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Journal of Integrative Agriculture  2015, Vol. 14 Issue (1): 29-41    DOI: 10.1016/S2095-3119(14)60780-2
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide analysis of the calcium-dependent protein kinase gene family in Gossypium raimondii
 LI Li-bei, YU Ding-wei, ZHAO Feng-li, PANG Chao-you, SONG Mei-zhen, WEI Heng-ling, FAN Shu-li, YU Shu-xun
State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, P.R.China
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摘要  Plant calcium-dependent protein kinases (CDPKs) play important roles in diverse physiological processes by regulating the downstream components of calcium signaling. To date, only a few species of the plant CDPK gene family have been functionally identified. In addition, there has been no systematic analysis of the CDPK family in cotton. Here, 41 putative cotton CDPK (GrCDPK) genes were identified via bioinformatics analysis of the entire genome of Gossypium raimondii and were classified into four groups based on evolutionary relatedness. Gene structure analysis indicated that most of these GrCDPK genes share a similar intron-exon structure (7 or 8 exons), strongly supporting their close evolutionary relationships. Chromosomal distributions and phylogenetics analysis showed that 13 pairs of GrCDPK genes arose via segmental duplication events. Furthermore, using microarray data of upland cotton (G. hirsutum L.), comparative profiles analysis of these GhCDPKs indicated that some of the encoding genes might be involved in the responses to multiple abiotic stresses and play important regulatory roles during cotton fiber development. This study is the first genome-wide analysis of the CDPK family in cotton, and it will provide valuable information for the further functional characterization of cotton CDPK genes.

Abstract  Plant calcium-dependent protein kinases (CDPKs) play important roles in diverse physiological processes by regulating the downstream components of calcium signaling. To date, only a few species of the plant CDPK gene family have been functionally identified. In addition, there has been no systematic analysis of the CDPK family in cotton. Here, 41 putative cotton CDPK (GrCDPK) genes were identified via bioinformatics analysis of the entire genome of Gossypium raimondii and were classified into four groups based on evolutionary relatedness. Gene structure analysis indicated that most of these GrCDPK genes share a similar intron-exon structure (7 or 8 exons), strongly supporting their close evolutionary relationships. Chromosomal distributions and phylogenetics analysis showed that 13 pairs of GrCDPK genes arose via segmental duplication events. Furthermore, using microarray data of upland cotton (G. hirsutum L.), comparative profiles analysis of these GhCDPKs indicated that some of the encoding genes might be involved in the responses to multiple abiotic stresses and play important regulatory roles during cotton fiber development. This study is the first genome-wide analysis of the CDPK family in cotton, and it will provide valuable information for the further functional characterization of cotton CDPK genes.
Keywords:  GrCDPK       cotton       stress       gene family       expression  
Received: 10 February 2014   Accepted: 08 January 2015
Fund: 

This work was supported by the National High-Tech R&D Program of China (2013AA102601).

Corresponding Authors:  FAN Shu-li, Tel: +86-372-2562249, E-mail: fansl@cricaas.com.cn;YU Shu-xun, Tel: +86-372-2562201, Fax: +86-372-2562256,E-mail: yu@cricaas.com.cn     E-mail:  fansl@cricaas.com.cn;yu@cricaas.com.cn
About author:  * These authors contributed equally to this study.

Cite this article: 

LI Li-bei, YU Ding-wei, ZHAO Feng-li, PANG Chao-you, SONG Mei-zhen, WEI Heng-ling, FAN Shu-li, YU Shu-xun. 2015. Genome-wide analysis of the calcium-dependent protein kinase gene family in Gossypium raimondii. Journal of Integrative Agriculture, 14(1): 29-41.

Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S. 2004.OsCDPK13, a calcium-dependent protein kinase gene fromrice, is induced by cold and gibberellin in rice leaf sheath.Plant Molecular Biology, 55, 541-552

Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, Takano M,Sato M, Furuhashi H, Mujin T, Takaiwa F, Wu C, Tada Y,Satozawa T, Sakamoto M, Shimada H. 2002. Rice SPK,a calmodulin-like domain protein kinase, is required forstorage product accumulation during seed development:Phosphorylation of sucrose synthase is a possible factor.The Plant Cell, 14, 619-628

Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S. 2005.Genome-wide identification of the rice calcium-dependentprotein kinase and its closely related kinase gene families:Comprehensive analysis of the CDPKs gene family in rice.Plant Cell Physiology, 46, 356-366

de Castro E, Sigrist C J, Gattiker A, Bulliard V, Langendijk-Genevaux P S, Gasteiger E, Bairoch A, Hulo N. 2006. ScanProsite: Detection of PROSITE signature matchesand ProRule-associated functional and structural residuesin proteins. Nucleic Acids Research, 34, W362-W365.

Cheng S H, Willmann M R, Chen H C, Sheen J. 2002. Calciumsignaling through protein kinases. The Arabidopsis calciumdependentprotein kinase gene family. Plant Physiology,129, 469-485

Choi H I, Park H J, Park J H, Kim S, Im M Y, Seo H H, KimY W, Hwang I, Kim S Y. 2005. Arabidopsis calciumdependentprotein kinase AtCPK32 interacts with ABF4, atranscriptional regulator of abscisic acid-responsive geneexpression, and modulates its activity. Plant Physioogy,139, 1750-1761

Chothia C, Gough J, Vogel C, Teichmann S A. 2003. Evolutionof the protein repertoire. Science, 300, 1701-1703

Curran B, Jonas D, Grundmann H, Pitt T, Dowson C G. 2004.Development of a multilocus sequence typing scheme forthe opportunistic pathogen Pseudomonas aeruginosa.Journal of Clinical Microbiology, 42, 5644-5649

Finn R D, Clements J, Eddy S R. 2011. HMMER web server:Interactive sequence similarity searching. Nucleic AcidsResearch, 39, W29-W37.

Gargantini P R, Gonzalez-Rizzo S, Chinchilla D, Raices M,Giammaria V, Ulloa R M, Frugier F, Crespi M D. 2006.A CDPK isoform participates in the regulation of nodulenumber in Medicago truncatula. The Plant Journal, 48,843-856

Gu Z, Cavalcanti A, Chen F C, Bouman P, Li W H. 2002.Extent of gene duplication in the genomes of Drosophila,nematode, and yeast. Molecular Biology Evolution, 19,256-262

Harmon A C. 2003. Calcium-regulated protein kinases of plants.Gravitational and Space Biology Bulletin, 16, 83-90

Harper J F, Breton G, Harmon A. 2004. Decoding Ca(2+)signals through plant protein kinases. Annual Review ofPlant Biology, 55, 263-288

He H, Dong Q, Shao Y, Jiang H, Zhu S, Cheng B, Xiang Y. 2012.Genome-wide survey and characterization of the WRKYgene family in Populus trichocarpa. Plant Cell Reports,31, 1199-1217

Hetherington A M, Brownlee C. 2004. The generation ofCa(2+) signals in plants. Annual Review of Plant Biology,55, 401-427

Hrabak E M, Chan C W, Gribskov M, Harper J F, Choi J H,Halford N, Kudla J, Luan S, Nimmo H G, Sussman M R,Thomas M, Walker-Simmons K, Zhu J K, Harmon A C.2003. The Arabidopsis CDPK-SnRK superfamily of proteinkinases. Plant Physiology, 132, 666-680

Hrabak E M, Dickmann L J, Satterlee J S, Sussman M R. 1996.Characterization of eight new members of the calmodulinlikedomain protein kinase gene family from Arabidopsisthaliana. Plant Molecular Biology, 31, 405-412

Huang Q S, Wang H Y, Gao P, Wang G Y, Xia G X. 2008.Cloning and characterization of a calcium dependent proteinkinase gene associated with cotton fiber development. PlantCell Reports, 27, 1869-1875

Hurst L D. 2002. The Ka/Ks ratio: Diagnosing the form ofsequence evolution. Trends in Genetics, 18, 486.Johnson D R, Bhatnagar R S, Knoll L J, Gordon J I. 1994.Genetic and biochemical studies of protein N-myristoylation.Annual Review Biochemistry, 63, 869-914

Kerr M K. 2003. Linear models for microarray data analysis:Hidden similarities and differences. Journal of ComputationalBiology, 10, 891-901

Komatsu S, Yang G, Khan M, Onodera H, Toki S, YamaguchiM. 2007. Over-expression of calcium-dependent proteinkinase 13 and calreticulin interacting protein 1 confers coldtolerance on rice plants. Molecular Genetic and Genomics,277, 713-723

Kong X, Lv W, Jiang S, Zhang D, Cai G, Pan J, Li D. 2013.Genome-wide identification and expression analysisof calcium-dependent protein kinase in maize. BMCGenomics, 14, 433.

Larkin M A, Blackshields G, Brown N P, Chenna R, McGettiganP A, McWilliam H, Valentin F, Wallace I M, Wilm A, LopezR, Thompson J D, Gibson T J, Higgins D G. 2007. ClustalW and Clustal X version 2.0. Bioinformatics, 23, 2947-2948

de Las Rivas B, Marcobal A, Munoz R. 2004. Allelic diversityand population structure in Oenococcus oeni as determinedfrom sequence analysis of housekeeping genes. Appliedand Environmental Microbiology, 70, 7210-7219

Lecourieux D, Ranjeva R, Pugin A. 2006. Calcium in plantdefence-signalling pathways. New Phytologist, 171, 249-269

Long M, Rosenberg C, Gilbert W. 1995. Intron phasecorrelations and the evolution of the intron/exon structureof genes. Proceeding of the National Academy of Sciencesof the United States of America, 92, 12495-12499

Lu S X, Hrabak E M. 2013. The myristoylated amino-terminus ofan Arabidopsis calcium-dependent protein kinase mediatesplasma membrane localization. Plant Molecular Biology,82, 267-278

Ma S Y, Wu W H. 2007. AtCPK23 functions in Arabidopsisresponses to drought and salt stresses. Plant MolecularBiology, 65, 511-518

Munemasa S, Hossain M A, Nakamura Y, Mori I C, Murata Y.2011. The Arabidopsis calcium-dependent protein kinase,CPK6, functions as a positive regulator of methyl jasmonatesignaling in guard cells. Plant Physiology, 155, 553-561

Ohno S, Wolf U, Atkin N B. 1968. Evolution from fish tomammals by gene duplication. Hereditas, 59, 169-187

Paterson A H, Wendel J F, Gundlach H, Guo H, Jenkins J, JinD, Llewellyn D, Showmaker K C, Shu S, Udall J, Yoo M J,Byers R, Chen W, Doron-Faigenboim A, Duke M V, GongL, Grimwood J, Grover C, Grupp K, Hu G, et al. 2012.Repeated polyploidization of Gossypium genomes and theevolution of spinnable cotton fibres. Nature, 492, 423-427

Ray S, Agarwal P, Arora R, Kapoor S, Tyagi A K. 2007.Expression analysis of calcium-dependent protein kinasegene family during reproductive development and abioticstress conditions in rice (Oryza sativa L. ssp. indica).Molecular Genetics and Genomics, 278, 493-505

 Romeis T, Piedras P, Jones J D. 2000. Resistance genedependentactivation of a calcium-dependent protein kinasein the plant defense response. The Plant Cell, 12, 803-816

Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K. 2000. Overexpressionof a single Ca2+-dependent protein kinaseconfers both cold and salt/drought tolerance on rice plants.The Plant Journal, 23, 319-327

Suyama M, Torrents D, Bork P. 2006. PAL2NAL: Robustconversion of protein sequence alignments into thecorresponding codon alignments. Nucleic Acids Research,34, W609-W612.

Szczegielniak J, Borkiewicz L, Szurmak B, Lewandowska-Gnatowska E, Statkiewicz M, Klimecka M, Ciesla J,Muszynska G. 2012. Maize calcium-dependent proteinkinase (ZmCPK11): Local and systemic response towounding, regulation by touch and components ofjasmonate signaling. Physiologia Plantarum, 146, 1-14

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, KumarS. 2011. MEGA5: Molecular evolutionary genetics analysisusing maximum likelihood, evolutionary distance, andmaximum parsimony methods. Molecular Biology Evolution,28, 2731-2739

Towler D A, Gordon J I, Adams S P, Glaser L. 1988. The biologyand enzymology of eukaryotic protein acylation. AnnualReview Biochemistry, 57, 69-99

Wan B, Lin Y, Mou T. 2007. Expression of rice Ca(2+)-dependent protein kinases (CDPKs) genes under differentenvironmental stresses. FEBS Letters, 581, 1179-1189

Wang H, Mei W, Qin Y, Zhu Y. 2011. 1-Aminocyclopropane-1-carboxylic acid synthase 2 is phosphorylated by calciumdependentprotein kinase 1 during cotton fiber elongation

Acta Biochimica et Biophysica Sinica, 43, 654-661

Wang K, Wang Z, Li F, Ye W, Wang J, Song G, Yue Z, CongL, Shang H, Zhu S, Zou C, Li Q, Yuan Y, Lu C, Wei H, GouC, Zheng Z, Yin Y, Zhang X, Liu K, et al. 2012. The draftgenome of a diploid cotton Gossypium raimondii. NatureGenetics, 44, 1098-1103

Wei K, Wang Y, Xie D. 2013. Identification and expressionprofile analysis of the protein kinase gene superfamily inmaize development. Molecular Breeding, 33, 155-172

Wernimont A K, Amani M, Qiu W, Pizarro J C, Artz J D, Lin YH, Lew J, Hutchinson A, Hui R. 2011. Structures of parasiticCDPK domains point to a common mechanism of activation.Proteins, 79, 803-820

Wernimont A K, Artz J D, Finerty Jr P, Lin Y H, Amani M, Allali-Hassani A, Senisterra G, Vedadi M, Tempel W, MackenzieF, Chau I, Lourido S, Sibley L D, Hui R. 2010. Structuresof apicomplexan calcium-dependent protein kinases revealmechanism of activation by calcium. Nature StructuralMolecular Biology, 17, 596-601

Yang S, Zhang X, Yue J X, Tian D, Chen J Q. 2008. Recentduplications dominate NBS-encoding gene expansion intwo woody species. Molecular Genetics and Genomics,280, 187-198

Ye S, Wang L, Xie W, Wan B, Li X, Lin Y. 2009. Expressionprofile of calcium-dependent protein kinase (CDPKs)genes during the whole lifespan and under phytohormonetreatment conditions in rice (Oryza sativa L. ssp. indica).Plant Molecular Biology, 70, 311-325

Yuan X, Deng K, Zhao X, Wu X, Qin Y, Tang D, Liu X. 2007.A calcium-dependent protein kinase is involved in planthormone signal transduction in Arabidopsis. Journal of PlantPhysiology and Molecular Biology, 33, 227.

Zhu S Y, Yu X C, Wang X J, Zhao R, Li Y, Fan R C, Shang Y,Du S Y, Wang X F, Wu F Q, Xu Y H, Zhang X Y, Zhang DP. 2007. Two calcium-dependent protein kinases, CPK4and CPK11, regulate abscisic acid signal transduction inArabidopsis. The Plant Cell, 19, 3019-3036

Zhu Y N, Shi D Q, Ruan M B, Zhang L L, Meng Z H, Liu J,Yang W C. 2013. Transcriptome analysis reveals crosstalkof responsive genes to multiple abiotic stresses in cotton(Gossypium hirsutum L.). PLOS ONE, 8, e80218.

Zuo R, Hu R, Chai G, Xu M, Qi G, Kong Y, Zhou G. 2013.Genome-wide identification, classification, and expressionanalysis of CDPK and its closely related gene families inpoplar (Populus trichocarpa). Molecular Biology Reports,40, 2645-2662
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