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Salicylic acid and calcium-induced protection of wheat against salinity

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Abstract

Soil salinity is one of the important environmental factors that produce serious agricultural problems. The objective of the present study was to determine the interactive effect of salicylic acid (SA) and calcium (Ca) on plant growth, photosynthetic pigments, proline (Pro) concentration, carbonic anhydrase (CA) activity and activities of antioxidant enzymes of Triticum aestivum L. (cv. Samma) under salt stress. Application of 90 mM of NaCl reduced plant growth (plant height, fresh weight (FW) and dry weight (DW), chlorophyll (Chl) a, Chl b, CA activity) and enhanced malondialdehyde (MDA) and Pro concentration. However, the application of SA or Ca alone as well as in combination markedly improved plant growth, photosynthetic pigments, Pro concentration, CA activity and activities of antioxidant enzymes peroxidase (POD), catalase (CAT), superoxide dismutase (SOD), glutathione reductase (GR) and ascorbate peroxidase (APX) under salt stress. It was, therefore, concluded that application of SA and Ca alone as well as in combination ameliorated the adverse effect of salinity, while combined application proved more effective to reduce the oxidative stress generated by NaCl through reduced MDA accumulation, Chl a/b ratio and Chls degradation and enhanced activities of antioxidant enzymes.

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Abbreviations

FW:

Fresh weight

DW:

Dry weight

Chl:

Chlorophyll

Pro:

Proline

MDA:

Malondialdehyde

CA:

Carbonic anhydrase

CAT:

Catalase

POD:

Peroxidase

SOD:

Superoxide dismutase

GR:

Glutathione reductase

APX:

Ascorbate peroxidase

EDTA:

Ethylenediaminetetraacetic acid

NBT:

Nitro blue tetrazolium

NADPH:

Nicotinamide adenine dinucleotide phosphate-oxidase

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  • Asada K, Endo T, Mano J, Miyake C (1998) Molecular mechanism for relaxation of and protection from light stress. In: Saton K, Murata N (eds) Stress responses of photosynthetic organisms. Elsevier, Amsterdam, pp 37–52

    Google Scholar 

  • Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Crit Revi Plant Sci 23:157–174

    Article  CAS  Google Scholar 

  • Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bethke PC, Jones RL (2001) Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J 25:19–29

    Article  PubMed  CAS  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 11:764–775

    Article  Google Scholar 

  • Chen WP, Silva H, Klessig RF (1993) Active oxygen species in the induction of plant systemic acquired resistance by SA. Science 262:1883–1886

    Article  PubMed  CAS  Google Scholar 

  • Cramer GR (1992) Kinetics of maize leaf elongation. II. Response of a Na-excluding cultivar and a Na-including cultivar to varying Na/Ca salinities. J Exp Bot 43:857–864

    Article  Google Scholar 

  • Cramer GR (2004) Sodium–calcium interactions under salinity stress. In: Läuchli A, Lüttge U (eds) Salinity: environment–plants–molecules. Kluwer, New York, pp 205–227

    Chapter  Google Scholar 

  • Dempsey DMA, Klessig DF (1994) Salicylic acid, active oxygen species and systemic acquired resistance in plants. Trends Cell Biol 4:334–338

    Article  PubMed  CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil 40:445–451

    Article  CAS  Google Scholar 

  • EI-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224

    Article  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that metabolize reactive oxygen species in barley aleurone cells are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Ganesan V, Thomas G (2001) Salicylic acid response in rice: influence of salicylic acid on H2O2 accumulation and oxidative stress. Plant Sci 160:1095–1106

    Article  PubMed  CAS  Google Scholar 

  • Gautam S, Singh PK (2009) Salicylic acid-induced salinity tolerance in corn grown under NaCl stress. Acta Physiol Plant 31:1185–1190

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, 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 164:728–736

    Article  PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • He Y, Liu Y, Cao W, Huai M, Xu B, Huang B (2005) Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentuky Blue grass. Crop Sci 45:988–995

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442

    Article  PubMed  CAS  Google Scholar 

  • Iyer S, Caplan A (1998) Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiol 116:203–211

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

    Article  CAS  Google Scholar 

  • Jiang Y, Huang B (2001) Effect of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 355:341–349

    Article  Google Scholar 

  • Kato M, Shimizu S (1985) Chlorophyll metabolism in higher plants VI. Involvement of peroxidase in chlorophyll degradation. Plant Cell Physiol 26:1291–1301

    CAS  Google Scholar 

  • Kawano T, Muto S (2000) Mechanism of peroxidase actions for salicylic acid–induced generation of active oxygen species and an increase in cytosolic calcium in tobacco cell suspension culture. J Exp Bot 51:685–693

    Article  PubMed  CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Khan MMA, Naeem M (2007) Salinity induced changes in growth, enzyme activities, photosynthesis, proline accumulation and yield in linseed genotypes. World J Agri Sci 3:685–695

    Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2010) 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

    Article  Google Scholar 

  • Khodary SFA (2004) Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt-stressed maize plants. Int J Agric Biol 6:5–8

    CAS  Google Scholar 

  • Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865

    Article  PubMed  Google Scholar 

  • Klessig DF, Malamy J (1994) Salicylic acid signal in plants. Plant Mol Biol 26:1439–1448

    Article  PubMed  CAS  Google Scholar 

  • Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov VV, Shevyakova NI (1999) Proline under stress: biological role, metabolism and regulation. Russ J Plant Physiol 46:274–287

    CAS  Google Scholar 

  • Lee H, León J, Raskin I (1995) Biosynthesis and metabolism of salicylic acid. Proc Natl Acad Sci USA 92:4076–4079

    Article  PubMed  CAS  Google Scholar 

  • Li A, Wang X, Leseberg CH, Jia J, Mao L (2008) Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.). Plant Signal Behav 3:654–656

    Article  PubMed  Google Scholar 

  • Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidant defense system, pigment composition and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1099

    Article  PubMed  CAS  Google Scholar 

  • Malamy J, Carr JP, Klessig DF (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 25:1002–1004

    Article  Google Scholar 

  • Marschner H (2002) Mineral nutrition of higher plants, 2nd edn. Academic, London

    Google Scholar 

  • Matysik J, Alia BB, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biol Plant 42:409–415

    Article  CAS  Google Scholar 

  • Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189

    Article  CAS  Google Scholar 

  • Moharekar ST, Moharekar SDL, Hara T, Tanaka R, Tanaka A, Chavan PD (2003) Effect of salicylic acid on chlorophyll and carotenoid contents of wheat and moong seedlings. Photosynthetica 41:315–317

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Pál M, Szalai G, Horvath E, Janda T, Paldi E (2002) Effect of salicylic acid during heavy metal stress. Proceedings of the seventh Hungarian congress on plant physiology. Acta Biol Szegediensis 246:119–120

    Google Scholar 

  • Rane J, Lakkineni KC, Kumar PA, Abrol YP (1995) Salicylic acid protects nitrate reductase activity of wheat leaves. Plant Physiol Biochem 22:119–121

    Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress and H2O2 metabolizing enzymes. Plant Physiol 115:137–149

    Article  PubMed  CAS  Google Scholar 

  • Raskin I (1992) Role of salicylic acid in plants. Ann Rev Plant Physiol Mol Biol 43:439–463

    Article  CAS  Google Scholar 

  • Raskin I, Skubatz H, Tang W, Meeuse BJD (1990) Salicylic acid levels in thermogenic and non-thermogenic plants. Ann Bot 66:369–373

    CAS  Google Scholar 

  • Reddy MP, Vora AB (1986) Changes in pigment composition, Hill reaction activity and saccharides metabolism in bajra (Pennisetumtyphoides S&H) leaves under NaCl salinity. Photosynthetica 20:50–55

    CAS  Google Scholar 

  • Sahu GK, Kar M, Sabat SC (2002) Electron transport activities of isolated thylakoids from wheat plants grown in salicylic acid. Plant Biol 4:321–328

    Article  CAS  Google Scholar 

  • Sakhabutdinova AR, Fatkhutdinova DR, Bezrukova MV, Shakirova FM (2003) Salicylic acid prevents the damaging action of stress factors on wheat plants. Bulg J Plant Physiol 314–319

  • Sanders D, Colin B, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706

    PubMed  CAS  Google Scholar 

  • Seeman JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behavior and photosynthetic capacity of salt-sensitive species Phaseolus vulgaris (L.). Planta 164:151–162

    Article  Google Scholar 

  • Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:57–161

    Article  Google Scholar 

  • Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fathutdinova RA, Fathutdinova DR (2003) Changes in hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164:317–322

    Article  CAS  Google Scholar 

  • Siddiqui MH, Khan MN, Mohammad F, Khan MMA (2008) Role of nitrogen and gibberellic acid (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J Agron Crop Sci 194:214–224

    Article  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN (2009a) Morphological and physio-biochemical characterization of Brassica juncea L. Czern.&Coss. genotypes under salt stress. J Plant Interact 4:67–80

    Article  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN, Naeem M, Khan MMA (2009b) Differential response of salt-sensitive and salt-tolerant Brassica juncea genotypes to N application: enhancement of N-metabolism and anti-oxidative properties in the salt-tolerant type. Plant Stress 3:55–63

    Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN, Al-Whaib MH, Bahkali AHA (2010) Nitrogen in relation to photosynthetic capacity and accumulation of osmoprotectant and nutrients in Brassica genotypes grown under salt stress. Agr Sci China 9:671–680

    Article  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MMA, Al-Whaibi MH (2011) Cumulative effect of nitrogen and sulphur on Brassica juncea L. genotypes under NaCl stress. Protoplasma. doi:10.1007/s00709-011-0273-6

  • Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141

    Article  CAS  Google Scholar 

  • Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytol 94:537–548

    Article  CAS  Google Scholar 

  • Soussi M, Ocana A, Lluch C (1998) Effect of salt stress on growth, photosynthesis and nitrogen fixation in chickpea (Cicer arietinum L.). J Exp Bot 49:1329–1337

    CAS  Google Scholar 

  • Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  PubMed  CAS  Google Scholar 

  • Wang LJ, Li SH (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694

    Article  CAS  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Professor Firoz Mohammad (Plant Physiology Section, Department of Botany, Aligarh Muslim University, Aligarh) and the anonymous reviewers for their valuable suggestions and critical reading of the manuscript. The financial support by the Deanship of Scientific Research of King Saud University, Riyadh, KSA though the Research Group No. RGP-VPP-153 is gratefully acknowledged.

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The authors declare that they have no conflict of interest.

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Correspondence to Manzer H. Siddiqui.

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Al-Whaibi, M.H., Siddiqui, M.H. & Basalah, M.O. Salicylic acid and calcium-induced protection of wheat against salinity. Protoplasma 249, 769–778 (2012). https://doi.org/10.1007/s00709-011-0322-1

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