Skip to main content
SpringerLink
Log in

The calcium sensor PeCBL1, interacting with PeCIPK24/25 and PeCIPK26, regulates Na+/K+ homeostasis in Populus euphratica

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

This paper is the first to directly link two types of ion channel regulation pathway into an emerging and complex CBL–CIPK signal system in wooden plant.

Abstract

In Arabidopsis thaliana, the calcineurin b-like (CBL) 1 gene has been shown to be necessary in response to abiotic stresses. In this study, we identified CBL1 in the woody plant Populus euphratica, designated as PeCBL1. Heterologous expression of PeCBL1 could build the resistance of sensitive phenotypes to low K+ stress in the corresponding Arabidopsis cbl1/cbl9 mutant, and display a salt-sensitive phenotype compared with the mutant. Protein interaction analysis showed that PeCBL1 can interact with PeCIPK24, 25 and 26, and form different complexes of PeCBL–PeCIPK. To further investigate the mechanism of PeCBL1, we analyzed the fluxes of K+ and Na+ in roots of the wild-type Arabidopsis, cbl1/9 mutant, and PeCBL1 transgenic plants under low K+ stress and high Na+ stress. These analyses revealed that, compared to the cbl1/9 mutant, the PeCBL1 transgenic plant roots exhibited a higher capacity to absorb K+ after exposure to low K+ stress, and a lower capacity to discharge Na+ after exposure to salt stress. The results suggest that CBL1 interacts with CIPK24, CIPK25 and CIPK26 to regulate Na+/K+ homeostasis in Populus euphratica.

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

Abbreviations

ABA:

Abscisic acid

AD:

Activation domain

BD:

Binding domain

BiFC:

Bimolecular fluorescence complementation

CaM:

Calmodulin

CaMV:

Cauliflower mosaic virus

CBL:

Calcineurin B-like

CDPK:

Calcium-dependent protein kinase

CIPK:

CBL-interacting protein kinases

GFP:

Green fluorescent protein

SOS:

Salt overly sensitive

WT:

Wild type

YFP:

Yellow fluorescent protein

References

  • Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein–protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063

    Article  PubMed  CAS  Google Scholar 

  • Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu Ü, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant response to abiotic stresses. Plant J36:457–470

    Google Scholar 

  • Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK proteins kinase network. Planta 219:915–924

    Article  PubMed  CAS  Google Scholar 

  • Batistič O, Sorek N, Schültke S, Yalovsky S, Kudlaa J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20(5):1346–1362

    Article  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Google Scholar 

  • Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845

    Article  PubMed  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 Jl 52:223–239

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740

    Article  PubMed  CAS  Google Scholar 

  • Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signaling connection. Nat Rev Mol Cell Bio 6:555–566

    Article  CAS  Google Scholar 

  • Hedrich R, Kudla J (2006) Calcium signaling network channel plant K+ uptake. Cell 125:1221–1223

    Article  PubMed  CAS  Google Scholar 

  • Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138(6):1184–1194

    Article  PubMed  CAS  Google Scholar 

  • Huang C, Ding S, Zhang H, Du H, An L (2011) CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci 181(1):57–64

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kim MC, Chung WS, Yun D, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21

    Article  PubMed  CAS  Google Scholar 

  • Kolukisaoglu Ü, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL–CIPK signaling networks. Plant Physiol 134:43–58

    Article  PubMed  CAS  Google Scholar 

  • Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulated a K+ channel for low-K+ response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14:389–400

    Google Scholar 

  • Pandey GK, Cheong YH, Kim KN, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924

    Article  PubMed  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 19:1415–1431

    Article  PubMed  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:401–417

    Google Scholar 

  • Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405

    PubMed  CAS  Google Scholar 

  • Waadt R, Kudla J (2008) In planta visualization of protein interactions using bimolecular fluorescence complementation (BiFC). CSH Protoc. doi:10.1101/pdb.prot4995

    PubMed  Google Scholar 

  • Weinl S, Kudla J (2009) The CBL–CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528

    Article  PubMed  CAS  Google Scholar 

  • White PJ, Broadley PJ (2003) Calcium in plant. Ann Bot 92:487–511

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    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  PubMed  CAS  Google Scholar 

  • Yu Y, Yin W, Xia X, Zhang H (2007) Comparative genomic analysis of CIPK gene family in Arabidopsis and Populus. Plant Growth Regul 52:101–110

    Article  CAS  Google Scholar 

  • Zhang H, Yin W, Xia X (2008) Calcineurin B-Like family in Populus: comparative genome analysis and expression pattern under cold, drought and salt stress treatment. Plant Growth Regul 56:129–140

    Article  CAS  Google Scholar 

  • Zhang H, Yin W, Xia X (2010) Shaker-like potassium channels in Populus, regulated by the CBL–CIPK signal transduction pathway, increase tolerance to low-K+ stress. Plant Cell Rep 29:1007–1012

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Key Technologies R&D Program of China (2011BAD38B01, 2009CB119101), National Natural Science Foundation of China (30972339, and 31070597), the Ministry of Science and Technology of China (2009CB119101), and the Scientific Research and Graduate Training Joint Programs from BMEC (Regulation of Tree WUE).

Author information

Authors and Affiliations

  1. National Engineering Laboratory of Forest Genetics and Tree Breeding, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Hechen Zhang, Fuling Lv, Xiao Han, Xinli Xia & Weilun Yin

  2. Horticulture Research Institute, Henan Academy of Agricultural Sciences, No. 116, Huayuan Road, Jinshui District, Zhengzhou, 450002, Henan Province, People’s Republic of China

    Hechen Zhang

Authors
  1. Hechen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fuling Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiao Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinli Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weilun Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xinli Xia or Weilun Yin.

Additional information

Communicated by L. Jouanin.

H. Zhang and F. Lv contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 76 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, H., Lv, F., Han, X. et al. The calcium sensor PeCBL1, interacting with PeCIPK24/25 and PeCIPK26, regulates Na+/K+ homeostasis in Populus euphratica . Plant Cell Rep 32, 611–621 (2013). https://doi.org/10.1007/s00299-013-1394-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1394-5

Keywords

Search

Navigation