Physiological Mechanism of Salicylic Acid for Alleviation of Salt Stress in Rice
Received date: 2016-04-12
Accepted date: 2016-07-07
Online published: 2016-12-28
Soil salinity is one of the most important problems of crop production in estuarine and coastal zones. Improvement in salt tolerance of major food crops is an important way for the economic utilization of coastal zones. This study proved that the application of salicylic acid (SA) improved the growth and yield under salt stress conditions and investigated its physiological mechanisms for salt tolerance. The investigation on the effect of SA for salt tolerance during germination showed that the decreased rates of germination and growth (in terms of shoot and root lengths) by the salt stress were significantly increased by the SA application (SA + NaCl). The treatment of SA to the high and low saline soils enhanced the growth, yield and nutrient values of rice. The effects of SA on Na+, K+ and Cl- ionic accumulation were traced under salt stress condition by inductively coupled plasma optical emission spectrometry and ion chromatography. It was revealed that the increased accumulation of Na+ and Clˉ ions by the salt stress were reduced by SA application. An increased concentration of endogenous SA level was detected from the SA-treated rice varieties (ASD16 and BR26) by liquid chromatography electrospray Ionization-tandem mass spectrometry. The activities of antioxidant enzymes such as superoxide dismutase, catalase and peroxidase were increased by salt stress whereas decreased by the SA application. The study proved that the application of SA could alleviate the adverse effects of salt stress by the regulation of physiological mechanism in rice plants. In spite of salt stress, it can be applied to the coastal and estuarine regions to increase the rice production.
Key words： salicylic acid; salt tolerance; Oryza sativa; NaCl; germination; physiology
Jini D., Joseph B. . Physiological Mechanism of Salicylic Acid for Alleviation of Salt Stress in Rice[J]. Rice Science, 2017 , 24(2) : 97 -108 . DOI: 10.1016/j.rsci.2016.07.007
| 1 | Ali E A, Mahmoud A M.2013. Effect of foliar spray by different salicylic acid and zinc concentrations on seed yield and yield components of mungbean in sandy soil.Asian J Crop Sci, 5(1): 33-40. |
| 2 | Alonso-Ramirez A, Rodriguez D, Reyes D, Jimenez J A, Nicolas G, Lopez-Climent M, Gomez-Cadenas A, Nicolas C.2009. Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds.Plant Physiol, 150(3): 1335-1344. |
| 3 | Amor N B, Jiménez A, Megdiche W, Lundqvist M, Sevilla F, Abdelly C.2007. Kinetics of the anti-oxidant response to salinity in the halophyte Cakile maritima.J Int Plant Biol, 49(7): 982-992. |
| 4 | Asadi M, Heidari M A, Kazemi M, Filinejad A R.2013. Salicylic acid induced changes in some physiological parameters in chickpea (Cicer arietinum L.) under salt stress.J Agric Technol, 9(2): 311-316. |
| 5 | Ashraf M, Athar H R, Harris P J C, Kwon T R.2008. Some prospective strategies for improving crop salt tolerance.Adv Agron, 97: 45-110. |
| 6 | Ashraf M.2009. Biotechnological approach of improving plant salt tolerance using antioxidants as markers.Biotechnol Adv, 27(1): 84-93. |
| 7 | Azooz M M.2009. Salt stress mitigation by seed priming with salicylic acid in two faba bean genotypes differing in salt tolerance.Int J Agric Biol, 11(4): 343-350. |
| 8 | Azooz M M, Youssef A M, Ahmad P.2011. Evaluation of salicylic acid (SA) application on growth, osmotic solutes and antioxidant enzyme activities on broad bean seedlings grown under diluted seawater.Int J Plant Physiol Biochem, 3(14): 253-264. |
| 9 | Bagheri M Z.2014. The effect of maize priming on germination characteristics, catalase and peroxidase enzyme activity, and total protein content under salt stress.Int J Biosci, 4(2): 104-112. |
| 10 | Bauer P J.1981. Affinity and stoichiometry of calcium binding by arsenazo III.Anal Biochem, 110(1): 61-72. |
| 11 | Beers R F, Sizer I W.1952. Colorimetric method for estimation of catalase.J Biol Chem, 195: 133-139. |
| 12 | Borsani O, Valpuesta V, Botella M A.2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings.Plant Physiol, 126(3): 1024-1030. |
| 13 | Boukraâ D, Benabdelli K, Belabid L, Bennabi F.2013. Effect of salinity on chickpea seed germination pre-treated with salicylic acid.Scient J Biol Sci, 2(4): 86-93. |
| 14 | Bratovcic A, Odobasic A.2011. Determination of fluoride and chloride contents in drinking water by ion selective electrode. In: Ekundayo E. Environmental Monitoring. Croatla: InTech: 109-120. |
| 15 | Candan N, Tarhan L.2003. The correlation between antioxidant enzyme activities and lipid peroxidation levels in Mentha pulegium organs grown in Ca2+, Mg2+, Cu2+, Zn2+ and Mn2+ stress conditions.Plant Sci, 165(4): 769-776. |
| 16 | Chandra A, Anand A, Dubey A.2007. Effect of salicylic acid on morphological and biochemical attributes in cowpea.J Environ Biol, 28(2): 193-196. |
| 17 | Cha-um S, Vejchasarn P, Kirdmanee C.2007. An effective defensive response in Thai aromatic rice varieties (Oryza sativa L. spp. indica) to salinity.J Crop Sci Biotechnol, 10(4): 257-264. |
| 18 | Comba M E, Benavides M P, Tomaro M L.1998. Effect of salt stress on antioxidant defence system in soybean root nodules.Funct Plant Biol, 25(6): 665-671. |
| 19 | Conn S, Gilliham M.2010. Comparative physiology of elemental distributions in plants.Ann Bot, 105(7): 1081-1102. |
| 20 | Cuin T A, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S.2011. Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: In planta quantification methods.Plant Cell Environ, 34(6): 947-961. |
| 21 | Daly J A, Ertingshausen G.1972. Direct method for determining inorganic phosphate in serum with the ‘CentrifiChem’.Clin Chem, 18(3): 263-265. |
| 22 | Delavari P M, Baghizadeh A, Enteshari S H, Kalantari K M, Yazdanpanah A, Mousavi E A.2010. The effects of salicylic acid on some of biochemical and morphological characteristic of Ocimum basilicucm under salinity stress.Aust J Basic Appl Sci, 4(10): 4832-4845. |
| 23 | Demiral T, Türkan İ.2005. Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance.Environ Exp Bot, 53: 247-257. |
| 24 | El-Tayeb M A.2005. Response of barley grains to the interactive effect of salinity and salicylic acid.Plant Growth Regul, 45(3): 215-224. |
| 25 | Erdal S, Aydın M, Genisel M, Taspınar M S, Dumlupinar R, Kaya O, Gorcek Z.2013. Effects of salicylic acid on wheat salt sensitivity.Afr J Biotechnol, 10: 5713-5718. |
| 26 | Esfandiari E, Shekari F, Shekari F, Esfandiari M.2007. The effect of salt stress on antioxidant enzymes’ activity and lipid peroxidation on the wheat seedling.Not Bot Hort Agrobot Cluj, 35(1): 48-56. |
| 27 | Eyidogan F, Öz M T.2007. Effect of salinity on antioxidant responses of chickpea seedlings.Acta Physiol Plant, 29: 485-493. |
| 28 | Fariduddin Q, Hayat S, Ahmad A.2003. Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea.Photosynthetica, 41(2): 281-284. |
| 29 | Flowers T J.2004. Improving crop salt tolerance.J Exp Bot, 55: 307-319. |
| 30 | Foyer C H, Noctor G.2003. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria.Physiol Plant, 119(3): 355-364. |
| 31 | Fridovich I.1989. Superoxide dismutases: An adaptation to a paramagnetic gas.J Biol Chem, 264: 7761-7764. |
| 32 | 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.J Plant Physiol, 164(6): 728-736. |
| 33 | Hamayun M, Khan S A, Khan A L, Shinwari Z K, Hussain J, Sohn E Y, Kang S M, Kim Y H, Khan M A, Lee I J.2010. Effect of salt stress on growth attributes and endogenous growth hormones of soybean cultivar Hwangkeumkong.Pak J Bot, 42(5): 3103-3112. |
| 34 | Hayat Q, Hayat S, Irfan M, Ahmad A.2010. Effect of exogenous salicylic acid under changing environment: A review.Environ Exp Bot, 68(1): 14-25. |
| 35 | Hernandez J A, Jimenez A, Mullineaux P, Sevilia F.2000. Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences.Plant Cell Environ, 23(8): 853-862. |
| 36 | Hussain K, Nawaz K, Majeed A, Ilyas U, Lin F, Ali K, Nisar M F.2011. Role of exogenous salicylic acid applications for salt tolerance in violet.Sarhad J Agric, 27(2): 171-175. |
| 37 | Javaheri M, Mashayekhi K, Dadkhah A, Tavallaee F Z.2012. Effects of salicylic acid on yield and quality characters of tomato fruit (Lycopersicum esculentum Mill.).Int J Agric Crop Sci, 4(16): 1184-1187. |
| 38 | Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S.2013. Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel.J Exp Bot, 64(8): 2255-2268. |
| 39 | Joseph B, Jini D.2010. Insight into the role of antioxidant enzymes for salt tolerance in plants.Int J Bot, 6: 456-464. |
| 40 | Karlidag H, Yildirim E, Turan M.2009. Salicylic acid ameliorates the adverse effect of salt stress on strawberry.Scient Agric, 66(2): 180-187. |
| 41 | Kaya C, Tuna A, Yokaş I.2009. Salinity and Water Stress. Netherlands: Springer: 45-50. |
| 42 | Khan N, Syeed S, Masood A, Nazar R, Iqbal N.2010. Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress.Int J Plant Biol, 1: 1-8. |
| 43 | Khush G S.2005. What it will take to feed 5.0 billion rice consumers in 2030.Plant Mol Biol, 59(1): 1-6. |
| 44 | Kono Y, Fridovich I.1983. Inhibition and reactivation of Mn-catalase: Implications for valence changes at the active site manganese.J Biol Chem, 258: 13646-13648. |
| 45 | Lee S, Kim S G, Park C M.2010. Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis.New Phytol, 188(2): 626-637. |
| 46 | Levy G B.1981. Determination of sodium with ion-selective electrodes.Clin Chem, 27(8): 1435-1438. |
| 47 | Loewus F A.1952. Improvement in anthrone method for determination of carbohydrates.Anal Chem, 24(1): 219. |
| 48 | Lowry O H, Rosebrough N J, Farr A L, Randall R J.1951. Protein measurement with the folin phenol reagent.J Biol Chem, 193: 265-275. |
| 49 | Lüttge A, Läuchli U.2002. Salinity: Environment-Plants- Molecules. Netherlands: Springer: 3-20. |
| 50 | Ma H, Chong K, Deng X W.2007. Rice research: Past, present and future.J Integr Plant Biol, 49: 729-730. |
| 51 | Mansour M M F, Salama K H, Ali F Z M, Abou Hadid A F.2005. Cell and plant responses to NaCl in Zea mays L. cultivars differing in salt tolerance.Gen Appl Plant Physiol, 31: 29-41. |
| 52 | Marino R, Ponnaiah M, Krajewski P, Frova C, Gianfranceschi L, Pè M E, Sari-Gorla M.2009. Addressing drought tolerance in maize by transcriptional profiling and mapping.Mol Genet Genom, 281(2): 163-179. |
| 53 | Mason J L.1963. Flame photometric determination of potassium in unashed plant leaves.Anal Chem, 35(7): 874-875. |
| 54 | Mittler R.2002. Oxidative stress, antioxidants and stress tolerance.Trends Plant Sci, 7(9): 405-410. |
| 55 | Munns R.2002. Comparative physiology of salt and water stress.Plant, Cell Environ, 25(2): 239-250. |
| 56 | Munns R, Tester M.2008. Mechanisms of salinity tolerance.Annu Rev Plant Biol, 59: 651-681. |
| 57 | Noreen S, Ashraf M.2008. Alleviation of adverse effects of salt stress on sunflower (Helianthus annuus L.) by exogenous application of salicylic acid: Growth and photosynthesis.Pak J Bot, 40(4): 1657-1663. |
| 58 | Noreen S, Ashraf M, Hussain M, Jamil A.2009. Exogenous application of salicylic acid enhances antioxidative capacity in salt stressed sunflower (Helianthus annuus L.) plants.Pak J Bot, 41(1): 473-479. |
| 59 | Parizi M D, Kalantari K M, Enteshari S, Baghizadeh A.2011. Effect of salicylic acid and salt stress on Na and K content in Ocimum basilicum L.Iran J Plant Physiol, 1(3): 135-139. |
| 60 | Passardi F, Cosio C, Penel C, Dunand C.2005. Peroxidases have more functions than a Swiss army knife.Plant Cell Rep, 24: 255-265. |
| 61 | Patel P K, Hemantaranjan A.2012. Salicylic acid induced alteration in dry matter partitioning, antioxidant defence system and yield in chickpea (Cicer arietinum L.) under drought stress.Asian J Crop Sci, 4(3): 86-102. |
| 62 | Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D.2006. Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms.Plant Physiol, 141(3): 910-923. |
| 63 | Rodrı?guez-Navarro A.2000. Potassium transport in fungi and plants.Biochim Biophys Acta, 1469(1): 1-30. |
| 64 | Rodrıguez-Rosales M P, Kerkeb L, Bueno P, 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(2): 143-150. |
| 65 | Saeidnejad A H, Mardani H, Naghibolghora M.2012. Protective effects of salicylic acid on physiological parameters and antioxidants response in maize seedlings under salinity stress.J Appl Environ Biol Sci, 2(8): 364-373. |
| 66 | 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(5): 1037-1046. |
| 67 | Sakhabutdinova A R, Fatkhutdinova D R, Bezrukova M V, Shakirova F M.2003. Salicylic acid prevents the damaging action of stress factors on wheat plants.Bulg J Plant Physiol, 29: 314-319. |
| 68 | Sankar P D, Saleh M A A M, Selvaraj C I.2011. Rice breeding for salt tolerance.Res Biotechnol, 2(2): 1-10. |
| 69 | Seo M, Koshiba T.2011. Transport of ABA from the site of biosynthesis to the site of action.J Plant Res, 124(4): 501-507. |
| 70 | Shalata A, Mittova V, Volokita M, Guy M, Tal M.2001. Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: The root antioxidative system.Physiol Plant, 112(4): 487-494. |
| 71 | Simaei M, Khavari-Nejad R A, Bernard F.2012. Exogenous application of salicylic acid and nitric oxide on the ionic contents and enzymatic activities in NaCl-stressed soybean plants.Am J Plant Sci, 3: 1495-1503. |
| 72 | Siringam K, Juntawong N, Cha-um S, Kirdmanee C.2009. Relationships between sodium ion accumulation and physiological characteristics in rice (Oryza sativa L. spp. indica) seedlings grown under iso-osmotic salinity stress.Pak J Bot, 41(4): 1837-1850. |
| 73 | Sreenivasulu N, Grimm B, Wobus U, Weschke W.2000. Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedlings of foxtail millet (Setaria italica).Physiol Plant, 109(4): 435-442. |
| 74 | Storey R, Schachtman D P, Thomas M R.2003. Root structure and cellular chloride, sodium and potassium distribution in salinized grapevines.Plant, Cell Environ, 26(6): 789-800. |
| 75 | Sudhakar C, Lakshmi A, Giridarakumar S.2001. Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity.Plant Sci, 161(3): 613-619. |
| 76 | Szalai G, Páldi E, Janda T.2005. Effect of salt stress on the endogenous salicylic acid content in maize (Zea mays L.) plants.Acta Biol Szeged, 49: 47-48. |
| 77 | Tammam A A, Alhamd M F A, Hemeda M M.2008. Study of salt tolerance in wheat (Triticum aestivum L.) cultivar Banysoif 1.Aust J Crop Sci, 1(3): 115-125. |
| 78 | Torabian A R.2010. Effect of salicylic acid on germination and growth of alfalfa (Medicago sativa L.) seedlings under water potential loss at salinity stress.Plant Ecophysiol, 2(4): 151-155. |
| 79 | Tufail A, Arfan M, Gurmani A R, Khan A, Bano A.2013. Salicylic acid induced salinity tolerance in maize (Zea mays).Pak J Bot, 45: 75-82. |
| 80 | Turhan E, Eris A.2005. Effects of sodium chloride applications and different growth media on ionic composition in strawberry plant.J Plant Nutr, 27(9): 1653-1665. |
| 81 | van Reeuwijik L P.2002. Procedures for Soil Analysis. 6th edn. Wageningen, Netherlands: International Soil Reference and Information Centre. |
| 82 | Wada K C, Takeno K.2010. Stress-induced flowering.Plant Signal Behav, 5(8): 944-947. |
| 83 | Waheed A, Ahmad H, Abbasi F M.2012. Different treatment of rice seed dormancy breaking, germination of both wild species and cultivated varieties (Oryza sativa L.).J Mater Environ Sci, 3(3): 551-560. |
| 84 | Wang Y Y, Mopper S, Hasenstein K H.2001. Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona.J Chem Ecol, 27(2): 327-342. |
| 85 | Wheal M S, Fowles T O, Palmer L T.2011. A cost-effective acid digestion method using closed polypropylene tubes for inductively coupled plasma optical emission spectrometry (ICP-OES) analysis of plant essential elements.Anal Methods, 3: 2854-2863. |
| 86 | Xu C X, Liu Y L, Zheng Q S, Liu Z P.2006. Silicate improves growth and ion absorption and distribution in Aloe vera under salt stress.J Plant Physiol Mol Biol, 32(1): 73-78. |
| 87 | Xu X Y, McGrath S P, Meharg A A, Zhao F J.2008. Growing rice aerobically markedly decreases arsenic accumulation.Environ Sci Technol, 42(15): 5574-5579. |
| 88 | Zhao F Y, Zhang H.2006. Salt and paraquat stress tolerance results from co-expression of the Suaeda salsa glutathione S-transferase and catalase in transgenic rice.Plant Cell, Tiss Organ Cult, 86(3): 349-358. |
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