Skip to main content
SpringerLink
Log in

Genome-wide analysis of CBL and CIPK family genes in cotton: conserved structures with divergent interactions and expression

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Calcineurin B-like proteins (CBLs) interact with CBL-interacting protein kinases (CIPKs) to form complex molecular modules in response to diverse abiotic stresses. Although previous studies demonstrated that the CBL-CIPK networks play a crucial role in plants response to abiotic stresses, however, little is known about their functions in cotton. In the present study, a total of 22 GhCBL and 79 GhCIPK gene family members were identified in upland cotton (Gossypium hirsutum Linn). Synteny analysis revealed that most genes of GhCBL and GhCIPK exist in pairs between At sub-genome and Dt sub-genome. Interaction analysis between GhCBL and GhCIPK proteins by yeast two-hybrid (Y2H) suggested that the GhCBL-GhCIPK networks were complex, and exhibited functional redundancy in cotton. Quantitative expression analysis by public transcriptome datasets revealed that some GhCBL and GhCIPK genes are differentially expressed under abiotic stress treatments, and especially under drought stress. Our results not only contribute to understanding the structural features of GhCBL and GhCIPK genes but also provide the basis for in-depth functional studies of GhCBL-GhCIPK networks in stress response for plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Batistic O, Waadt R, Steinhorst L, Held K, Kudla J (2010) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J 61(2):211–222

    Article  CAS  Google Scholar 

  • Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52(2):223–239

    Article  CAS  Google Scholar 

  • Cui Y, Su Y, Wang J, Jia B, Wu M, Pei W, Zhang J, Yu J (2020) Genome-wide characterization and analysis of CIPK gene family in two cultivated allopolyploid cotton species: sequence variation, association with seed oil content, and the role of GhCIPK6. Int J Mol Sci 21(3):863

    Article  CAS  Google Scholar 

  • Deng J, Yang X, Sun W, Miao Y, He L, Zhang X (2020) The calcium sensor CBL2 and its interacting kinase CIPK6 are involved in plant sugar homeostasis via interacting with tonoplast sugar transporter TST2. Plant Physiol 183(1):236–249

    Article  Google Scholar 

  • Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS ONE 9(11):e111988

    Article  Google Scholar 

  • Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6(2):559–569

    Article  CAS  Google Scholar 

  • Du W, Lin H, Chen S, Wu Y, Zhang J, Fuglsang AT, Palmgren MG, Wu W, Guo Y (2011) Phosphorylation of SOS3-like calcium-binding proteins by their interacting SOS2-like protein kinases is a common regulatory mechanism in Arabidopsis. Plant Physiol 156(4):2235–2243

    Article  CAS  Google Scholar 

  • Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na(+)/H(+) antiporter from rice. Plant Cell Physio 45(2):146–159

    Article  CAS  Google Scholar 

  • Gu Z, Gu L, Eils R, Schlesner M, Brors B (2014) Circlize implements and enhances circular visualization in R. Bioinformatics 30(19):2811–2812

    Article  CAS  Google Scholar 

  • Guo Y, Halfter U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant cell 13(6):1383–1400

    Article  CAS  Google Scholar 

  • Hashimoto K, Eckert C, Anschutz U, Scholz M, Held K, Waadt R, Reyer A, Hippler M, Becker D, Kudla J (2012) 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(11):7956–7968

    Article  CAS  Google Scholar 

  • He L, Yang X, Wang L, Zhu L, Zhou T, Deng J, Zhang X (2013) Molecular cloning and functional characterization of a novel cotton CBL-interacting protein kinase gene (GhCIPK6) reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Biochem Biophys Res Commun 435(2):209–215

    Article  CAS  Google Scholar 

  • Huertas R, Olías R, Eljakaoui Z, Gálvez FJ, Li J, De Morales PA, Belver A, Rodríguez-Rosales MP (2012) Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ 35(8):1467–1482

    Article  CAS  Google Scholar 

  • Ilyas M, Nisar M, Khan N, Hazrat A, Khan AH, Hayat K, Fahad S, Khan A, Ullah A (2020) Drought tolerance strategies in plants: a mechanistic approach. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10174-5

    Article  Google Scholar 

  • Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schültke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52(3):473–484

    Article  CAS  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant cell 22(3):541–563

    Article  CAS  Google Scholar 

  • Li J, Long Y, Qi GN, Li J, Xu ZJ, Wu WH, Wang Y (2014) The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex. Plant cell 26(8):3387–3402

    Article  CAS  Google Scholar 

  • Li R, Zhang J, Wei J, Wang H, Wang Y, Ma R (2009) Functions and mechanisms of the CBL–CIPK signaling system in plant response to abiotic stress. Prog Nat Sci 19(6):667–676

    Article  Google Scholar 

  • Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14(1):37–42

    Article  CAS  Google Scholar 

  • Manik SM, Shi S, Mao J, Dong L, Su Y, Wang Q, Liu H (2015) The Calcium Sensor CBL-CIPK Is Involved in Plant's Response to Abiotic Stresses. Int J Genomics 2015:493191

    Article  Google Scholar 

  • Mohanta TK, Mohanta N, Mohanta YK, Parida P, Bae H (2015) Genome-wide identification of Calcineurin B-Like (CBL) gene family of plants reveals novel conserved motifs and evolutionary aspects in calcium signaling events. BMC Plant Biol 15:189

    Article  Google Scholar 

  • Ohta M, Guo Y, Halfter U, Zhu JK (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100(20):11771–11776

    Article  CAS  Google Scholar 

  • Pandey GK, Grant JJ, Cheong YH, Kim BG, le Li G, Luan S (2008) Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol Plant 1(2):238–248

    Article  CAS  Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99(12):8436–8441

    Article  CAS  Google Scholar 

  • Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant cell 19(4):1415–1431

    Article  CAS  Google Scholar 

  • Sánchez-Barrena MJ, Martínez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345(5):1253

    Article  Google Scholar 

  • Sun T, Wang Y, Wang M, Li T, Zhou Y, Wang X, Wei S, He G, Yang G (2015) Identification and comprehensive analyses of the CBL and CIPK gene families in wheat (Triticum aestivum L.). BMC Plant Biol 15:269

    Article  Google Scholar 

  • Tang R-J, Liu H, Bao Y, Lv Q-D, Yang L, Zhang H-X (2010) The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol Biol 74(4):367–380

    Article  CAS  Google Scholar 

  • Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX, Luan S (2015) Tonoplast CBL-CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad Sci USA 112(10):3134–3139

    Article  CAS  Google Scholar 

  • Tu LL, Zhang XL, Liang SG, Liu DQ, Zhu LF, Zeng FC, Nie YC, Guo XP, Deng FL, Tan JF (2007) Genes expression analyses of sea-island cotton (Gossypium barbadense L.) during fiber development. Plant Cell Rep 26(8):1309–1320

    Article  CAS  Google Scholar 

  • Ullah A, Sun H, Yang X, Zhang X (2017) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnol J 15(3):271–284

    Article  CAS  Google Scholar 

  • Ullah A, Ul Qamar MT, Nisar M, Hazrat A, Rahim G, Khan AH, Hayat K, Ahmed S, Ali W, Khan A, Yang X (2020) Characterization of a novel cotton MYB gene, GhMYB108-like responsive to abiotic stresses. Mol Biol Rep 47:1573–1581

    Article  CAS  Google Scholar 

  • Xi Y, Liu J, Dong C, Cheng ZM (2017) 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

    Article  Google Scholar 

  • Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125(7):1347–1360

    Article  CAS  Google Scholar 

  • Yang W, Kong Z, Omo-Ikerodah E, Xu W, Li Q, Xue Y (2008) Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). J Genet Genomics 35(9):531–543

    Article  CAS  Google Scholar 

  • Yasuda S, Aoyama S, Hasegawa Y, Sato T, Yamaguchi J (2017) Arabidopsis CBL-interacting protein kinases regulate carbon/nitrogen-nutrient response by phosphorylating ubiquitin ligase ATL31. Mol Plant 10(4):605–618

    Article  CAS  Google Scholar 

  • Yu Q, An L, Li W (2014) The CBL-CIPK network mediates different signaling pathways in plants. Plant Cell Rep 33(2):203–214

    Article  CAS  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J (2015) Sequencing of allotetraploid cotton (Gossypiumhirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33(5):531–537

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by funding from the National Key Project of Research and the Development Plan (2016YFD0101006) and National Natural Science Foundation of China (31371675).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Weinan Sun, Bing Zhang, Jinwu Deng, Lin Chen & Xiyan Yang

  2. Department of Botany, University of Malakand, Chakdara Dir Lower, 18800, Khyber Pakhtunkhwa, Pakistan

    Abid Ullah

Authors
  1. Weinan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinwu Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abid Ullah
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiyan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Abid Ullah or Xiyan Yang.

Ethics declarations

Conflict of interest

The authors declare that there is no conflicts of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, W., Zhang, B., Deng, J. et al. Genome-wide analysis of CBL and CIPK family genes in cotton: conserved structures with divergent interactions and expression. Physiol Mol Biol Plants 27, 359–368 (2021). https://doi.org/10.1007/s12298-021-00943-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-00943-1

Keywords

Search

Navigation