biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 64:773-783, 2020 | DOI: 10.32615/bp.2020.123

Identifying citrus CBL and CIPK gene families and their expressions in response to drought and arbuscular mycorrhizal fungi colonization

B. SHU1, D. CAI2, F. ZHANG1, D.J. ZHANG1, C.Y. LIU1, Q.S. WU1, C. LUO1,*
1 College of Horticulture and Gardening, Yangtze University, Jingzhou 434025, P.R. China
2 Yunnan Vocational and Technical College of Agriculture, Kunming 650031, P.R. China

The calcineurin B-like protein (CBL)-interacting protein kinase (CIPK) complex is an essential calcium sensor and contributes to biotic and abiotic stress responses. However, citrus CBL and CIPK gene family members and their underlying roles during drought and arbuscular mycorrhizal fungi (AMF) colonization remain relatively unknown. In the present study, CBLs and CIPKs were characterized in Citrus sinensis by analyzing the presence of specific domains such as the elongation factor (EF)-hand motif in CBLs, and a protein kinase and an Asn-Ala-Phe domain in CIPKs. After mining the C. sinensis genome, we identified 8 CsCBLs and 17 CsCIPKs. Among these genes, three CsCBLs and nine CsCIPKs showed syntenic relationships with the Arabidopsis thaliana homologs AtCBLs and AtCIPKs, respectively. According to gene expression and cis-acting element analysis, all 8 CsCBLs and 16 CsCIPKs were expressed in the roots, where the regulation of expression was not consistent with their promoter cis-elements. Drought treatment remarkably downregulated the expression of CsCBL8 and upregulated CsCBL7, CsCIPK4, and CsCIPK7 expressions. The AMF colonization induced CsCBL4, 5, 6, and 7 as well as CsCIPK2, 4, 10, 11, 13, 14, and 16 expressions and repressed CsCBL1, 2, 3, and 8 and CsCIPK1, 3, 6, 8, 9, and 12 expressions. Based on the expression data and co-expression analysis, CsCBL1-CsCIPK1, CsCBL1-CsCIPK3, CsCBL1-CsCIPK6, and CsCBL1-CsCIPK9 showed the significant positive correlations to drought and AMF responses.

Keywords: calcineurin B-like protein, CBL-interacting protein kinase, gene structure, phylogenetic analysis, transcriptional regulation.

Received: June 23, 2020; Revised: August 15, 2020; Accepted: August 24, 2020; Published online: November 4, 2020  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SHU, B., CAI, D., ZHANG, F., ZHANG, D.J., LIU, C.Y., WU, Q.S., & LUO, C. (2020). Identifying citrus CBL and CIPK gene families and their expressions in response to drought and arbuscular mycorrhizal fungi colonization. Biologia plantarum, 64, Article 773-783. https://doi.org/10.32615/bp.2020.123
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileShu6522_Suppl.pdf

    File size: 817.46 kB

    References

    1. Akaboshi, M., Hashimoto, H., Ishida, H., Saijo, S., Koizumi, N., Sato, M., Shimizu, T.: The crystal structure of plant-specific calcium-binding protein AtCBL2 in complex with the regulatory domain of AtCIPK14. - J. mol. Biol. 377: 246-257, 2008. Go to original source...
    2. Aslam, M., Fakher, B., Jakada, B.H., Zhao, L., Cao, S., Cheng, Y., Qin, Y.: Genome-wide identification and expression profiling of CBL-CIPK gene family in pineapple (Ananas comosus) and the role of AcCBL1 in abiotic and biotic stress response. - Biomolecules 9: 293, 2019. Go to original source...
    3. Chen, C., Xia, R., Chen, H., He, Y.T.: A toolkit for biologists integrating various HTS-data handling tools with a user-friendly interface. - bioRxiv, https://doi.org/10.1101/289660, 2018. Go to original source...
    4. Cheong, Y.H., Sung, S.J., Kim, B.G., Pandey, G.K., Cho, J.S., Kim, K.N., Luan, S.: Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. - Mol. Cells 29: 159-165, 2010. Go to original source...
    5. Chow, C.N., Chiang-Hsieh, Y.F., Chien, C.H., Zheng, H.Q., Lee, T.Y., Wu, N.Y., Tseng, K.C., Hou, P.F., Chang, W.C.: Delineation of condition specific cis- and trans-acting elements in plant promoters under various endo-and exogenous stimuli. - BMC Genomics 19: 85, 2018. Go to original source...
    6. Cui, X.Y., Du, Y.T., Fu, J.D., Yu, T.F., Wang, C.T., Chen, M., Chen, J., Ma, Y.Z., Xu, Z.S.: Wheat CBL-interacting protein kinase 23 positively regulates drought stress and ABA responses. - BMC Plant Biol. 18: 93, 2018. Go to original source...
    7. 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...
    8. Edgar, R.C.: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797, 2004. Go to original source...
    9. Fuju, T., Zhiheng, Y., Shipeng, L.: ZmCIPK8, a CBL-interacting protein kinase, regulates maize response to drought stress. - Plant Cell Tissue Organ Cult. 124: 459-469, 2016. Go to original source...
    10. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D., Bairoch, A.: Expasy: the proteomics server for in-depth protein knowledge and analysis. - Nucleic Acids Res. 31: 3784-3788, 2003. Go to original source...
    11. Guo, Y., Halfter, U., Ishitani, M., Zhu, J.K.: Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. - Plant Cell 13: 1383-1400, 2001. Go to original source...
    12. Hashimoto, K., Eckert, C., Anschütz, U., Scholz, M., Held, K., Waadt, R., Reyer, A., Hippler, M., Becker, D., Kudla, J.: Phosphorylation of calcineurin b-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins. - J. biol. Chem. 287: 7956-7968, 2012. Go to original source...
    13. Hématy, K., Höfte, H.: Novel receptor kinases involved in growth regulation. - Curr. Opin. Plant Biol. 11: 321-328, 2008. Go to original source...
    14. Kang, H.K., Nam, K.H.: Reverse function of ROS-induced CBL10 during salt and drought stress responses. - Plant Sci. 243: 49-55, 2016. Go to original source...
    15. Kolukisaoglu, Ü., 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...
    16. Kumar, S., Stecher, G., Tamura K.: MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. - Mol. Biol. Evol. 33: 1870-1874, 2016. Go to original source...
    17. Kurusu, T., Hamada, J., Nokajima, H., Kitagawa, Y., Kiyoduka, M., Takahashi, A., Hanamata, S., Ohno, R., Hayashi, T., Okada, K., Koga, J., Hirochika, H., Yamane, H., Kuchitsu, K.: Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. - Plant Physiol. 153: 678-692, 2010. Go to original source...
    18. Liu, L.L., Ren, H.M., Chen, L.Q., Wang, Y., Wu, W.H.: A protein kinase, calcineurin b-like protein-interacting protein kinase9, interacts with calcium sensor calcineurin b-like protein3 and regulates potassium homeostasis under low-potassium stress in Arabidopsis. - Plant Physiol. 161: 266-277, 2013. Go to original source...
    19. Liu, P., Duan, Y., Liu, C., Xue, Q., Guo, J., Qi, T., Kang, Z., Guo, J.: The calcium sensor TaCBL4 and its interacting protein TaCIPK5 are required for wheat resistance to stripe rust fungus. - J. exp. Bot. 69: 4443-4457, 2018. Go to original source...
    20. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
    21. Luan, S.: The CBL-CIPK network in plant calcium signaling. - Trends Plant Sci. 14: 37-42, 2009. Go to original source...
    22. Luo, Q., Wei, Q., Wang, R., Zhang, Y., Zhang, F., He, Y., Zhou, S., Feng, J., Yang, G., He, G.: BdCIPK31, a calcineurin B-like protein-interacting protein kinase, regulates plant response to drought and salt stress. - Front. Plant Sci. 8: 1184, 2017. Go to original source...
    23. Ma, Q.J., Sun, M.H., Lu, J., Liu, Y.J., You, C.X., Hao, Y.J.: An apple CIPK protein kinase targets a novel residue of AREB transcription factor for ABA-dependent phosphorylation. - Plant Cell Environ. 40: 2207-2219, 2017. Go to original source...
    24. Ma, Y., Cao, J., Chen, Q., He, J., Liu, Z., Wang, J., Li, X., Yang, Y.: The kinase CIPK11 functions as a negative regulator in drought stress response in Arabidopsis. - Int. J. mol. Sci. 20: 2422, 2019. Go to original source...
    25. Quan, R., Lin, H., Mendoza, I., Zhang, Y., Cao, W., Yang, Y., Shang, M., Chen, S., Pardo, J.M., Guo, Y.: SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. - Plant Cell 19: 1415-1431, 2007. Go to original source...
    26. Ren, X.L., Qi, G.N., Feng, H.Q., Zhao, S., Zhao, S.S., Wang, Y., Wu, W.H.: Calcineurin B-like protein CBL 10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. - Plant J. 74: 258-266, 2013. Go to original source...
    27. Rodríguez-Gamir, J., Primo-Millo, E., Forner, J.B., Forner-Giner, M.A.: Citrus rootstock responses to water stress. - Sci. Hort. (Amsterdam) 126: 95-102, 2010. Go to original source...
    28. Rombauts, S., Déhais, P., Montagu, M.V., Rouzé, P.: PlantCARE, a plant cis-acting regulatory element database. - Nucl. Acids Res. 27: 295-296, 1999. Go to original source...
    29. Sanchez-Barrena, M.J., Martinez-Ripoll, M., Zhu, J.K., Albert, A.: The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. - J. mol. Biol. 345: 1253-1264, 2005. Go to original source...
    30. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., Ideker, T.: Cytoscape: a software environment for integrated models of biomolecular interaction networks. - Genome Res. 13: 2498-2504, 2003. Go to original source...
    31. Shu, B., Li, W.C., Liu, L.Q., Wei, Y.Z., Shi, S.Y.: Transcriptomes of arbuscular mycorrhizal fungi and litchi host interaction after tree girdling. - Front. Microbiol. 7: 408, 2016. Go to original source...
    32. Shu, B., Xia, R.X., Wang, P.: Differential regulation of Pht1 phosphate transporters from trifoliate orange (Poncirus trifoliata L. Raf) seedlings. - Sci. Hort. (Amsterdam) 146: 115-123, 2012. Go to original source...
    33. Su, W., Huang, L., Ling, H., Mao, H., Huang, N., Su, Y., Ren, Y., Wang, D., Xu, L., Muhammad, K., Que, Y.: Sugarcane calcineurin B-like (CBL) genes play important but versatile roles in regulation of responses to biotic and abiotic stresses. - Sci. Rep. 10: 1-13, 2020. Go to original source...
    34. Tang, J., Lin, J., Li, H., Li, X., Yang, Q., Cheng, Z.M., Chang, Y.: Characterization of CIPK family in Asian pear (Pyrus bretschneideri Rehd) and co-expression analysis related to salt and osmotic stress responses. - Front. Plant Sci. 7: 1361, 2016. Go to original source...
    35. Wang, Y., Tang, H., DeBarry, J.D., Tan, X., Li, J., Wang, X., Lee, T., Jin, H., Marler, B., Guo, H., Kissinger, J.C., Paterson, A.H.: MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. - Nucleic Acids Res. 40: e49, 2012. Go to original source...
    36. Wu, Q.S., Srivastava, A.K., Zou, Y.N.: AMF-induced tolerance to drought stress in citrus: a review. - Sci. Hort. (Amsterdam) 164: 77-87, 2013. Go to original source...
    37. Xi, Y., Liu, J., Dong, C., Cheng, Z.M.M.: The CBL and CIPK gene family in grapevine (Vitis vinifera): Genome-wide analysis and expression profiles in response to various abiotic stresses. - Front. Plant Sci. 8: 978, 2017. Go to original source...
    38. Xiang, Y., Huang, Y., Xiong, L.: Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. - Plant Physiol. 3: 1416-1428, 2007. Go to original source...
    39. Xie, Y., Zhang, Y., Han, J., Luo, J., Li, G., Huang, J., Wu, H., Tian, Q., Zhu, Q., Chen, Y., Kawano, Y., Liu, Y.G., Chen, L.: The intronic cis element SE1 recruits trans-acting repressor complexes to repress the expression of ELONGATED UPPERMOST INTERNODE1 in rice. - Mol. Plants 11: 720-735, 2018. Go to original source...
    40. Xu, W., Shen, W., Ma, J., Ya, R., Zheng, Q., Wu, N., Yu, Q., Yao, W., Zhang, N., Zhang, J.: Role of an Amur grape CBL-interacting protein kinase VaCIPK02 in drought tolerance by modulating ABA signaling and ROS production. - Environ. exp. Bot. 172: 103999, 2020. Go to original source...
    41. Yan, Y., He, X., Hu, W., Liu, G., Wang, P., He, C., Shi, H.: Functional analysis of MeCIPK23 and MeCBL1/9 in cassava defense response against Xanthomonas axonopodis pv. manihotis. - Plant Cell Rep. 37: 887-900, 2018. Go to original source...
    42. Yang, W., Kong, Z., Omo-Ikerodah, E., Xu, W., Li, Q., Xue, Y.: Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). - J. Genet. Genome 9: 531-543, 2008. Go to original source...
    43. Yin, X., Wang, Q., Chen, Q., Xiang, N., Yang, Y., Yang, Y.: Genome-wide identification and functional analysis of the calcineurin B-like protein and calcineurin B-like protein-interacting protein kinase gene families in turnip (Brassica rapa var. rapa). - Front. Plant Sci. 8: 1191, 2017. Go to original source...
    44. Zhang, F., Zou, Y.N., Wu, Q.S., Kuča, K.: Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. - Environ. exp. Bot. 171: 103926, 2020a. Go to original source...
    45. Zhang, X., Li, X., Zhao, R., Zhou, Y., Jiao, Y.: Evolutionary strategies drive a balance of the interacting gene products for the CBL and CIPK gene families. - New Phytol. 226: 1506-1516, 2020b. Go to original source...

    Return to the content