Differential expression of CPKs and cytosolic Ca2+ variation in resistant and susceptible apple cultivars (Malus x domestica) in response to the pathogen Erwinia amylovora and mechanical wounding

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Kanchiswamy, Chidananda Nagamangala ^a   Mohanta, Tapan K ^b   Capuzzo, Andrea ^b   Occhipinti, Andrea ^b   Verrillo, Francesca ^b   Maffei, Massimo E ^b   Malnoy, Mickael ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Calcium dependent Protein Kinases; Cytosolic calcium variations; Erwinia amylovora; Gene expression; Malus x domestica; Phylogenetic analysis

Indexed keywords

CALCIUM ION; CALCIUM PROTEIN KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG;

APPLE; ARABIDOPSIS THALIANA; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CULTIVAR; CYTOSOL; ERWINIA AMYLOVORA; FIRE BLIGHT; GENE EXPRESSION; MAIZE; MULTIGENE FAMILY; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PLANT DAMAGE; PLANT GENE; PLANT RESPONSE; POPULUS TRICHOCARPA; REAL TIME POLYMERASE CHAIN REACTION; RICE; SPECIES DIFFERENCE;

ARABIDOPSIS THALIANA; DICOTYLEDONEAE; ERWINIA AMYLOVORA; MALUS; MALUS X DOMESTICA; ORYZA SATIVA; ZEA MAYS;

CALCIUM SIGNALING; DISEASE RESISTANCE; ERWINIA AMYLOVORA; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MALUS; PHYLOGENY; PLANT DISEASES; PROTEIN KINASES; STRESS, MECHANICAL;

EID: 84887076380     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-760     Document Type: Article

References (68)

1. Harper JF, Harmon A. Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 2005, 6(7):555-566. 10.1038/nrm1679, 16072038.
2. Knight MR, Campbell AK, Smith SM, Trewavas AJ. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 1991, 352(6335):524-526. 10.1038/352524a0, 1865907.
3. Kanchiswamy CN, Takahashi H, Quadro S, Maffei ME, Bossi S, Bertea C, Zebelo SA, Muroi A, Ishihama N, Yoshioka H, et al. Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol 2010, 10:97. 10.1186/1471-2229-10-97, 3095362, 20504319.
4. Arimura G, Maffei ME. Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem Biophys Res Commun 2010, 400(4):455-460. 10.1016/j.bbrc.2010.08.134, 20816754.
5. Ma W. Roles of Ca2+ and cyclic nucleotide gated channel in plant innate immunity. Plant Sci: Int J Exp Plant Biol 2011, 181(4):342-346.
6. Gao X, Chen X, Lin W, Chen S, Lu D, Niu Y, Li L, Cheng C, McCormack M, Sheen J, et al. Bifurcation of Arabidopsis NLR immune signaling via Ca(2)(+)-dependent protein kinases. PLoS Pathog 2013, 9(1):e1003127. 10.1371/journal.ppat.1003127, 3561149, 23382673.
7. Sanders D, Brownlee C, Harper JF. Communicating with calcium. The Plant cell 1999, 11(4):691-706. 144209, 10213787.
8. Hernandez Sebastia C, Hardin SC, Clouse SD, Kieber JJ, Huber SC. Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch Biochem Biophys 2004, 428(1):81-91. 10.1016/j.abb.2004.04.025, 15234272.
9. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 2003, 132(2):666-680. 10.1104/pp.102.011999, 167006, 12805596.
10. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 2002, 14(Suppl):S389-400. 151268, 12045290.
11. Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithofer A. CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiol 2012, 159(3):1159-1175. 10.1104/pp.112.198150, 3387702, 22570470.
12. Ma P, Liu J, Yang X, Ma R. Genome-wide identification of the maize calcium-dependent protein kinase gene family. Appl Biochem Biotechnol 2013, 169(7):2111-2125. 10.1007/s12010-013-0125-2, 23397323.
13. Zuo R, Hu R, Chai G, Xu M, Qi G, Kong Y, Zhou G. Genome-wide identification, classification, and expression analysis of CDPK and its closely related gene families in poplar (Populus trichocarpa). Mol Biol Rep 2013, 40(3):2645-2662. 10.1007/s11033-012-2351-z, 23242656.
14. Li AL, Zhu YF, Tan XM, Wang X, Wei B, Guo HZ, Zhang ZL, Chen XB, Zhao GY, Kong XY, et al. Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 2008, 66(4):429-443. 10.1007/s11103-007-9281-5, 18185910.
15. Cheng SH, Willmann MR, Chen HC, Sheen J. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 2002, 129(2):469-485. 10.1104/pp.005645, 1540234, 12068094.
16. Harper JF, Breton G, Harmon A. Decoding Ca(2+) signals through plant protein kinases. Annu Rev Plant Biol 2004, 55:263-288. 10.1146/annurev.arplant.55.031903.141627, 15377221.
17. Harmon AC, Yoo BC, McCaffery C. Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 1994, 33(23):7278-7287. 10.1021/bi00189a032, 8003491.
18. Ito T, Nakata M, Fukazawa J, Ishida S, Takahashi Y. Alteration of substrate specificity: the variable N-terminal domain of tobacco Ca(2+)-dependent protein kinase is important for substrate recognition. Plant Cell 2010, 22(5):1592-1604. 10.1105/tpc.109.073577, 2899867, 20442373.
19. Camoni L, Harper JF, Palmgren MG. 14-3-3 proteins activate a plant calcium-dependent protein kinase (CDPK). FEBS Lett 1998, 430(3):381-384. 10.1016/S0014-5793(98)00696-6, 9688575.
20. Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, et al. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 2006, 4(10):e327. 10.1371/journal.pbio.0040327, 1592316, 17032064.
21. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, et al. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 2007, 19(10):3019-3036. 10.1105/tpc.107.050666, 2174700, 17921317.
22. Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP. The Arabidopsis Ca(2+) -dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 2011, 192(1):61-73. 10.1111/j.1469-8137.2011.03793.x, 21692804.
23. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J. Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 2010, 464(7287):418-422. 10.1038/nature08794, 2841715, 20164835.
24. Gao X, He P. Nuclear dynamics of Arabidopsis calcium-dependent protein kinases in effector-triggered immunity. Plant Signal Behav 2013, 8(4):e23868. PMID: 23425856; http://dx.doi.org/10.4161/psb.23868, 10.4161/psb.23868, 23425856.
25. Shulaev V, Korban SS, Sosinski B, Abbott AG, Aldwinckle HS, Folta KM, Iezzoni A, Main D, Arus P, Dandekar AM, et al. Multiple models for Rosaceae genomics. Plant Physiol 2008, 147(3):985-1003. 10.1104/pp.107.115618, 2442536, 18487361.
26. Malnoy M, Martens S, Norelli JL, Barny MA, Sundin GW, Smits TH, Duffy B. Fire blight: applied genomic insights of the pathogen and host. Annu Rev Phytopathol 2012, 50:475-494. 10.1146/annurev-phyto-081211-172931, 22702352.
27. Venisse JS, Malnoy M, Faize M, Paulin JP, Brisset MN. Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. Mol Plant 2002, 15(12):1204-1212.
28. Baldo A, Norelli JL, Farrell RE, Bassett CL, Aldwinckle HS, Malnoy M. Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus x domestica) with Erwinia amylovora. BMC Plant Biol 2010, 10:1. 10.1186/1471-2229-10-1, 2827420, 20047654.
29. Gardiner SE, Norelli JL, De Silva N, Fazio G, Peil A, Malnoy M, Horner M, Bowatte D, Carlisle C, Wiedow C, et al. Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus 'Robusta 5' accessions. BMC Genet 2012, 13:25. 3443455, 22471693.
30. Jensen PJ, Halbrendt N, Fazio G, Makalowska I, Altman N, Praul C, Maximova SN, Ngugi HK, Crassweller RM, Travis JW, et al. Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. BMC Genomics 2012, 13:9. 10.1186/1471-2164-13-9, 3277459, 22229964.
31. Sarowar S, Zhao Y, Soria-Guerra RE, Ali S, Zheng D, Wang D, Korban SS. Expression profiles of differentially regulated genes during the early stages of apple flower infection with Erwinia amylovora. J Exp Bot 2011, 62(14):4851-4861. 10.1093/jxb/err147, 3193002, 21725032.
32. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 2012, 40(D1):D1178-D1186. 10.1093/nar/gkr944, 3245001, 22110026.
33. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D. The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 2010, 42(10):833-+.
34. Zou J-J, Wei F-J, Wang C, Wu J-J, Ratnasekera D, Liu W-X, Wu W-H. Arabidopsis Calcium-Dependent Protein Kinase CPK10 Functions in Abscisic Acid- and Ca2 + -Mediated Stomatal Regulation in Response to Drought Stress. Plant Physiol 2010, 154(3):1232-1243. 10.1104/pp.110.157545, 2971602, 20805328.
35. Asano T, Hayashi N, Kikuchi S, Ohsugi R. CDPK-mediated abiotic stress signaling. Plant Signal Behav 2012, 7(7):817-821. 10.4161/psb.20351, 3583972, 22751324.
36. Boudsocq M, Droillard MJ, Regad L, Lauriere C. Characterization of Arabidopsis calcium-dependent protein kinases: activated or not by calcium?. Biochem J 2012, 447(2):291-299. 10.1042/BJ20112072, 22827269.
37. Holder AA, Mohd Ridzuan MA, Green JL. Calcium dependent protein kinase 1 and calcium fluxes in the malaria parasite. Microbes Infect 2012, 14(10):825-830. 10.1016/j.micinf.2012.04.006, 22584104.
38. Szczegielniak J, Borkiewicz L, Szurmak B, Lewandowska-Gnatowska E, Statkiewicz M, Klimecka M, Ciesla J, Muszynska G. Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to wounding, regulation by touch and components of jasmonate signaling. Physiol Plant 2012, 146(1):1-14. 10.1111/j.1399-3054.2012.01587.x, 22289134.
39. Zebelo SA, Matsui K, Ozawa R, Maffei ME. Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Sci: Int J Exp Plant Biol 2012, 196:93-100.
40. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, et al. The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 2010, 42(10):833-839. 10.1038/ng.654, 20802477.
41. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P-F, Lindquist EA, Kamisugi Y, et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 2008, 319(5859):64-69. 10.1126/science.1150646, 18079367.
42. Ramakrishna W, Dubcovsky J, Park YJ, Busso C, Emberton J, SanMiguel P, Bennetzen JL. Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 2002, 162(3):1389-1400. 1462341, 12454082.
43. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, et al. A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2007, 2(12):e1326. 10.1371/journal.pone.0001326, 2147077, 18094749.
44. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 2012, 40(D1):D1202-D1210. 10.1093/nar/gkr1090, 3245047, 22140109.
45. Rocks O, Peyker A, Kahms M, Verveer PJ, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, Bastiaens PIH. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 2005, 307(5716):1746-1752. 10.1126/science.1105654, 15705808.
46. Asano T, Tanaka N, Yang GX, Hayashi N, Komatsu S. 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 2005, 46(2):356-366. 10.1093/pcp/pci035, 15695435.
47. Eckardt NA. Alternative splicing and the control of flowering time. The Plant cell 2002, 14(4):743-747. 10.1105/tpc.000000, 543397, 11971131.
48. Barbazuk WB, Fu Y, McGinnis KM. Genome-wide analyses of alternative splicing in plants: Opportunities and challenges. Genome Res 2008, 18(9):1381-1392. 10.1101/gr.053678.106, 18669480.
49. Furnham N, Ruffle S, Southan C. Splice variants: A homology modeling approach. Proteins-Structure Function and Genetics 2004, 54(3):596-608.
50. Wurzinger B, Mair A, Pfister B, Teige M. Cross-talk of calcium-dependent protein kinase and MAP kinase signaling. Plant Signal Behav 2011, 6(1):8-12. 10.4161/psb.6.1.14012, 3121996, 21248475.
51. Lu SX, Hrabak EM. The myristoylated amino-terminus of an Arabidopsis calcium-dependent protein kinase mediates plasma membrane localization. Plant Mol Biol 2013, 82(3):267-278. 10.1007/s11103-013-0061-0, 3668125, 23609608.
52. Ozawa R, Bertea CM, Foti M, Narayana R, Arimura G, Muroi A, Horiuchi J, Nishioka T, Maffei ME, Takabayashi J. Exogenous polyamines elicit herbivore-induced volatiles in lima bean leaves: involvement of calcium, H2O2 and Jasmonic acid. Plant Cell Physiol 2009, 50(12):2183-2199. 10.1093/pcp/pcp153, 19884250.
53. Mithofer A, Mazars C, Maffei ME. Probing Spatio-temporal Intracellular Calcium Variations in Plants. Methods Mol Biol 2009, 479:79-92. 10.1007/978-1-59745-289-2_5, 19083174.
54. Maffei ME, Mithofer A, Arimura G, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, et al. Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 2006, 140(3):1022-1035. 10.1104/pp.105.071993, 1400574, 16443697.
55. Maffei M, Bossi S, Spiteller D, Mithofer A, Boland W. Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 2004, 134(4):1752-1762. 10.1104/pp.103.034165, 419848, 15051862.
56. Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J: Cell Mol Biol 2000, 23(4):441-450.
57. Ma W, Smigel A, Tsai YC, Braam J, Berkowitz GA. Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 2008, 148(2):818-828. 10.1104/pp.108.125104, 2556846, 18689446.
58. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, Von Bodman S, Berkowitz GA. Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 2007, 19(3):1081-1095. 10.1105/tpc.106.045096, 1867353, 17384171.
59. Kado CI, Heskett MG. Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology 1970, 60(6):969-976. 10.1094/Phyto-60-969, 5469886.
60. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
61. Sigrist CJA, De Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I. New and continuing developments at PROSITE. Nucleic Acids Res 2013, 41(D1):E344-E347.
62. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
63. Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 2008, 21(11):639-644. 10.1093/protein/gzn039, 2569006, 18753194.
64. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22(2):195-201. 10.1093/bioinformatics/bti770, 16301204.
65. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
66. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.
67. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3(7):research0034.0031 - research0034.0011.
68. Bricchi I, Occhipinti A, Bertea CM, Zebelo SA, Brillada C, Verrillo F, De Castro C, Molinaro A, Faulkner C, Maule AJ, et al. Separation of early and late responses to herbivory in Arabidopsis by changing plasmodesmal function. Plant J 2013, 73(1):14-25.