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MAPKs as a cross point in H2O2 and auxin signaling under combined cadmium and zinc stress in rice roots

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Abstract

Previously, we have reported the role of MAPKs (mitogen-activated protein kinases) under cadmium stress. This work continue to explore the relationship between MAPKs, H2O2, auxin signaling, and OsHMA and OsZIP gene expression in rice (Oryza sativa L.) roots under combined cadmium (Cd) and zinc (Zn) stress. Compared with Cd, Cd+Zn reduced Cd levels but increased Zn accumulation in the roots. Three OsMAPK genes were negatively regulated, while two OsHMA and two OsZIP genes were positively regulated by MAPK pathways under Cd+Zn stress. Transgenic rice expressing DR5-GUS exhibited enhanced GUS activity in H2O2-, PD (MAPKK inhibitor PD98059)-, or (Cd+Zn)-treated roots, which also exhibited increased H2O2 concentrations, whereas GUS staining decreased in roots in response to Cd+Zn+PD, DMTU (N,N′-dimethylthiourea, a H2O2 scavenger), or Cd+Zn+DMTU treatment, with reduced H2O2 levels. GUS levels were consistent with H2O2 levels, suggesting that MAPK pathway-mediated auxin redistribution occurs via H2O2, and H2O2 functions downstream of MAPK but upstream of auxin signaling pathways. Furthermore, MAPK pathways serve specific functions in regulating the expression of some key genes of auxin signaling (OsYUCCA, OsPIN, OsARF, and OsIAA) under Cd+Zn stress. Overall, MAPK cascades function in the integration of metal transport, H2O2 generation, and auxin signaling in rice seedlings grown under Cd+Zn stress.

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Abbreviations

JA:

jasmonic acid

MAPK:

mitogen-activated protein kinase

PD:

PD 98059

References

  1. Ishimaru, Y., Suzuki, M., Kobayashi, T., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K., OsZIP4, a novel zinc-regulated zinc transporter in rice, J. Exp. Bot., 2005, vol. 56, pp. 3207–3214.

    Article  CAS  PubMed  Google Scholar 

  2. Ebbs, S.D. and Kochian, L.V., Toxicity of zinc and copper to Brassica species: implications for phytoremediation, J. Environ. Qual., 1997, vol. 26, pp. 776–781.

    Article  CAS  Google Scholar 

  3. Cherif, J., Mediouni, C., Ben Ammar, W., and Jemal, F., Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum), J. Environ. Sci. (China), 2011, vol. 23, pp. 837–844.

    Article  CAS  Google Scholar 

  4. Agrawal, G.K., Tamogami, S., Iwahashi, H., Agrawal, V.P., and Rakwal, R., Transient regulation of jasmonic acidinducible rice MAP kinase gene (OsBWMK1) by diverse biotic and abiotic stresses, Plant Physiol. Biochem., 2003, vol. 41, pp. 355–361.

    CAS  Google Scholar 

  5. Lin, C.W., Chang, H.B., and Huang, H.J., Zinc induces mitogen-activated protein kinase activation mediated by reactive oxygen species in rice roots, Plant Physiol. Biochem., 2005, vol. 43, pp. 963–968.

    CAS  PubMed  Google Scholar 

  6. Jeong, M.J., Lee, S.K., Kim, B.G., Kwon, T.R., Cho, W.S., Park, Y.T., Lee, J.O., Kwon, H.B., Byun, M.O., and Park, S.C., A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses, Plant Cell, Tissue Organ Cult., 2006, vol. 85, pp. 151–160.

    Article  CAS  Google Scholar 

  7. Agrawal, G.K., Agrawal, S.K., Shibato, J., Iwahashi, H., and Rakwal, R., Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation, Biochem. Biophys. Res. Commun., 2003, vol. 300, pp. 775–783.

    Article  CAS  PubMed  Google Scholar 

  8. Hung, W.C., Huang, D.D., Yeh, C.M., and Huang, H.J., Reactive oxygen species, calcium and serine/threonine phosphatase are required for copperinduced MAP kinase gene, OsMAPK2, expression in rice, Plant Growth Regul., 2005, vol. 45, pp. 233–241.

    Article  CAS  Google Scholar 

  9. Yeh, C.M., Chien, P.S., and Huang, H.J., Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots, J. Exp. Bot., 2007, vol. 58, pp. 659–671.

    Article  CAS  PubMed  Google Scholar 

  10. Zhao, F.Y., Hu, F., Zhang, S.Y., Wang, K., Zhang, C.R., and Liu, T., MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice, Environ. Sci. Pollut. Res., 2013, vol. 20, pp. 5449–5460.

    Article  CAS  Google Scholar 

  11. Mishra, N.S., Tuteja, R., and Tuteja, N., Signaling through MAP kinase networks in plants, Arch. Biochem. Biophys., 2006, vol. 452, pp. 55–68.

    Article  CAS  PubMed  Google Scholar 

  12. Kovtun, Y., Chiu, W.L., Zeng, W., and Sheen, J., Suppression of auxin signal transduction by a MAPK cascade in higher plants, Nature, 1998, vol. 395, pp. 716–720.

    Article  CAS  PubMed  Google Scholar 

  13. Lee, J.S., Wang, S., Sritubtim, S., Chen, J.G., and Ellis, B.E., Arabidopsis mitogen-activated protein kinase MAPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling, Plant J., 2009, vol. 57, pp. 975–985.

    Article  CAS  PubMed  Google Scholar 

  14. Mizoguchi, T., Gotoh, Y., Nishida, E., Yamaguchi-Shinozaki, K., Hayashida, N., Iwasaki, T., Kamada, H., and Shinozaki, K., Characterization of two cDNAs that encode MAP kinase homologues in Arabidopsis thaliana and analysis of the possible role of auxin in activating such kinase activities in cultured cells, Plant J., 1994, vol. 5, pp. 111–122.

    Article  CAS  PubMed  Google Scholar 

  15. Mockaitis, K. and Howell, S.H., Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings, Plant J., 2000, vol. 24, pp. 785–796.

    Article  CAS  PubMed  Google Scholar 

  16. Tena, G. and Renaudin, J.P., Cytosolic acidification but not auxin at physiological concentration is an activator of MAP kinases in tobacco cells, Plant J., 1998, vol. 16, pp. 173–182.

    Article  CAS  PubMed  Google Scholar 

  17. Zhao, F.Y., Hu, F., Han, M.M., Zhang, S.Y., and Liu, W., Superoxide radical and auxin are implicated in redistribution of root growth and the expression of auxin and cell-cycle genes in cadmium-stressed rice, Russ. J. Plant Physiol., 2011, vol. 58, pp. 864–870.

    Google Scholar 

  18. Hu, F., Xu, Z.J., Han, M.M., Wang, K., and Zhao, F.Y., Response of the ascorbate-glutathione cycle to combined cadmium and zinc in transgenic rice, Seed, 2010, vol. 29, pp. 6–10.

    CAS  Google Scholar 

  19. Chen, Y.C., Lin, H.H., and Jeng, S.T., Calcium influxes and mitogen-activated protein kinase kinase activation mediate ethylene inducing ipomoelin gene expression in sweet potato, Plant Cell Environ., 2008, vol. 31, pp. 62–72.

    Article  CAS  PubMed  Google Scholar 

  20. Zhao, F.Y., Han, M.M., Zhang, S.Y., Wang, K., Zhang, C.R., Liu, T., and Liu, W., Hydrogen peroxidemediated growth of the root system occurs via auxin signaling modification and variations in the expression of cell-cycle genes in rice seedlings exposed to cadmium stress, J. Integr. Plant Biol., 2012, vol. 54, pp. 991–1006.

    Article  CAS  PubMed  Google Scholar 

  21. Talarczyk, A., Krzymowska, M., Borucki, W., and Hennig, J., Effect of yeast CAT1 gene expression on response of tobacco plants to tobacco mosaic virus infection, Plant Physiol., 2002, vol. 129, pp. 1032–1044.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Loreto, F. and Velikova, V., Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes, Plant Physiol., 2001, vol. 127, pp. 1781–1787.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Petersson, S.V., Johansson, A.I., Kowalczyk, M., Makoveychuk, A., Wang, J.Y., Moritz, T., Grebe, M., Benfey, P.N., Sandberg, G., and Ljung, K., An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis, Plant Cell, 2009, vol. 21, pp. 1659–1668.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Wang, D., Pei, K., Fu, Y., Sun, Z., Li, S., Liu, H., Tang, K., Han, B., and Tao, Y., Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa L.), Gene, 2007, vol. 394, pp. 13–24.

    Article  CAS  PubMed  Google Scholar 

  25. Lee, S., Kim, Y.Y., Lee, Y., and An, G., Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein, Plant Physiol., 2007, vol. 145, pp. 831–842.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Pitzschke, A. and Hirt, H., Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling, Plant Physiol., 2009, vol. 149, pp. 606–615.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Yamamoto, Y., Kamiya, N., Morinaka, Y., Matsuoka, M., and Sazuka, T., Auxin biosynthesis by the YUCCA genes in rice, Plant Physiol., 2007, vol. 43, pp. 1362–1371.

    Article  Google Scholar 

  28. Wang, J.R., Hu, H., Wang, G.H., Li, J., Chen, J.Y., and Wu, P., Expression of PIN genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones, Mol. Plant, 2009, vol. 2, pp. 823–831.

    Article  CAS  PubMed  Google Scholar 

  29. Song, Y., Wang, L., and Xiong, L.Z., Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments, Planta, 2009, vol. 229, pp. 577–591.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to F. Y. Zhao.

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Zhao, F.Y., Han, M.M., Zhang, S.Y. et al. MAPKs as a cross point in H2O2 and auxin signaling under combined cadmium and zinc stress in rice roots. Russ J Plant Physiol 61, 608–618 (2014). https://doi.org/10.1134/S1021443714040232

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  • DOI: https://doi.org/10.1134/S1021443714040232

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