Syringaldazine Peroxidase Stimulates Lignification by Enhancing Polyamine Catabolism in Wheat during Heat and Drought Stress

Abstract

Six wheat cultivars, namely PBW 343, PBW 550 (stress susceptible), PBW 621, PBW 175 (drought tolerant), C 306 and HD 2967 (heat tolerant), were used in this study to evaluate the effect of heat and drought stress on the activities of peroxidases (POXs), diamine oxidase (DAO), polyamine oxidase (PAO) and arginine decarboxylase (ADC) and ornithine decarboxylase (ODC) in relation to contents of polyamines (PAs), lipid peroxide and lignin. High temperature (HT) elevated activities of syringaldazine peroxidase (SPX), guaiacol peroxidase (GPX) and coniferyl alcohol peroxidase (CPX) in heat tolerant cultivars while, drought stress accentuated ADC/ODC activities in drought tolerant cultivars. Both heat and drought stress enhanced activities of DAO and PAO alongwith contents of H2O2 in PBW 175 and C 306. Amongst studied POXs, SPX activity was relatively more and coincided well with lignin content under HT stress while, the levels of ADC/ODC paralleled with putrescine and spermidine contents under drought stress. Higher build up of thiobarbituric acid reactive substances in cultivars PBW 343 and PBW 550 indicated their membrane instability during both the stresses. Our results revealed that SPX mediated lignification leading to higher cell wall rigidity under heat stress and drought increased PAs involved in ROS scavenging due to presence of positive charges which can bind strongly to the negative charges in cellular components such as proteins and phospholipids and thereby stabilize the membranes under stress conditions.

References

  1. Asthir, B., Duffus, C.M., Smith, R.C. Spoor, W. 2002. Diamine oxidase is involved in H2O2 production in the chalazal cells during barley grain filling. J. Exp. Bot. 53:677–682.

    CAS  Article  Google Scholar 

  2. Asthir, B., Spoor, W., Duffus, C.M. 2004. Involvement of polyamine, diamine oxidase and polyamine oxidase in resistance of barley to Blumeria graminis f. Sp. hordei. Euphytica 136:307–312.

    CAS  Article  Google Scholar 

  3. Birecka, H., Bitonti, A.J., McCann, P.P. 1985. Assaying ornithine and arginine decarboxylase in some plant species. Plant Physiol. 79:509–514.

    CAS  Article  Google Scholar 

  4. Bouchereau, A., Aziz, A., Larher, F., Martin-Tanguy, J. 1999. Polyamines and environmental challenges: recent development. Plant Sci. 140:103–125.

    CAS  Article  Google Scholar 

  5. Denness, L., McKenna, J.F., Segonzac, C., Wormit, A., Madhou, P., Bennett, M., Mansfield, J., Zipfel, C., Hamann, T. 2011. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species and jasmonic acid dependent process in Arabidopsis. Plant Physiol. 156:1364–1374.

    CAS  Article  Google Scholar 

  6. Dhillon-Grewal, R., Virk, D.S., Mangat, B.K., Basra, R.K., Basra, A.S. 1992. Polyamine levels in anthers of poly-cytoplasmic isonuclear male sterile lines of pearl millet. Bot. Bull. Acad. Sin. 33:97–100.

    CAS  Google Scholar 

  7. Duan, J.J., Li, J., Guo, S., Kang, Y. 2008. Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity. J. Plant Physiol. 165:1620–1635.

    CAS  Article  Google Scholar 

  8. Gao, J.M., Xiao, Q., Ding, L.P., Chen, M.J., Yin, L., Li, J.Z., Zhou, S.Y., He, G.Y. 2008. Differential responses of lipid peroxidation and antioxidants in Alternanthera phioxeroides and Oryza sativa subjected to drought stress. Plant Growth Regul. 56:89–95.

    CAS  Article  Google Scholar 

  9. Goyal, M., Asthir, B. 2010. Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress. Plant Growth Regul. 60:13–25.

    CAS  Article  Google Scholar 

  10. Groppa, M.D., Benavides, M.P. 2008. Polyamines and abiotic stress: recent advance. Amino Acids 34:35–45.

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  12. Hu, W.H., Xiao, Y.A., Zeng, J.J., Hu, X.H. 2010. Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses. Biol. Plant. 54:761–765.

    CAS  Article  Google Scholar 

  13. Iannone, M.F., Rosales, E.P., Groppa, M.D., Benavides, M.P. 2013. H2O2 involvement in polyamine-induced cell death in tobacco leaf discs. J. Plant Growth Regul. 32:745–757.

    CAS  Article  Google Scholar 

  14. Kotak, S., Larkindale, J., Lee, U., von Koskull-Doring, P., Vierling, E., Scharf, K.D. 2007. Complexity of heat stress response in plants. Curr. Opin. Plant Biol. 10:310–316.

    CAS  Article  Google Scholar 

  15. Kumar, S., Kaur, R., Kaur, N., Bhandhari, K., Kaushal, N., Gupta, K., Bains, T.S., Nayyar, H. 2011. Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiol. Plant. 33:2091–2101.

    CAS  Article  Google Scholar 

  16. Lee, T.M, Lin, Y.H. 1995. Changes in soluble and cell wall-bound peroxidase activities with growth in anoxia-treated rice (Oryza sativa L.) coleoptiles and roots. Plant Sci. 106:1–7.

    CAS  Article  Google Scholar 

  17. Lin, C.C., Kao, C.H. 2001. Cell wall peroxidase activity, hydrogen peroxidase level and NaCl-inhibited root growth of rice seedling. Plant Soil. 230:135–143.

    CAS  Article  Google Scholar 

  18. Liu, H.P., Dong, B.H., Zhang, Y., Liu, Z.P., Liu, Y.L. 2010. Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Sci. 166:1261–1267.

    Article  Google Scholar 

  19. Liu, J.H., Kitashiba, H., Wang, J., Ban, Y., Moriguchi, T. 2007. Polyamine and their ability to provide environmental stress tolerance to plants. Plant Biotechnol. 24:117–126.

    CAS  Article  Google Scholar 

  20. Liu, J.H., Wang, W., Wu, H., Gong, X., Moriguchi, T. 2015. Polyamines function in stress tolerance: from synthesis to regulation Front. Plant Sci. 6:827.

    Google Scholar 

  21. Magda, P., Szalai, G., Janda, T. 2015. Speculation: Polyamines are important in abiotic stress signalling. A review. Plant Sci. 237:16–23.

    Google Scholar 

  22. Nakashima, J., Chen, F., Jackson, L., Shadle, G., Dixon, R.A. 2008. Multi-site genetic modification of monolignol biosynthesis in alfalfa (Medicago sativa): effects on lignin composition in specific cell types. New Phytol. 179:738–750.

    CAS  Article  Google Scholar 

  23. Oktem, H.A., Eyidooan, F., Demirba, D., Bayrac, A.T., Oz, M.T., Ozgur, E., Selcuk, F., Yucel, M. 2008. Antioxidant responses of lentil to cold and drought stress. J. Plant Biochem. Biotechnol. 17:15–21.

    CAS  Article  Google Scholar 

  24. Pathak, M.R., da Silva, J.A.T., Wani, S.H. 2014. Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops and Food 5:87–96.

    Article  Google Scholar 

  25. Quiroga, M., Guerrero, C., Botella, M.A., Barcelo, A., Amaya, I., Medina, M.I., Alonso, F.J., Forchetti, S.M., Tigier, H., Valpuesta, V. 2000. A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol. 122:1119–1127.

    CAS  Article  Google Scholar 

  26. Ros-Barcelo, A., Pomar, F., Lopes-Serrano, M., Martinez, P., Pendreno, M.A. 2002. Developmental regulation of the H2O2 producing system and basic peroxidase isoenzyme in the Zinnia elegans lignifying xylem. Plant Physiol. Biochem. 40:325–332.

    CAS  Article  Google Scholar 

  27. Savidge, R., Udagama-Randeniya, P. 1992. Cell-wall-bound coniferyl alcohol oxidase associated with lignification in conifers. Phytochem. 31:2959–2966.

    CAS  Article  Google Scholar 

  28. Sergiev, I., Alexieva, V., Karanov, E. 1997. Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. C. R. Acad. Bulg. Sci. 51:121–124.

    Google Scholar 

  29. Shu, S., Yuan, Y., Chen, J., Jin, S., Zhang, W., Tang, Y., Zhong, M., Guo, S. 2015. The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress. Scientific Reports DOI: 10.1038/srep14390

  30. Suzuki, N., Mittler, R. 2006. Reactive oxygen species and temperature stresses: a delicate balance between signalling and destruction. Physiol. Plant. 126:45–51.

    CAS  Article  Google Scholar 

  31. Tao, S., Khanizadeh, S., Zhang, H., Zhang, S. 2009. Anatomy, ultrastructure and lignin distribution of stone cells in two Pyrus species, Plant Sci. 176:413–419.

    CAS  Article  Google Scholar 

  32. Zao, F.G., Liu, Y.L. 2000. Study on determination of ADC and TGase activities. Plant Physiol. Commun. 36:442–444.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to B. Asthir.

Additional information

Communicated by A. Pécsváradi

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bala, S., Asthir, B. & Bains, N.S. Syringaldazine Peroxidase Stimulates Lignification by Enhancing Polyamine Catabolism in Wheat during Heat and Drought Stress. CEREAL RESEARCH COMMUNICATIONS 44, 561–571 (2016). https://doi.org/10.1556/0806.44.2016.028

Download citation

Keywords

  • arginine decarboxylase
  • lignin
  • membrane stability
  • ornithine decarboxylase
  • peroxidases