calcium signaling and salt tolerance are diversely entwined in plants. Plant signaling and behavior 14(11), 1665455.
Shaki F, Ebrahimzadeh H, Niknam M.V. 2017. Central role of salicylic acid in resistance of safflower (Carthamus tinctorius L.) against salinity. Journal of Plant Interactions 12(1), 414-420.
Shakirova F.M, Sakhabutdinova A.R, Bezrukova M.V, Fatkhutdinova R.A, Fatkhutdinova D.R. 2003. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science 164, 317–322.
Shahmoradi H, Naderi D. 2018. Improving effects of salicylic acid on morphological, physiological and biochemical responses of salt-imposed winter Jasmine. International Journal of Horticultural Science and Technology 5(2), 219-230.
Shimada K, Fujikawa K, Yahara K, Nakamura T. 1992. Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. Journal of Agricultural and Food Chemistry 40, 945–948.
Szepesi A, Csiszar J, Bajkan S, Gemes K, Horvath F, Erdel L, Deer A.K, Simon M.L, Tari I. 2005. Role of salicylic acid pretreatment on the acclimation of tomato plants to salt and osmotic stress. Acta Biologica Szegediensis 49, 123–125.
Tanveer K, Gilani S, Hussain Z, Ishaq R, Muhammad Adeel M, Ilyas N. 2020. Effect of salt stress on tomato plant and the role of calcium. Journal of Plant Nutrition 43, 28-35.
Tavakkoli E, Rengasamy P, McDonald G.K. 2010. High concentrations of Na‏ and Cl ions in soil solution have simultaneous detrimental effects on growth of Faba bean under salinity stress. Journal of Experimental Botany 61 (15), 4449–59.
Trabelsi L, Gargouri K, Ben Hassena A, Mbadra C, Ghrab M, Ncube B, Van Staden J, Gargouri R. 2019. Impact of drought and salinity on olive water status and physiological performance in an arid climate. Agricultural Water Management 213, 749–759.
Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K. 1999. Cloning of chlorophyllase, the key enzyme in chlorophyll degradation. Finding of a lipase motif and the induction by methyl jasmonate. Proceedings of the National Academy Sciences 96 (26), 15362–7.
Tuna A.L, Kaya C, Ashraf M, Altunlu H, Yokas I, Yagmur B. 2007. The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environmental and Experimental Botany 59(2), 173–178.
Wanger G.J. 1979. Content and vacuole/extra vacuole distribution of neutral sugars, free amino acids, and anthocyanins in protoplasts. Plant Physiology 64, 88-93.
Winkel Shirley B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218–223.
Xu W.P, Peng H, Yang T.B, Whitaker B, Huang L.H, Sun J.H, Chen P. 2014. Effect of calcium on strawberry fruit flavonoid pathway gene expression and anthocyanin accumulation. Plant Physiology and Biochemistry 82, 289–298.
Zafar S, Ashraf MY, Anwar S, Ali Q, Noman A. 2016. Yield enhancement in wheat by soil and foliar fertilization of K and Zn under saline environment. Soil and Environment 35 (1), 46–55.
Zafar S, Ashraf MY, Saleem M. 2018. Shift in physiological and biochemical processes in wheat supplied with zinc and potassium under saline condition. Journal of Plant Nutrition 41 (1), 19–28.

Zhu M, Yu J, Tang W, Fan S, Bai M, Chen M, Yang G. 2019. Role of calcium in regulating anthocyanin accumulation in ‘Manicure Finger’ grape berries. Scientia Horticulturae 256, 108585.