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Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

Treatment with 0.5 mM salicylic acid (SA) significantly alleviated growth inhibition induced by drought in wheat seedlings, manifested by less decreassed fresh mass, dry mass, plant height, root length, and less increased lipid peroxidation. Under drought stress, SA significantly increased the content of ascorbate (ASA) and glutathione (GSH). We determined the full-length cDNA sequences of genes encoding the glutathione-S-transferase 1 (GST1) and 2 (GST2) and we also measured the transcription of eight genes related to ASA-GSH cycle. The results indicated that exogenous SA significantly enhanced the transcription of GST1, GST2, glutathione reductase (GR), and monodehydroascorbate reductase (MDHAR) genes during almost the entire drought period, but only increased those of dehydroascorbate reductase (DHAR) at 12 h, glutathione peroxidase (GPX1) at 48 h, phospholipid hydroperoxide glutathione peroxidase (GPX2) at 12 and 24 h, and glutathione synthetase (GSHS) at 12, 24, and 48 h. This implies that SA alleviates the detrimental effects of drought stress on wheat seedling growth by influencing the ASA-GSH cycle.

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Abbreviations

ASA:

ascorbate

CAT:

catalase

DHAR:

dehydroascorbate reductase

GPX:

glutathione peroxidase

GR:

glutathione reductase

GSH:

glutathione

GSHS:

glutathione synthetase

GST:

glutathione-S-transferase

MDA:

malondialdehyde

MDHAR:

monodehydroascorbate reductase

POX:

peroxidase

qPCR:

quantitative real-time PCR

RACE:

the rapid amplification of cDNA ends

ROS:

reactive oxygen species

SA:

salicylic acid

SOD:

superoxide dismutase

References

  • Asada, K.: The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. — Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 601–639, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Ashraf, M., Akram, N.A., Arteca, R.N., Foolad, M.R.: The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. — Crit. Rev. Plant Sci. 29: 162–190, 2010.

    Article  CAS  Google Scholar 

  • Bai, T.H., Li, C.Y., Ma, F.W., Shu, H.R., Han, M.Y.: Exogenous salicylic acid alleviates growth inhibition and oxidative stress induced by hypoxia stress in Malus robusta Rehd. — J. Plant Growth Regul. 28: 358–366, 2009.

    Article  CAS  Google Scholar 

  • Chen, S., Liu, Z., Cui, J., Ding, J., Xia, X., Liu, D., Yu, J.: Alleviation of chilling-induced oxidative damage by salicylic acid pretreatment and related gene expression in eggplant seedlings. — Plant Growth Regul. 65: 101–108, 2011.

    Article  CAS  Google Scholar 

  • Clarke, S.M., Mur, L.A.J., Wood, J.E., Scott, I.M.: Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. — Plant J. 38: 432–447, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Ding, C.K., Wang, C.Y., Gross, K.C., Smith, D.L.: Jasmonate and salicylate induce the expression of pathogenesis-related protein genes and increase resistance to chilling injury in tomato fruit. — Planta 214: 895–901, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Doyle, A.D., Fischer. R.A.: Dry matter accumulation and water use relationships in wheat crops. — Aust. J. agr. Res. 30: 815–829, 1979.

    Article  Google Scholar 

  • EI-Tayeb, M.A.: Response of barley grains to the interactive effect of salinity and salicylic acid. — Plant Growth Regul. 45: 215–224, 2005.

    Article  Google Scholar 

  • Elberse, I.A.M., Van Damme, J.M.M., Van Tienderen, H.P.: Plasticity of growth characteristics in wild barley (Hordeum spontaneum) in response to nutrient limitation. — J. Ecol. 91: 371–382, 2003.

    Article  Google Scholar 

  • Gao, L., Yan, X., Li, X., Guo, G., Hu, Y., Ma, W., Yan, Y.: Proteome analysis of wheat leaf under salt stress by two-dimensional difference gel electrophoresis (2D-DIGE). — Phytochemistry 72: 1180–1181, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Hayata, Q., Hayata, S., Irfan, M., Ahmad, A.: Effect of exogenous salicylic acid under changing environment: a review. — Environ. exp. Bot. 68: 14–25, 2010.

    Article  Google Scholar 

  • He, Y., Zhu Z.J.: Exogenous salicylic acid alleviates NaCl toxicity and increases antioxidative enzyme activity in Lycopersicon esculentum. — Biol. Plant. 52: 792–795, 2008.

    Article  CAS  Google Scholar 

  • Horváth, E., Pál, M., Szalai, G, Páldi, E., Janda, T.: Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. — Biol. Plant. 51: 480–487, 2007a.

    Article  Google Scholar 

  • Horváth, E., Szalai, G., Janda, T.: Induction of abiotic stress tolerance by salicylic acid signaling. — J. Plant Growth Regul. 26: 290–300, 2007b.

    Google Scholar 

  • Kampfenkel, K., Van Montagu, M., Inze, D.: Extraction and determination of ascorbate and dehydroascorbate from plant tissue. — Anal. Biochem. 225: 165–167, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Kang, G.Z., Wang, C.H., Sun, G.C., Wang, Z.X.: Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. — Environ. exp. Bot. 50: 9–15, 2003.

    Article  CAS  Google Scholar 

  • Kang, H.M., Saltveit, M.E.: Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. — Physiol. Plant. 115: 571–576, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Kim, H., Mun, J.H., Byun, B.H., Hwang, H.J., Kwon, Y.M., Kim, S.G.: Molecular cloning and characterization of the gene encoding osmotin protein in Petunia hybrida. — Plant Sci. 162: 745–752, 2002.

    Article  CAS  Google Scholar 

  • Kuźniak, E., Skłodowska, M.: Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. — Plant Sci. 160: 723–731, 2001.

    Article  PubMed  Google Scholar 

  • Li, M., Liang, D., Pu, F., Ma, F., Hou, C., Liu, T.: Ascorbate levels and the activity of key enzymes in ascorbate biosynthesis and recycling in the leaves of 22 Chinese persimmon cultivars. — Sci. Hort. 120: 250–256, 2009.

    Article  CAS  Google Scholar 

  • Li, Y.H., Liu, Y.J., Xu, X.L., Jin, M., An, L.Z., Zhang, H.: Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana. — Biol. Plant. 56: 187–191, 2012.

    Article  Google Scholar 

  • Liu, Y., Yuan, Y., Liu, Y., Fu, J., Zheng, J., Wang, G.: Gene families of maize glutathione-ascorbate redox cycle respond differently to abiotic stresses. — J. Plant Physiol. 169: 183–192, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. — Methods 25: 402–408, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Ma, Y.H., Ma, F.W., Zhang, J.K., Li, M.Y., Wang, Y.H., Liang, D.: Effects of high temperature on activities and gene expression of enzymes involved in ascorbate-glutathione cycle in apple leaves. — Plant Sci. 175: 761–766, 2008.

    Article  CAS  Google Scholar 

  • Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Mutlu, S., Atici, Ö., Nalbantoglu, B.: Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. — Biol. Plant. 53: 334–338, 2009.

    Article  CAS  Google Scholar 

  • Prabhavathi, V.R., Rajam, M.V.: Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. — Plant Biotechnol. J. 24: 273–282, 2007.

    Article  CAS  Google Scholar 

  • Saruhan, N., Saglam, A., Kadioglu, A.: Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. — Acta Physiol. Plant 34: 97–106, 2012.

    Article  CAS  Google Scholar 

  • Senaratna, T., Touchell, D., Bunn, E., Dixon, K.: Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. — Plant Growth Regul. 30: 157–161, 2000.

    Google Scholar 

  • Shan, C., Liang, Z.: Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. — J. Plant Physiol. 178: 130–139, 2010.

    CAS  Google Scholar 

  • Smirnoff, N.: Plant resistance to environmental stress. — Curr. Opin. Biotechnol. 9: 214–219, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Smith, I.: Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. — Plant Physiol. 79: 1044–1047, 1985.

    Article  PubMed  CAS  Google Scholar 

  • Snyman, M., Cronjé, M.J.: Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. — J. exp. Bot. 59: 2125–2132, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Thapa, G., Dey, M., Sahoo, L., Panda, S.K.: An insight into the drought stress induced alterations in plants. — Biol. Plant. 55: 603–613, 2011.

    Article  CAS  Google Scholar 

  • Zheng, Y.H., Jia, A.J., Ning, T.Y., Xu, J.L., Li, Z.J., Jiang, G.M.: Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance. — J. Plant Physiol. 165: 1455–1465, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, Z.S., Guo, K., Elbaz, A., Yang, Z.M.: Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. — Environ. exp. Bot. 65: 27–34, 2009.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Key Laboratory of Physiology, Ecology and Genetic Improvement of Food Crops in Henan Province, Henan Agricultural University, Zhengzhou, 450002, P.R. China

    G. Z. Kang, G. Z. Li, G. Q. Liu, W. Xu, X. Q. Peng, C. Y. Wang, Y. J. Zhu & T. C. Guo

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  1. G. Z. Kang
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  2. G. Z. Li
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  3. G. Q. Liu
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  4. W. Xu
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  5. X. Q. Peng
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  6. C. Y. Wang
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  7. Y. J. Zhu
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  8. T. C. Guo
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Corresponding authors

Correspondence to G. Z. Kang or T. C. Guo.

Additional information

Acknowledgements: This study was financially supported by the Open Item of the State Key Laboratory of Plant Cell and Chromosome Engineering (2010-PCCE-KF-02), the Open Item of the State Key Laboratory of Crop Genetics and Gerplasm Enhancement (ZW2009003) and the National Basic Research Program of China (2009CB118602). We would like to thank to Dr. Jianwu Li for his valuable suggestions on the revised manuscript.

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Kang, G.Z., Li, G.Z., Liu, G.Q. et al. Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. Biol Plant 57, 718–724 (2013). https://doi.org/10.1007/s10535-013-0335-z

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  • DOI: https://doi.org/10.1007/s10535-013-0335-z

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