Abstract
Calcium-dependent protein kinases (CDPKs) are Ca2+-binding proteins known to play crucial roles in Ca2+ signal transduction pathways which have been identified throughout plant kingdom and in certain types of protists. Genome-wide analysis of CDPKs have been carried out in Arabidopsis, rice and wheat, and quite a few of CDPKs were proved to play crucial roles in plant stress responsive signature pathways. In this study, a comprehensive analysis of Populus CDPK and its closely related gene families was performed, including phylogeny, chromosome locations, gene structures, and expression profiles. Thirty Populus CDPK genes and twenty closely related kinase genes were identified, which were phylogenetically clustered into eight distinct subfamilies and predominately distributed across fifteen linkage groups (LG). Genomic organization analyses indicated that purifying selection has played a pivotal role in the retention and maintenance of Populus CDPK gene family. Furthermore, microarray analysis showed that a number of Populus CDPK and its closely related genes differentially expressed across disparate tissues and under various stresses. The expression profiles of paralogous pairs were also investigated to reveal their evolution fates. In addition, quantitative real-time RT-PCR was performed on nine selected CDPK genes to confirm their responses to drought stress treatment. These observations may lay the foundation for future functional analysis of Populus CDPK and its closely related gene families to unravel their biological roles.
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References
Trewavas AJ, Malhó R (1998) Ca2+ signalling in plant cells: the big network! Curr Opin Plant Biol 1(5):428–433
Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6(6):262–267
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:S389–S400
Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci 160(3):381–404
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417
Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151(1):35–66
Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11(4):691–706
Hernández Sebastià C, Hardin SC, Clouse SD, Kieber JJ, Huber SC (2004) Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch Biochem Biophys 428(1):81–91
Hrabak EM, Chan CWM, 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(2):666–680
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(1):43–58
McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159(3):585–598
Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Phys 49:697–725
Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129(2):469–485
Yang TB, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8(10):505–512
Wernimont AK, Amani M, Qiu W, Pizarro JC, Artz JD, Lin YH, Lew J, Hutchinson A, Hui R (2011) Structures of parasitic CDPK domains point to a common mechanism of activation. Proteins 79(3):803–820
Wernimont AK, Artz JD, Finerty P Jr, Lin YH, Amani M, Allali-Hassani A, Senisterra G, Vedadi M, Tempel W, Mackenzie F, Chau I, Lourido S, Sibley LD, Hui R (2010) Structures of apicomplexan calcium-dependent protein kinases reveal mechanism of activation by calcium. Nat Struct Mol Biol 17(5):596–601
Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6(7):555–566
Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23(3):319–327
Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55(4):541–552
Asano T, Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75(1):179–191
Asano T, Wakayama M, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2010) Overexpression of a calcium-dependent protein kinase gene enhances growth of rice under low-nitrogen conditions. Plant Biotechnol 27(4):369–373
Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154(3):1232–1243
Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19(10):3019–3036
Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2011) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192(1):61–73
Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65(4):511–518
Xu J, Tian YS, Peng RH, Xiong AS, Zhu B, Jin XF, Gao F, Fu XY, Hou XL, Yao QH (2010) AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231(6):1251–1260
Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46(2):356–366
Ray S, Agarwal P, Arora R, Kapoor S, Tyagi AK (2007) Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica). Mol Genet Genomics 278(5):493–505
Li AL, Zhu YF, Tan XM, Wang X, Wei B, Guo HZ, Zhang ZL, Chen XB, Zhao GY, Kong XY, Jia JZ, Mao L (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66(4):429–443
Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303(5662):1361–1364
Leclercq J, Ranty B, Sanchez-Ballesta MT, Li Z, Jones B, Jauneau A, Pech JC, Latche A, Ranjeva R, Bouzayen M (2005) Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J Exp Bot 56(409):25–35
Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30(1):235–238
Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2008) CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 21(11):639–644
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882
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(10):2731–2739
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
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29(8):1023–1026
Barrett T, Edgar R (2006) Gene expression omnibus: microarray data storage, submission, retrieval, and analysis. Methods Enzymol 411:352–369
Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149(2):981–993
Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18(1):207–208
Cohen D, Bogeat-Triboulot MB, Tisserant E, Balzergue S, Martin-Magniette ML, Lelandais G, Ningre N, Renou JP, Tamby JP, Le Thiec D, Hummel I (2010) Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics 11:630
Yuan Y, Chung JD, Fu X, Johnson VE, Ranjan P, Booth SL, Harding SA, Tsai CJ (2009) Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis. Proc Natl Acad Sci USA 106(51):22020–22025
Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61(14):4011–4019
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11(2):113–116
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25(4):402–408
Hrabak EM, Dickmann LJ, Satterlee JS, Sussman MR (1996) Characterization of eight new members of the calmodulin-like domain protein kinase gene family from Arabidopsis thaliana. Plant Mol Biol 31(2):405–412
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604
Christodoulou J, Malmendal A, Harper JF, Chazin WJ (2004) Evidence for differing roles for each lobe of the calmodulin-like domain in a calcium-dependent protein kinase. J Biol Chem 279(28):29092–29100
Franz S, Ehlert B, Liese A, Kurth J, Cazale AC, Romeis T (2011) Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 4(1):83–96
Johnson DR, Bhatnagar RS, Knoll LJ, Gordon JI (1994) Genetic and biochemical studies of protein N-myristoylation. Annu Rev Biochem 63:869–914
Mehlmer N, Wurzinger B, Stael S, Hofmann-Rodrigues D, Csaszar E, Pfister B, Bayer R, Teige M (2010) The Ca(2+)-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant J 63(3):484–498
Luan S (2011) Coding and decoding of calcium signals in plants, vol. 10. Springer, Berlin
Lindzen E, Choi JH (1995) A carrot cDNA encoding an atypical protein kinase homologous to plant calcium-dependent protein kinases. Plant Mol Biol 28(5):785–797
Zhang L, Liu BF, Liang S, Jones RL, Lu YT (2002) Molecular and biochemical characterization of a calcium/calmodulin-binding protein kinase from rice. Biochem J 368(Pt 1):145–157
Liu Z, Xia M, Poovaiah BW (1998) Chimeric calcium/calmodulin-dependent protein kinase in tobacco: differential regulation by calmodulin isoforms. Plant Mol Biol 38(5):889–897
Patil S, Takezawa D, Poovaiah BW (1995) Chimeric plant calcium/calmodulin-dependent protein kinase gene with a neural visinin-like calcium-binding domain. Proc Natl Acad Sci USA 92(11):4897–4901
Takezawa D, Ramachandiran S, Paranjape V, Poovaiah BW (1996) Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J Biol Chem 271(14):8126–8132
Hu R, Chi X, Chai G, Kong Y, He G, Wang X, Shi D, Zhang D, Zhou G (2012) Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS ONE 7(2):e31149
Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145
Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21(12):3749–3766
Barakat A, Bagniewska-Zadworna A, Choi A, Plakkat U, DiLoreto DS, Yellanki P, Carlson JE (2009) The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression. BMC Plant Biol 9:26
Barakat A, Choi A, Yassin NB, Park JS, Sun Z, Carlson JE (2011) Comparative genomics and evolutionary analyses of the O-methyltransferase gene family in Populus. Gene 479(1–2):37–46
Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59
Zhuang J, Cai B, Peng RH, Zhu B, Jin XF, Xue Y, Gao F, Fu XY, Tian YS, Zhao W, Qiao YS, Zhang Z, Xiong AS, Yao QH (2008) Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Biophys Res Commun 371(3):468–474
Tuominen LK, Johnson VE, Tsai CJ (2011) Differential phylogenetic expansions in BAHD acyltransferases across five angiosperm taxa and evidence of divergent expression among Populus paralogues. BMC Genomics 12:236
Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16(7):1679–1691
Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16(7):1667–1678
Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102(15):5454–5459
Yang X, Tuskan GA, Cheng MZ (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142(3):820–830
Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3(11):827–837
Urao T, Katagiri T, Mizoguchi T, Yamaguchi-Shinozaki K, Hayashida N, Shinozaki K (1994) Two genes that encode Ca(2+)-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol Gen Genet 244(4):331–340
Acknowledgments
This study was supported by grants from the National Basic Research Program of China (2012CB114501), the National High-Tech Research and Development Program of China (2011AA100209), the National Natural Science Foundation of China (31070272, 31000311 and 30901157), the Program of 100 Distinguished Young Scientists of the Chinese Academy of Sciences (to Gongke Zhou), the Promotive Research Fund for Young and Middle-aged Scientists of Shandong Province (BS2011SW055), and the Qingdao Municipal Science and Technology Plan Project (11-2-4-8-(1)-jch, 11-2-4-8-(2)-jch and 12-1-4-9-(2)-jch). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Zuo, R., Hu, R., Chai, G. et al. Genome-wide identification, classification, and expression analysis of CDPK and its closely related gene families in poplar (Populus trichocarpa). Mol Biol Rep 40, 2645–2662 (2013). https://doi.org/10.1007/s11033-012-2351-z
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DOI: https://doi.org/10.1007/s11033-012-2351-z