Calcium-dependent protein kinase (CDPK) and CDPK-related kinase (CRK) gene families in tomato: genome-wide identification and functional analyses in disease resistance

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• 作者：Ji-Peng Wang ; You-Ping Xu ; Jean-Pierre Munyampundu…
• 关键词：Calcium ; dependent protein kinase (CDPK) ; CDPK ; related kinase (CRK) ; Genome ; wide identification ; Phylogeny ; Resistance ; Tomato
• 刊名：Molecular Genetics and Genomics
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：291
• 期：2
• 页码：661-676
• 全文大小：3,445 KB
• 参考文献：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 46:356–366CrossRef PubMed
  Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36CrossRef PubMed
  Bologna G, Yvon C, Duvaud S, Veuthey AL (2004) N-terminal myristoylation predictions by ensembles of neural networks. Proteomics 4:1626–1632CrossRef PubMed
  Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40CrossRef PubMed PubMedCentral
  Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–422CrossRef PubMed PubMedCentral
  Cai X, Wang C, Xu Y, Xu Q, Zheng Z, Zhou X (2007) Efficient gene silencing induction in tomato by a viral satellite DNA vector. Virus Res 125:169–175CrossRef PubMed
  Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, San Segundo B (2014) Overexpression of a Calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiol 165:688–704CrossRef PubMed PubMedCentral
  Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485CrossRef PubMed PubMedCentral
  Cheng WS, Xu QF, Li F, Xu YP, Cai XZ (2012) Establishment of a suitable control vector for Tobacco rattle virus-induced gene silencing analysis in Nicotiana benthamiana. J Zhejiang Univ (Agric Life Sci) 38:10–20
  Coca M, San Segundo B (2010) AtCPK1 calcium-dependent protein kinase mediates pathogen resistance in Arabidopsis. Plant J 63:526–540CrossRef PubMed
  Confalonieri S, Di Fiore PP (2002) The Eps15 homology (EH) domain. FEBS Lett 513:24–29CrossRef PubMed
  Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRef PubMed PubMedCentral
  Gao X, Chen X, Lin W, Chen S, Lu D, Niu Y, Li L, Cheng C, McCormack M, Sheen J (2013) Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLoS Pathog 9:e1003127CrossRef PubMed PubMedCentral
  Guo A, Zhu Q, Chen X, Luo J (2007) GSDS: a gene structure display server. Yi chuan 29:1023–1026CrossRef PubMed
  Hamel LP, Sheen J, Séguin A (2014) Ancient signals: comparative genomics of green plant CDPKs. Trends Plant Sci 19:79–89CrossRef PubMed PubMedCentral
  Harmon AC, Gribskov M, Harper JF (2000) CDPKs–a kinase for every Ca2+ signal? Trends Plant Sci 5:154–159CrossRef PubMed
  Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6:555–566CrossRef PubMed
  Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288CrossRef PubMed
  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 132:666–680CrossRef PubMed PubMedCentral
  Huttner IG, Strahl T, Osawa M, King DS, Ames JB, Thorner J (2003) Molecular interactions of yeast frequenin (Frq1) with the phosphatidylinositol 4-kinase isoform, Pik1. J Biol Chem 278:4862–4874CrossRef PubMed
  Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMed
  Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H (2010) Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J 64:140–150PubMed
  Kim H-J, Chen C, Kabbage M, Dickman MB (2011) Identification and characterization of Sclerotinia sclerotiorum NADPH oxidases. Appl Environ Microbiol 77(21):7721–7729CrossRef PubMed PubMedCentral
  Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080CrossRef PubMed PubMedCentral
  Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563CrossRef PubMed PubMedCentral
  Leclercq J, Ranty B, Sanchez-Ballesta MT, Li ZG, 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 56:25–35PubMed
  Li RJ, Hua W, Lu YT (2006) Arabidopsis cytosolic glutamine synthetase AtGLN1;1 is a potential substrate of AtCRK3 involved in leaf senescence. Biochem Biophys Res Commun 342:119–126CrossRef PubMed
  Li AL, Zhu YF, Tan XM, Wang X, Wei B, Guo HZ, Zhang ZL, Chen XB, Zhao GY, Kong XY (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66:429–443CrossRef PubMed
  Liu HT, Gao F, Li GL, Han JL, Liu DL, Sun DY, Zhou RG (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55:760–773CrossRef PubMed
  Liu W, Li W, He Q, Daud MK, Chen J, Zhu S (2014) Genome-wide survey and expression analysis of calcium-dependent protein kinase in Gossypium raimondii. PLoS One 9:e98189CrossRef PubMed PubMedCentral
  Ludwig AA, Romeis T, Jones JD (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55:181–188CrossRef PubMed
  Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736–10741CrossRef PubMed PubMedCentral
  Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A, Segonzac C, Malinovsky FG, Rathjen JP, MacLean D, Romeis T (2014) The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16:605–615CrossRef PubMed
  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 278:493–505CrossRef PubMed
  Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032CrossRef PubMed PubMedCentral
  Rigo G, Ayaydin F, Tietz O, Zsigmond L, Kovacs H, Pay A, Salchert K, Darula Z, Medzihradszky KF, Szabados L, Palme K, Koncz C, Cseplo A (2013) Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25:1592–1608CrossRef PubMed PubMedCentral
  Romeis T, Herde M (2014) From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Curr Opin Plant Biol 20:1–10CrossRef PubMed
  Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556–5567CrossRef PubMed PubMedCentral
  Saand MA, Xu YP, Li W, Wang JP, Cai XZ (2015) Cyclic nucleotide gated channel gene family in tomato:genome-wide identification and functional analyses in disease resistance. Front Plant Sci 6:303CrossRef PubMed PubMedCentral
  Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(suppl.):S401–S417PubMed PubMedCentral
  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 28:2731–2739CrossRef PubMed PubMedCentral
  Tao XC, Lu YT (2013) Loss of AtCRK1 gene function in Arabidopsis thaliana decreases tolerance to salt. J Plant Biol 56:306–314CrossRef
  Valmonte GR, Arthur K, Higgins CM, MacDiarmid RM (2014) Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol 55:551–569CrossRef PubMed
  Wang Y, Liang SP, Xie QG, Lu YT (2004) Characterization of a calmodulin-regulated Ca2+-dependent-protein-kinase-related protein kinase, AtCRK1, from Arabidopsis. Biochem J 383:73–81CrossRef PubMed PubMedCentral
  Wang C, Cai X, Wang X, Zheng Z (2006) Optimisation of tobacco rattle virus-induced gene silencing in Arabidopsis. Funct Plant Biol 33:347–355CrossRef
  Xie K, Chen J, Wang Q, Yang Y (2014) Direct phosphorylation and activation of a mitogen-activated protein kinase by a calcium-dependent protein kinase in rice. Plant Cell 26:3077–3089CrossRef PubMed PubMedCentral
  Zhang XS, Choi JH (2001) Molecular evolution of calmodulin-like domain protein kinases (CDPKs) in plants and protists. J Mol Evol 53:214–224CrossRef PubMed
  Zhang H, Liu WZ, Zhang Y, Deng M, Niu F, Yang B, Wang X, Wang B, Liang W, Deyholos MK (2014) Identification, expression and interaction analyses of calcium-dependent protein kinase (CPK) genes in canola (Brassica napus L.). BMC Genom 15:211CrossRef
  Zhao Y, Liu W, Xu YP, Cao JY, Braam J, Cai XZ (2013) Genome-wide identification and functional analyses of calmodulin genes in Solanaceous species. BMC Plant Biol 13:70CrossRef PubMed PubMedCentral
  Zhou L, Lan W, Jiang Y, Fang W, Luan S (2013) A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol Plant 7:369–376CrossRef PubMed
  Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036CrossRef PubMed PubMedCentral
  Zuo R, Hu R, Chai G, Xu M, Qi G, Kong Y, Zhou G (2013) Genome-wide identification, classification, and expression analysis of CDPK and its closely related gene families in poplar (Populus trichocarpa). Mol Biol Rep 40:2645–2662CrossRef PubMed
  
• 作者单位：Ji-Peng Wang (1)
  You-Ping Xu (2)
  Jean-Pierre Munyampundu (1)
  Tian-Yu Liu (1)
  Xin-Zhong Cai (1)
  
  1. Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou, 310058, China
  2. Center of Analysis and Measurement, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou, 310058, China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Biochemistry
  Microbial Genetics and Genomics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1617-4623

文摘

Calcium-dependent protein kinases (CDPKs) and CDPK-related kinases (CRKs) play multiple roles in plant. Nevertheless, genome-wide identification of these two families is limited to several plant species, and role of CRKs in disease resistance remains unclear. In this study, we identified the CDPK and CRK gene families in genome of the economically important crop tomato (Solanum lycopersicum L.) and analyzed their function in resistance to various pathogens. Twenty-nine CDPK and six CRK genes were identified in tomato genome. Both SlCDPK and SlCRK proteins harbored an STKc_CAMK type protein kinase domain, while only SlCDPKs contained EF-hand type Ca2+ binding domain(s). Phylogenetic analysis revealed that plant CRK family diverged early from CDPKs, and shared a common ancestor gene with subgroup IV CDPKs. Subgroup IV SlCDPK proteins were basic and their genes contained 11 introns, which were distinguished from other subgroups but similar to CRKs. Subgroup I SlCDPKs generally did not carry an N-terminal myristoylation motif while those of the remaining subgroups and SlCRKs universally did. SlCDPK and SlCRK genes were differently responsive to pathogenic stimuli. Furthermore, silencing analyses demonstrated that SlCDPK18 and SlCDPK10 positively regulated nonhost resistance to Xanthomonas oryzae pv. oryzae and host resistance to Pseudomonas syringae pv. tomato (Pst) DC3000, respectively, while SlCRK6 positively regulated resistance to both Pst DC3000 and Sclerotinia sclerotiorum in tomato. In conclusion, CRKs apparently evolved from CDPK lineage, SlCDPK and SlCRK genes regulate a wide range of resistance and SlCRK6 is the first CRK gene proved to function in plant disease resistance.