Protoplasma

, Volume 249, Issue 3, pp 769–778 | Cite as

Salicylic acid and calcium-induced protection of wheat against salinity

  • Mohamed H. Al-Whaibi
  • Manzer H. Siddiqui
  • Mohammed O. Basalah
Original Article
First Online:
Received:
Accepted:

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.

Keywords

Antioxidant system Calcium Carbonic anhydrase Photosynthetic pigments Proline Triticum aestivum Salicylic acid Salinity 

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

Notes

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.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126PubMedCrossRefGoogle Scholar
  2. 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 37–52Google Scholar
  3. Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Crit Revi Plant Sci 23:157–174CrossRefGoogle Scholar
  4. 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 32:85–100CrossRefGoogle Scholar
  5. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  6. Bethke PC, Jones RL (2001) Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J 25:19–29PubMedCrossRefGoogle Scholar
  7. Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 11:764–775CrossRefGoogle Scholar
  8. Chen WP, Silva H, Klessig RF (1993) Active oxygen species in the induction of plant systemic acquired resistance by SA. Science 262:1883–1886PubMedCrossRefGoogle Scholar
  9. 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 43:857–864CrossRefGoogle Scholar
  10. Cramer GR (2004) Sodium–calcium interactions under salinity stress. In: Läuchli A, Lüttge U (eds) Salinity: environment–plants–molecules. Kluwer, New York, pp 205–227CrossRefGoogle Scholar
  11. Dempsey DMA, Klessig DF (1994) Salicylic acid, active oxygen species and systemic acquired resistance in plants. Trends Cell Biol 4:334–338PubMedCrossRefGoogle Scholar
  12. Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil 40:445–451CrossRefGoogle Scholar
  13. EI-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224CrossRefGoogle Scholar
  14. 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 126:156–166PubMedCrossRefGoogle Scholar
  15. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefGoogle Scholar
  16. Ganesan V, Thomas G (2001) Salicylic acid response in rice: influence of salicylic acid on H2O2 accumulation and oxidative stress. Plant Sci 160:1095–1106PubMedCrossRefGoogle Scholar
  17. Gautam S, Singh PK (2009) Salicylic acid-induced salinity tolerance in corn grown under NaCl stress. Acta Physiol Plant 31:1185–1190CrossRefGoogle Scholar
  18. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314PubMedCrossRefGoogle Scholar
  19. 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 164:728–736PubMedCrossRefGoogle Scholar
  20. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  21. 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 45:988–995CrossRefGoogle Scholar
  22. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198PubMedCrossRefGoogle Scholar
  23. Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442PubMedCrossRefGoogle Scholar
  24. Iyer S, Caplan A (1998) Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiol 116:203–211CrossRefGoogle Scholar
  25. 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 208:175–180CrossRefGoogle Scholar
  26. 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 355:341–349CrossRefGoogle Scholar
  27. Kato M, Shimizu S (1985) Chlorophyll metabolism in higher plants VI. Involvement of peroxidase in chlorophyll degradation. Plant Cell Physiol 26:1291–1301Google Scholar
  28. 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 51:685–693PubMedCrossRefGoogle Scholar
  29. 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 3:685–695Google Scholar
  30. 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 32:121–132CrossRefGoogle Scholar
  31. Khodary SFA (2004) Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt-stressed maize plants. Int J Agric Biol 6:5–8Google Scholar
  32. 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 26:857–865PubMedCrossRefGoogle Scholar
  33. Klessig DF, Malamy J (1994) Salicylic acid signal in plants. Plant Mol Biol 26:1439–1448PubMedCrossRefGoogle Scholar
  34. Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324PubMedCrossRefGoogle Scholar
  35. Kuznetsov VV, Shevyakova NI (1999) Proline under stress: biological role, metabolism and regulation. Russ J Plant Physiol 46:274–287Google Scholar
  36. Lee H, León J, Raskin I (1995) Biosynthesis and metabolism of salicylic acid. Proc Natl Acad Sci USA 92:4076–4079PubMedCrossRefGoogle Scholar
  37. 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 3:654–656PubMedCrossRefGoogle Scholar
  38. 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 119:1091–1099PubMedCrossRefGoogle Scholar
  39. Malamy J, Carr JP, Klessig DF (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 25:1002–1004CrossRefGoogle Scholar
  40. Marschner H (2002) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  41. Matysik J, Alia BB, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532Google Scholar
  42. Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biol Plant 42:409–415CrossRefGoogle Scholar
  43. Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189CrossRefGoogle Scholar
  44. 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 41:315–317CrossRefGoogle Scholar
  45. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  46. 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 246:119–120Google Scholar
  47. Rane J, Lakkineni KC, Kumar PA, Abrol YP (1995) Salicylic acid protects nitrate reductase activity of wheat leaves. Plant Physiol Biochem 22:119–121Google Scholar
  48. 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 115:137–149PubMedCrossRefGoogle Scholar
  49. Raskin I (1992) Role of salicylic acid in plants. Ann Rev Plant Physiol Mol Biol 43:439–463CrossRefGoogle Scholar
  50. Raskin I, Skubatz H, Tang W, Meeuse BJD (1990) Salicylic acid levels in thermogenic and non-thermogenic plants. Ann Bot 66:369–373Google Scholar
  51. 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 20:50–55Google Scholar
  52. Sahu GK, Kar M, Sabat SC (2002) Electron transport activities of isolated thylakoids from wheat plants grown in salicylic acid. Plant Biol 4:321–328CrossRefGoogle Scholar
  53. 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 314–319Google Scholar
  54. Sanders D, Colin B, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706PubMedGoogle Scholar
  55. 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 164:151–162CrossRefGoogle Scholar
  56. 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 30:57–161CrossRefGoogle Scholar
  57. 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 164:317–322CrossRefGoogle Scholar
  58. 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 194:214–224CrossRefGoogle Scholar
  59. 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 4:67–80CrossRefGoogle Scholar
  60. 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 3:55–63Google Scholar
  61. 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 9:671–680CrossRefGoogle Scholar
  62. 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
  63. Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141CrossRefGoogle Scholar
  64. Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytol 94:537–548CrossRefGoogle Scholar
  65. 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 49:1329–1337Google Scholar
  66. Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206PubMedCrossRefGoogle Scholar
  67. 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 170:685–694CrossRefGoogle Scholar
  68. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Mohamed H. Al-Whaibi
    • 1
  • Manzer H. Siddiqui
    • 1
  • Mohammed O. Basalah
    • 1
  1. 1.Department of Botany and Microbiology, College of ScienceKing Saud UniversityRiyadhSaudi Arabia

Personalised recommendations