Abstract
Calcium-dependent protein kinases (CDPKs) are important sensors of Ca+2 flux in plants, which control plant development and responses by regulating downstream components of calcium signaling pathways. Availability of the whole genome sequence and microarray platform allows investigation of genome-wide organization and expression profile of CDPK genes in rice with a view to ultimately define their function in plant systems. Genome-wide analysis led to identification of 31 CDPK genes in rice after a thorough annotation exercise based upon HMM profiles. Twenty-nine already identified CDPK genes were verified and two new members were added to the CDPK gene family of rice. Relative expression of all these genes has been analyzed by using Affymetrix rice genome array™ during three vegetative stages, six stages of panicle (P1–P6) and five stages of seed (S1–S5) development along with three abiotic stress conditions, viz. cold, salt and desiccation, given to seedling. Thirty-one CDPK genes were found to express in at least one of the experimental stages studied. Of these, transcripts for twenty three genes accumulated differentially during reproductive developmental stages; nine of them were preferentially up-regulated only in panicle, five were up-regulated in stages of panicles as well as seed development, whereas, expression of one gene was found to be specific to the S1 stage of seed development. Eight genes were found to be down-regulated during the panicle and seed developmental stages. Six CDPK genes were found to be induced while the expression of one gene was down-regulated under stress conditions. The differential expression of CDPK genes during reproductive development and stress is suggestive of their involvement in the underlying signal transduction pathways. Furthermore, up-regulation of common genes both during reproductive development as well as stress responses is indicative of common element between reproduction and stress.
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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 55:541–552
Akimoto-Tomiyama C, Sakata K, Yazaki J, Nakamura K, Fujii F, Shimbo K, Yamamoto K, Sasaki T, Kishimoto N, Kikuchi S, Shibuya N, Minami E (2003) Rice gene expression in response to N-acetylchitooligosaccharide elicitor: comprehensive analysis by DNA microarray with randomly selected ESTs. Plant Mol Biol 52:537–551
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, Takano M, Sato M, Furuhashi H, Mujin T, Takaiwa F, Wu CY, Tada Y, Satozawa T, Sakamoto M, Shimada H (2002) Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor. Plant Cell 14:619–628
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 46:356–366
Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In: Proceeding of the second international conference on intelligent systems for molecular biology, pp 28–36
Berberich T, Kusano T (1997) Cycloheximide induces a subset of low temperature-inducible genes in maize. Mol Gen Genet 254:275–283
Botella JR, Arteca JM, Somodevilla M, Arteca RN (1996) Calcium-dependent protein kinase gene expression in response to physical and chemical stimuli in mungbean (Vigna radiata). Plant Mol Biol 30:1129–1137
Breviario D, Morello L, Giani S (1995) Molecular cloning of two novel rice cDNA sequences encoding putative calcium-dependent protein kinase. Plant Mol Biol 27:953–967
Chehab EW, Patharkar OR, Hegeman AD, Taybi T, Cushman JC (2004) Autophosphorylation and subcellular localization dynamics of a salt- and water deficit-induced calcium-dependent protein kinase from ice plant. Plant Physiol 135:1430–1446
Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485
Chico JM, Raices M, Tellez-Inon MT, Ulloa RM (2002) A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol 128:256–270
Davletova S, Meszaros T, Miskolczi P, Oberschall A, Torok K, Magyar Z, Dudits D, Deak M (2001) Auxin and heat shock activation of a novel member of the calmodulin like domain protein kinase gene family in cultured alfalfa cells. J Exp Bot 52:215–221
Diaz-De-Leon F, Klotz KL, Lagrimini LM (1993) Nucleotide sequence of the tobacco (Nicotiana tabacum) anionic peroxidase gene. Plant Physiol 101:1117–1118
Dunn MA, White AJ, Vural S, Hughes MA (1998) Identification of promoter elements in a low-temperature-responsive gene (blt4.9) from barley (Hordeum vulgare L.). Plant Mol Biol 38:551–564
Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763
Estruch JJ, Kadwell S, Merlin E, Crossland L (1994) Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci USA 91:8837–8841
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 30:235–238
Frattini M, Morello L, Breviario D (1999) Rice calcium-dependent protein kinase isoforms OsCDPK2 and OSCDPK11 show different responses to light and different expression patterns during seed development. Plant Mol Biol 41:753–764
Furutani I, Sukegawa S, Kyozuka J (2006) Genome-wide analysis of spatial and temporal gene expression in rice panicle development. Plant J 46:503–511
Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA, Mundodi S, Reiser L, Rhee SY, Scholl R, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P (2002) TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2:239–253
Harmon AC, Yoo BC, McCaffery C (1994) Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33:7278–7287
Harmon AC, Gribskov M, Harper JF (2000) CDPKs—a kinase for every Ca2+ signal? Trends Plant Sci 5:154–159
Harmon AC, Gribskov M, Gubrium E, Harper JF (2001) The CDPK superfamily of protein kinases. New Phytol 151:175–183
Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6:555–566
Harper JF, Sussman MR, Schaller GE, Putnam-Evans C, Charbonneau H, Harmon AC (1991) A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science 252:951–954
Harper JF, Breton G, Harmon A (2004) Decoding Ca(2+) signals through plant protein kinases. Annu Rev Plant Biol 55:263–288
Hattori T, Terada T, Hamasuna S (1995) Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7:913–925
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
International Rice Genome Sequencing Project (2005) The map-based sequence of rice genome. Nature 436:793–800
Ishino T, Orito Y, Chinzei Y, Yuda M (2006) A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Micro 59:1175–1184
Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47
Ivashuta S, Liu J, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911–2921
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651
Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development and regulation by light and abiotic stress. Plant Physiol 143:1–17
Kawasaki T, Hayashida N, Baba T, Shinozaki K, Shimada H (1993) The gene encoding a calcium-dependent protein kinase located near the sbe1 gene encoding starch branching enzyme I is specifically expressed in developing rice seeds. Gene 129:183–189
Kim SY, Wu R (1990) Multiple protein factors bind to a rice glutelin promoter region. Nucleic Acids Res 18:6845–6852
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 19:1065–1080
Komatsu S, Yang G, Khan M, Onodera H, Toki S, Yamaguchi M (2007) Overexpression of calcium-dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants. Mol Genet Genomics 277:713–723
Kumar KG, Ullanat R, Jayabaskaran C (2004) Molecular cloning, characterization, tissue-specific and phytohormone-induced expression of calcium-dependent protein kinase gene in cucumber (Cucumis sativus L.). J Plant Physiol 161:1061–1071
Lan L, Li M, Lai Y, Xu W, Kong Z, Ying K, Han B, Xue Y (2005) Microarray analysis reveals similarities and variations in genetic programs controlling pollination/fertilization and stress responses in rice (Oryza sativa L.). Plant Mol Biol 59:151–164
Lantin S, O’Brien M, Matton DP (1999) Pollination, wounding and jasmonate treatments induce the expression of a developmentally regulated pistil dioxygenase at a distance, in the ovary, in the wild potato Solanum chacoense Bitt. Plant Mol Biol 41:371–386
Lee SS, Cho HS, Yoon GM, Ahn JW, Kim HH, Pai HS (2003) Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26 S proteasome in Nicotiana tabacum. Plant J 33:825–840
Liu G, Chen J, Wang X (2006) VfCPK1, a gene encoding calcium-dependent protein kinase from Vicia faba, is induced by drought and abscisic acid. Plant Cell Environ 29:2091–2099
Llop-Tous I, Dominguez-Puigjaner E, Vendrell M (2002) Characterization of a strawberry cDNA clone homologous to calcium-dependent protein kinases that is expressed during fruit ripening and affected by low temperature. J Exp Bot 53:2283–2285
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:S389–400
Ludwig AA, Romeis T, Jones JD (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55:181–188
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158
Monroy AF, Dhindsa RS (1995) Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. Plant Cell 7:321–331
Morello L, Frattini M, Giani S, Christou P, Breviario D (2000) Overexpression of the calcium-dependent protein kinase OsCDPK2 in transgenic rice is repressed by light in leaves and disrupts seed development. Transgenic Res 9:453–462
Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314
Murillo I, Jaeck E, Cordero MJ, San Segundo B (2001) Transcriptional activation of a maize calcium-dependent protein kinase gene in response to fungal elicitors and infection. Plant Mol Biol 45:145–158
Ohono S (1970) Evolution by gene duplication. Springer, Heidelberg
Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908
Patharkar OR, Cushman JC (2000) A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. Plant J 24:679–691
Raices M, Chico JM, Tellez-Inon MT, Ulloa RM (2001) Molecular characterization of StCDPK1, a calcium-dependent protein kinase from Solanum tuberosum that is induced at the onset of tuber development. Plant Mol Biol 46:591–601
Raices M, Gargantini PR, Chinchilla D, Crespi M, Tellez-Inon MT, Ulloa RM (2003) Regulation of CDPK isoforms during tuber development. Plant Mol Biol 52:1011–1024
Reddy AS (2001) Calcium: silver bullet in signalling. Plant Sci 160:381–404
Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556–5567
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 23:319–327
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–417
Schadt EE, Li C, Ellis B, Wong WH (2001) Feature extraction and normalization algorithms for high-density oligonucleotide gene expression array data. J Cell Biochem 37(Suppl):120–125
Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900–1902
Singh G, Kumar S, Singh P (2003) A quick method to isolate RNA from wheat and other carbohydrate-rich seeds. Plant Mol Biol Rep 21:93a–93f
Snedden WA, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant resposes to the environment. Trends Plant Sci 3:299–304
Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66
Szczegielniak J, Klimecka M, Liwosz A, Ciesielski A, Kaczanowski S, Dobrowolska G, Harmon AC, Muszynska G (2005) A wound-responsive and phospholipid-regulated maize calcium-dependent protein kinase. Plant Physiol 139:1970–1983
Takaiwa F, Oono K, Kato A (1991) Analysis of the 5′ flanking region responsible for the endosperm-specific expression of a rice glutelin chimeric gene in transgenic tobacco. Plant Mol Biol 16:49–58
The Rice Chromosomes 11, 12 Sequencing Consortia (2005) The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol 3:20
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 25:4876–4882
Trewavas AJ, Malho R (1998) Ca2+ signalling in plant cells: the big network! Curr Opin Plant Biol 1:428–433
Ullanat R, Jayabaskaran C (2002) Distinct light, cytokinin and tissue specific regulation of calcium dependent protein kinase gene expression in cucumber (Cucumis sativus). Plant Sci 162:153–163
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 244:331–340
Vij S, Tyagi AK (2007) Emerging trends in the functional genomics of the abiotic stress response in crop plants. Plant Biotechnol J 5:361–380
Wan B, Lin Y, Mou T (2007) Expression of rice Ca(2+)-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581:1179–1189
Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205
Wu Z, Irazzary RA, Gentleman R, Murillo FM, Spencer F (2004) A model based background adjustment for oligonucleotide expression arrays. Johns Hopkins University, Dept. of Biostatistics Working Papers. Working Paper 1
Xing T, Wang XJ, Malik K, Miki BL (2001) Ectopic expression of an Arabidopsis calmodulin-like domain protein kinase-enhanced NADPH oxidase activity and oxidative burst in tomato protoplasts. Mol Plant Microbe Interact 14:1261–1264
Yamaguchi-Shinozaki K, Shinozaki K (1993) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101:1119–1120
Yang G, Sheen S, Yans S, Komatsu S (2003) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced in response to cold and gibberellin. Plant Physiol Biochem 41:369–374
Yoon GM, Cho HS, Ha HJ, Liu JR, Lee HS (1999) Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol Biol 39:991–1001
Yoon GM, Dowd PE, Gilroy S, McCubbin AG (2006) Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18:867–878
Zhang M, Liang S, Lu YT (2005) Cloning and functional characterization of NtCPK4, a new tobacco calcium-dependent protein kinase. Biochim Biophys Acta 1729:174–185
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SR and RA acknowledge the award of Research Fellowship from the Council for Scientific and Industrial Research, New Delhi and PA acknowledges the award of Research Fellowship from University Grants Commission, New Delhi. This research work was supported financially by the Department of Biotechnology, Government of India. We gratefully acknowledge the IRGSP, KOME and TIGR, database resources for availability of detailed sequence information on rice.
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Communicated by J.-K. Zhu.
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Ray, S., Agarwal, P., Arora, R. et al. 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, 493–505 (2007). https://doi.org/10.1007/s00438-007-0267-4
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DOI: https://doi.org/10.1007/s00438-007-0267-4