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Evolutionary analysis of CBL-interacting protein kinase gene family in plants

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Abstract

Calcineurin B-like proteins (CBLs) and CBL-interacting protein kinases (CIPKs) form the CBL-CIPK complexes, perceiving calcium signals and relaying the signals to downstream responses in plants. To further understand the CBL-CIPK signaling system, here we focused on the evolutionary analysis of CIPKs. We re-evaluated eight plant genomes and identified 146 CIPKs, providing several new CIPKs in rice and poplar. A phylogenetic tree was constructed, showing that these 146 CIPKs are grouped into intron-rich and intron-less clades. Furthermore, all the CIPKs from the non-angiosperm species were found in intron-rich clade. We identified 30 conserved protein motifs among these 146 CIPKs. Analysis of gene duplication showed that the expansion of CIPKs in both clades is partly contributed by segmental duplications, however, tandem duplicates were found only in intron-less clade. Ka/Ks ratios showed that CIPK genes have experienced purifying selective pressure. Additionally, clustering of gene expression revealed that some CIPK genes in two clades share similar expression patterns under abiotic stresses and four CIPKs in intron-less clade form a distinct cluster (i.e., different expression patterns), suggesting the complexity of CIPK gene expression under abiotic stresses. Taken together, our results provided some new insights into the evolution of CIPKs and the hint that the expansion of CIPKs in intron-less clade is adaptive to environmental stresses.

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Abbreviations

CBLs:

Calcineurin B-like proteins

CIPKs:

CBL-interacting protein kinases

HMM:

Hidden Markov model

CAMs:

Calmodulins

CDPKs:

Calcium-dependent protein kinases

SOS:

Salt overly sensitive

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 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intel Syst Mol Biol 2:28–36

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Gu Z, Xin D, Hao L, Liu C, Huang J, Ma B, Zhang H (2011) Identification and characterization of putative CIPK genes in maize. J Genet Genomics 38:77–87

    Article  PubMed  CAS  Google Scholar 

  • Demuth JP, Hahn MW (2009) The life and death of gene families. BioEssays 31:29–39

    Article  PubMed  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    Article  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    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 

  • Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148:993–1003

    Article  PubMed  CAS  Google Scholar 

  • Harmon AC, Gribskov M, Harper JF (2000) CDPKs—a kinase for every Ca2+ signal? Trends Plant Sci 5:154–159

    Article  PubMed  CAS  Google Scholar 

  • Herrero J, Valencia A, Dopazo J (2001) A hierarchical unsupervised growing neural network for clustering gene expression patterns. Bioinformatics 17:126–136

    Article  PubMed  CAS  Google Scholar 

  • Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680

    Article  PubMed  CAS  Google Scholar 

  • Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, Finn RD, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Laugraud A, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, Mistry J, Mitchell A, Mulder N, Natale D, Orengo C, Quinn AF, Selengut JD, Sigrist CJ, Thimma M, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211–D215

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    Article  PubMed  CAS  Google Scholar 

  • Kolukisaoglu U, 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 

  • Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723

    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(Suppl):S389–S400

    PubMed  CAS  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 100:11771–11776

    Article  PubMed  CAS  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301

    Article  PubMed  CAS  Google Scholar 

  • Roy SW, Penny D (2007) Patterns of intron loss and gain in plants: intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 24:171–181

    Article  PubMed  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–S417

    PubMed  CAS  Google Scholar 

  • Schumann N, Navarro-Quezada A, Ullrich K, Kuhl C, Quint M (2011) Molecular evolution and selection patterns of plant F-box proteins with C-terminal kelch repeats. Plant Physiol 155:835–850

    Article  PubMed  CAS  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 

  • Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66

    Article  CAS  Google Scholar 

  • Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinform 8:77–80

    Article  CAS  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 

  • Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428

    Article  PubMed  CAS  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 125:1347–1360

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:1189–1200

    Article  PubMed  CAS  Google Scholar 

  • Ye CY, Li T, Tuskan GA, Tschaplinski TJ, Yang X (2011) Comparative analysis of GT14/GT14-like gene family in Arabidopsis, Oryza, Populus, Sorghum and Vitis. Plant Sci 181:688–695

    Article  PubMed  CAS  Google Scholar 

  • Ye CY, Li T, Yin H, Weston DJ, Tuskan GA, Tschaplinski TJ, Yang X (2012) Evolutionary analyses of non-family genes in plants. Plant J. doi:10.1111/tpj.12073

    PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from the Ministry of Science and Technology of China (2011BAD38B01, 2009CB119101), the National Natural Science Foundation of China (31070597, 31270656, and 31100492), Joint Programs of the Scientific Research and Graduate Training from BMEC (Stress Resistance Mechanism of Poplar), and Beijing Forestry University Technology Innovation Program (BLYJ200904).

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Correspondence to Xinli Xia or Weilun Yin.

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Ye, CY., Xia, X. & Yin, W. Evolutionary analysis of CBL-interacting protein kinase gene family in plants. Plant Growth Regul 71, 49–56 (2013). https://doi.org/10.1007/s10725-013-9808-5

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