Biologia Plantarum 63: 183-192, 2019 | DOI: 10.32615/bp.2019.021

Overexpression of CBL interacting protein kinase 2 improves plant tolerance to salinity and mercury

W.H. Pan1, Z.Z. Zheng2, X. Yan2,3, J.Q. Shen2, J.X. Shou1, L.X. Jiang4, J.W. Pan3,*
1 College of Life Sciences, Shaoxing University, Shaoxing, Zhejiang 312000, P.R. China
2 College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, Zhejiang 321004, P.R. China
3 School of Life Sciences, Lanzhou University, Lanzhou 730000, P.R. China
4 College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, P.R. China

In plants, calcineurin B-like proteins (CBLs) and CBL-interacting protein kinases (CIPKs) regulate Ca2+ signalling and so responses to biotic and abiotic stresses. However, the details of specific CIPKs functions in various stress responses are poorly understood. Here, we report roles of dicot and monocot CIPK2 genes in response to salinity and heavy metals. Arabidopsis thaliana AtCIPK2 was found to be universally expressed in different tissues and organs and furthermore induced by salinity. Overexpression of AtCIPK2 or Tibetan Plateau wild barley (Hordeum spontaneum) HsCIPK2 in Arabidopsis alleviated toxic effects of NaCl and mercury on seed germination and root growth. Similarly, reduced toxic effects of copper and cadmium on seed germination, but not on root growth, were observed in these transgenic lines. Live-cell fluorescence imaging analysis revealed that HsCIPK2 was predominantly distributed in the cytoplasm and nucleus and weakly localized at the plasma membrane (PM), but its PM association was rapidly enhanced upon exposure to high salinity and mercury. These results suggest an involvement of CIPK2 in plant tolerance to salinity and mercury and provide a new insight into physiological functions of CIPKs in plant response to heavy metals.

Keywords: cadmium, copper, gene expression, NaCl, root growth, seed germination, subcellular localization

Accepted: November 15, 2018; Prepublished online: November 15, 2018; Published online: January 19, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Pan, W.H., Zheng, Z.Z., Yan, X., Shen, J.Q., Shou, J.X., Jiang, L.X., & Pan, J.W. (2019). Overexpression of CBL interacting protein kinase 2 improves plant tolerance to salinity and mercury. Biologia plantarum63, 183-192. doi: 10.32615/bp.2019.021.
Download citation

Supplementary files

Download filePAN5075Suppl.pdf

File size: 3.83 MB

References

  1. Batistič, O., Kudla, J.: Analysis of calcium signaling pathways in plants. -Biochim. biophys. Acta 1820: 1283-1293, 2012.
  2. Chen, L., Wang, Q.Q., Zhou, L., Ren, F., Li, D.D., Li, X.B.: Arabidopsis CBL-interacting protein kinase (CIPK6) is involved in plant response to salt/osmotic stress and ABA. - Mol. Biol. Rep. 40: 4759-4767, 2013. Go to original source...
  3. DalCorso, G., Manara, A., Furini, A.: An overview of heavy metal challenge in plants: from roots to shoots. - Metallomics 5: 1117-1132, 2013. Go to original source...
  4. De la Torre, F., Gutiérrez-Beltrán, E., Pareja-Jaime, Y., Chakravarthy, S., Martin, G.B., Del Pozo, O.: The tomato calcium sensor Cbl10 and its interacting protein kinase Cipk6 define a signaling pathway in plant immunity. - Plant Cell 25: 2748-2764, 2013. Go to original source...
  5. Dodd, A.N., Kudla, J., Sanders, D.: The language of calcium signaling. - Annu. Rev. Plant Biol. 61: 593-620, 2010. Go to original source...
  6. Guo, Y., Qiu, Q.S., Quintero, F.J., Pardo, J.M., Ohta, M., Zhang, C.Q., Schumaker, K.S., Zhu, J.K.: Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. - Plant Cell 16: 435-449, 2004. Go to original source...
  7. Hashimoto, K., Kudla, J.: Calcium decoding mechanisms in plants. - Biochimie 93: 2054-2059, 2011. Go to original source...
  8. Kolukisaoglu, U., Weinl, S., Blazevic, D., Batistic, O., Kudla, J.: Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. - Plant Physiol. 134: 43-58, 2004. Go to original source...
  9. Li, R., Zhang, J., Wu, G., Wang, H., Chen, Y., Wei, J.: HbCIPK2, a novel CBL-interacting protein kinase from halophyte Hordeum brevisubulatum, confers salt and osmotic stress tolerance. - Plant Cell Environ. 35: 1582-600, 2012. Go to original source...
  10. Luan, S.: The CBL-CIPK network in plant calcium signaling. - Trends Plant Sci. 14: 37-42, 2009. Go to original source...
  11. Pan, J.W., Zheng, K., Ye, D., Yi, H.L., Jiang, Z.M., Jing, C.T., Pan, W.H., Zhu, M.Y.: Ultraweak luminescence and sister-chromatid exchanges in root tip cells serve as sensitive indicators for Al toxicity and tolerance in barley. - Plant Sci. 167: 1391-1399, 2004. Go to original source...
  12. Piao, H.L., Xuan, Y.L., Park, S.H., Je, B.I., Park, S.J., Park, S.H., Kim, C.M., Huang, J., Wang, G.K., Kim, M.J.: OsCIPK31, a CBL-interacting protein kinase is involved in germination and seedling growth under abiotic stress conditions in rice plants. - Mol. Cell 30: 19-27, 2010. Go to original source...
  13. Sanders, D., Pelloux, J., Brownlee, C., Harper, J.F.: Calcium at the crossroads of signaling. - Plant Cell 14 (Suppl): S401-S417, 2002. Go to original source...
  14. Sharma, S.S., Dietz, K.J., Mimura, T.: Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. - Plant Cell Environ. 39: 1112-1126, 2016. Go to original source...
  15. Shen, J.Q., Zheng, Z.Z., Pan, W.H., Pan, J.W.: Functions and action mechanisms of CBL-CIPK signaling system in plants. - Plant Physiol. J. 50: 641-650, 2014. In Chin., ab: E
  16. Shen, Q., Jiang, M., Li, H., Che, L.L., Yang, Z.M.: Expression of a Brassica napus heme oxygenase confers plant tolerance to mercury toxicity. - Plant Cell Environ. 34: 752-763, 2011. Go to original source...
  17. Sun, Q., Gao, F., Zhao, L., Li, K., Zhang, J.: Identification of a new 130 bp cis-acting element in the TsVP1 promoter involved in the salt stress response from Thellungiella halophila. - BMC Plant Biol. 10: 90, 2010. Go to original source...
  18. Tripathi, V., Parasuraman, B., Laxmi, A., Chattopadhyay, D.: CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. - Plant J. 58: 778-790, 2009. Go to original source...
  19. Wang, C., Hu, T., Yan, X., Meng, T., Wang, Y., Wang, Q., Zhang, X., Gu, Y., Sánchez-Rodríguez, C., Gadeyne, A., Lin, J., Persson, S., Van Damme, D., Li, C., Bednarek, S.Y., Pan, J.: Differential regulation of clathrin and its adaptor proteins, AP-2 and the TPLATE complex, during their membrane recruitment in Arabidopsis. - Plant Physiol. 171: 215-229, 2016. Go to original source...
  20. Wang, C., Yan, X., Chen, Q., Jiang, N., Fu, W., Ma, B.J., Liu, J.Z,, Li, C.Y., Bednarek, S.Y., Pan, J.: Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and development in Arabidopsis. - Plant Cell 25: 499-516, 2013. Go to original source...
  21. Weinl, S., Kudla, J.: The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. - New Phytol. 184: 517-528, 2009. Go to original source...
  22. Xiang, Y., Huang, Y., Xiong, L.: Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. - Plant Physiol. 144: 1416-1428, 2007. Go to original source...
  23. Xu, J., Li, H.D., Chen, L.Q., Wang, Y., Liu, L.L., He, L., Wu, W.H.: A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. - Cell 125: 1347-1360, 2006. Go to original source...
  24. Yu, Q., Zhang, Y., Wang, J., Yan, X., Wang, C., Xu, J., Pan, J.: Clathrin-mediated auxin efflux and maxima regulates hypocotyl hook formation and light-stimulated hook opening in Arabidopsis. - Mol. Plant 9: 101-112, 2016. Go to original source...
  25. Zhao, J., Sun, Z., Zheng, J., Guo, X., Dong, Z., Huai, J., Gou, M., He, J., Jin, Y., Wang, J., Wang, G.: Cloning and characterization of a novel CBL-interacting protein kinase from maize. - Plant mol. Biol. 69: 661-674, 2009. Go to original source...
  26. Zheng, L.L., Gao, Z., Wang, J., Zhang, H.R., Wang, Y.C.: Molecular cloning and functional characterization of a novel CBL-interacting protein kinase NtCIPK2 in the halophyte Nitraria tangutorum. - Genet. mol. Res. 13: 4716-4728, 2014. Go to original source...
  27. Zhou, H.L., Cao, W.H., Cao, Y.R., Liu, J., Hao, Y.J., Zhang, J.S., Chen, S.Y.: Roles of ethylene receptor NTHK1 domains in plant growth, stress response and protein phosphorylation. -FEBS Lett. 580: 1239-1250, 2006. Go to original source...
  28. Zhu, S., Zhou, X., Wu, X., Jiang, Z.: Structure and function of the CBL-CIPK Ca2+-decoding system in plant calcium signaling. - Plant mol. Biol. Rep. 31: 1193-1202, 2013. Go to original source...