Abstract
Rice (Oryza sativa L.) as a model and crop plant with a sequenced genome offers an outstanding experimental system for discovering and functionally analyzing the major cell cycle control elements in a cereal species. In this study, we identified the core cell cycle genes in the rice genome through a hidden Markov model search and multiple alignments supported with the use of short protein sequence probes. In total we present 55 rice putative cell cycle genes with locus identity, chromosomal location, approximate chromosome position and EST accession number. These cell cycle genes include nine cyclin dependent-kinase (CDK) genes, 27 cyclin genes, one CKS gene, two RBR genes, nine E2F/DP/DEL genes, six KRP genes, and one WEE gene. We also provide characteristic protein sequence signatures encoded by CDK and cyclin gene variants. Promoter analysis by the FootPrinter program discovered several motifs in the regulatory region of the core cell cycle genes. As a first step towards functional characterization we performed transcript analysis by RT-PCR to determine gene specific variation in transcript levels along the rice leaves. The meristematic zone of the leaves where cells are actively dividing was identified based on kinematic analysis and flow cytometry. As expected, expression of the majority of cell cycle genes was exclusively associated with the meristematic region. However genes such as different D-type cyclins, DEL1, KRP1/3, and RBR2 were also expressed in leaf segments representing the transition zone in which cells start differentiation.
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Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster GTS, Inzé D (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 17(22):64–78
Barrôco RM, De Veylder L, Magyar Z, Engler G, Inzé D, Mironov V (2003) Novel complexes of cyclin-dependent kinases and a cyclin-like protein from Arabidopsis thaliana with a function unrelated to cell division. Cell Mol Life Sci 60:401–412
Barrôco RM, Peres A, Droual A-M, Nguyen LSL, De Wolf J, De Veylder L, Mironov V, Peerbolte R, Beemster GTS, Inzé D, Broekaert WF, Frankard V (2006) The cyclin-dependent kinase inhibitor Orysa;KRP1 plays an important role in rice seed development. Plant Physiol 142:1053–1064
Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116(4):1515–1526
Beemster GTS, Masle J, Williamson RE, Farquhar GD (1996) Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L.): kinematic analysis of leaf elongation. J Exp Bot 47:1663–1678
Beemster GTS, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inzé D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:734–743
Ben-Haj-Salah H, Tardieu F (1995) Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length. Analysis of the coordination between cell division and cell expansion. Plant Physiol 109:861–870
Berckmans B, Lammens T, Van Den Daele H, Magyar Z, Bögre L, De Veylder L (2011) Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol 157:1440–1451
Bisova K, Krylov DM, Umen JG (2005) Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol 137:475–491
Blanchette M, Tompa M (2003) FootPrinter: a program designed for phylogenetic footprinting. Nucleic Acids Res 31:3840–3842
Calingacion M, Laborte A, Nelson A, Resurreccion A, Concepcion JC (2014) Diversity of global rice markets and the science required for consumer-targeted rice breeding. PLoS One 9:e85106
Cobrinik D (2005) Pocket proteins and cell cycle control. Oncogene 24:2796–2809
Colasanti J, Tyers M, Sundaresan V (1991) Isolation and characterization of cDNA clones encoding a functional homologue from Zea mays. Proc Natl Acad Sci USA 88:3377–3381
Cooper B, Hutchison D, Park S, Guimil S, Luginbuhl P, Ellero C, Goff SA, Glazebrook J (2003) Identification of rice (Oryza sativa) proteins linked to the cyclin-mediated regulation of the cell cycle. Plant Mol Biol 53:273–279
Cross FR, Umen JG (2015) The chlamydomonas cell cycle. Plant J 82:370–392
Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R, Zamioudis C, Miskolczi P, Nieuwland J, Benjamins R, Dhonukshe P, Caballero-Pérez J, Horvath B, Long Y, Mähönen AP, Zhang H, Xu J, Murray JA, Benfey PN, Bako L, Marée AF, Scheres B (2012) A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:1002–1015
Dante RA, Larkins BA, Sabelli PA (2014) Cell cycle control and seed development. Front Plant Sci 5:493
De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668
del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14:3057–3071
Desvoyes B, Fernández-Marcos M, Sequeira-Mendes J, Otero S, Vergara Z, Gutierrez C (2014) Looking at plant cell cycle from the chromatin window. Front Plant Sci 5:369
Dewitte W, Murray JA (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264
Dudits D, Cserháti M, Miskolczi P, Horvath VG (2007) The growing family of plant cyclin-dependent kinases with multiple functions in cellular and developmental regulation. In: Inze D (ed) Cell cycle control and plant development. Blackwell Publishing, Oxford, pp 1–30
Dudits D, Abrahám E, Miskolczi P, Ayaydin F, Bilgin M, Horváth GV (2011) Cell-cycle control as a target for calcium, hormonal and developmental signals: the role of phosphorylation in the retinoblastoma-centred pathway. Ann Botany 107:1193–1202
Endo M, Nakayama S, Umeda-Hara C, Ohtsuki N, Saika H, Umeda M, Toki S (2012) CDKB2 is involved in mitosis and DNA damage response in rice. Plant J 69:967–977
Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611
Ferrario S, Immink RG, Angenent GC (2004) Conservation and diversity in flower land. Curr Opin Plant Biol 7:84–91
Ferreira PC, Hemerly AS, Villarroel R, Van Montagu M, Inzé D (1991) The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3:531–540
Fiorani F, Beemster GTS (2006) Quantitative analyses of cell division in plants. Plant Mol Biol 60:963–979
Francis D (2011) A commentary on the G2/M transition of the plant cell cycle. Ann Bot 107:1065–1070
Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T (2010) Rice expression atlas in reproductive development. Plant Cell Physiol 51:2060–2081
Fülöp K, Pettkó-Szandtner A, Magyar Z, Miskolczi P, Kondorosi É, Dudits D, Bakó L (2005) The Medicago CDKC;1-CYCLINT;1 kinase complex phosphorylates the carboxy-terminal domain of RNA polymerase II and promotes transcription. Plant J 42:810–820
Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340
Granier C, Inzé D, Tardieu F (2000) Spatial distribution of cell division rate can be deduced from that of p34cdc2 kinase activity in maize leaves grown at contrasting temperatures and soil water conditions. Plant Physiol 124:1393–1402
Guo J, Song J, Wang F, Zhang XS (2007) Genome-wide identification and expression analysis of rice cell cycle genes. Plant Mol Biol 64:349–360
Gutierrez C (2005) Coupling cell proliferation and development in plants. Nat Cell Biol 7:535–541
Higo K, Ugawa Y, Iwamoto M, Korenaga Y (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Hirt H, Páy A, Györgyey J, Bakó L, Németh K, Bögre L, Schweyen RJ, Heberle-Bors E, Dudits D (1991) Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologous to p34cdc2. Proc Natl Acad Sci USA 88:1636–1640
Hu X, Cheng X, Jiang H, Zhu S, Cheng B, Xiang Y (2010) Genome-wide analysis of cyclins in maize (Zea mays). Genet Mol Res 9:1490–1503
Huang X, Lu T, Han B (2013) Resequencing rice genomes: an emerging new era of rice genomics. Trends Genet 29:225–232
Inagaki S, Umeda M (2011) Cell-cycle control and plant development. Int Rev Cell Mol Biol 291:227–261
International Rice Genome Sequencing Project (IRGSP) (2005) The map-based sequence of the rice genome. Nature 426:793–800
Inzé D (2005) Green light for the cell cycle. EMBO J 24:657–662
Joubès J, Chevalier C, Dudits D, Heberle-Bors E, Inzé D, Umeda M, Renaudin JP (2000) CDK-related protein kinases in plants. Plant Mol Biol 43:607–620
Kalve S, De Vos D, Beemster GT (2014) Leaf development: a cellular perspective. Front Plant Sci 5:362
Keller B, Feuillet C (2000) Colinearity and gene density in grass genomes. Trends Plant Sci 5:246–251
Komaki S, Sugimoto K (2012) Control of the plant cell cycle by developmental and environmental cues. Plant Cell Physiol 53:953–964
Kono A, Umeda-Hara C, Lee J, Ito M, Uchimiya H, Umeda M (2003) Arabidopsis D-type cyclin CYCD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinase. Plant Physiol 132:1315–1321
Koroleva OA, Tomlinson M, Parinyapong P, Sakvarelidze L, Leader D, Shaw P, Doonan JH (2004) CycD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16:2364–2379
Kosugi S, Ohashi Y (2002) E2F sites that can interact with E2F proteins cloned from rice are required for meristematic tissue-specific expression of rice and tobacco proliferating cell nuclear antigen promoters. Plant J 29:45–59
Kuwabara A, Gruissem W (2014) Arabidopsis RETINOBLASTOMA-RELATED and Polycomb group proteins: cooperation during plant cell differentiation and development. J Exp Bot 65:2667–2676
La H, Li J, Ji Z, Cheng Y, Li X, Jiang S, Venkatesh PN, Ramachandran S (2006) Genome-wide analysis of cyclin family in rice (Oryza Sativa L.). Mol Genet Genomics 275:374–386
Lendvai Á, Pettkó-Szandtner A, Csordás-Tóth É, Miskolczi P, Horváth GV, Györgyey J, Dudits D (2007) Dicot and monocot plants differ in retinoblastoma-related protein subfamilies. J Exp Bot 58:1663–1675
Lin S, Carpenter EJ (1999) A PSTTLRE-form of cdc2-like gene in the marine microalga Dunaliella tertiolecta. Gene 239:39–48
Ling HQ, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90
Lu Z, Huang X, Ouyang Y, Yao J (2013) Genome-wide identification, phylogenetic and co-expression analysis of OsSET gene family in rice. PLoS One 8:e65426
Magyar Z, Mészaros T, Miskolczi P, Deák M, Fehér A, Brown S, Kondorosi E, Athanasiadis A, Pongor S, Bilgin M, Bakó L, Koncz C, Dudits D (1997) Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. Plant Cell 9:223–235
Meguro A, Sato Y (2014) Salicylic acid antagonizes abscisic acid inhibition of shoot growth and cell cycle progression in rice. Sci Rep 4(4555):1–11
Menges M, Murray JA (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J 30:203–212
Menges M, Hennig L, Gruissem W, Murray JA (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53:423–442
Menges M, de Jager SM, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566
Mészáros T, Miskolczi P, Ayaydin F, Pettkó-Szandtner A, Peres A, Magyar Z, Horváth GV, Bakó L, Fehér A, Dudits D (2000) Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Plant Mol Biol 43:595–605
Mizutani M, Naganuma T, Tsutsumi K, Saitoh Y (2010) The syncytium-specificexpression of the Orysa;KRP3 CDK inhibitor: implication of its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm. J Exp Bot 61:791–798
Nelissen H, Rymen B, Jikumaru Y, Demuynck K, Lijsebettens MV, Kamiya Y, Inzé D, Beemster GTS (2012) A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division Curr Biol 22:1183–1187
Ozawa K (2009) Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). Plant Sci 176:522–527
Pettkó-Szandtner A, Mészáros T, Horváth VG, Bakó L, Csordás-Tóth É, Blastyák A, Zhiponova M, Miskolczi P, Dudits D (2006) Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Plant J 46:111–123
Polyn S, Willems A, De Veylder L (2015) Cell cycle entry, maintenance, and exit during plant development. Curr Opin Plant Biol 23C:1–7
Porceddu A, Stals H, Reichheld JP, Segers G, De Veylder L, Barrôco RP, Casteels P, Van Montagu M, Inzé D, Mironov V (2001) A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plants. J Biol Chem 276:36354–36360
Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66
Robbens S, Khadaroo B, Camasses A, Derelle E, Ferraz C, Inzé D, Van de Peer Y, Moreau H (2005) Genome-wide analysis of core cell cycle genes in the unicellular green alga Ostreococcus tauri. Mol Biol Evol 22:589–597
Rutledge RG, Côté C (2003) Mathematics of quantitative kinetic PCR and the application of standard curves. Nucleic Acids Res 31:e93
Rymen B, Fiorani F, Kartal F, Vandepoele K, Inzé D, Beemster GTS (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143:1429–1438
Rymen B, Coppens F, Dhondt S, Fiorani F, Beemster GTS (2010) Kinematic analysis of cell division and expansion. Methods Mol Biol 655:203–227
Sabelli PA, Dante RA, Leiva-Neto JT, Jung R, Gordon-Kamm WJ, Larkins BA (2005) RBR3, a member of the retinoblastoma-related family from maize, is regulated by the RBR1/E2F pathway. Proc Natl Acad Sci USA 102:13005–13012
Sabelli PA, Liu Y, Dante RA, Lizarraga LE, Nguyen HN, Brown SW, Klingler JP, Yu J, LaBrant E, Layton TM, Feldman M, Larkins BA (2013) Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endosperm. Proc Natl Acad Sci USA 110:E1827–E1836
Schnittger A, Schobinger U, Bouyer D, Weinl C, Stierhof YD, Hulskamp M (2002) Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc Natl Acad Sci USA 99:6410–6415
Schnittger A, Weinl C, Bouyer D, Schobinger U, Hulskamp M (2003) Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 15:303–315
Schnyder HS, Seo S, Rademacher IF, Kühbauch W (1990) Spatial distribution of growth rates and of epidermal cell lengths in the elongation zone during leaf development in Lolium perenne L. Planta 181:423–431
Sun Y, Dilkes BP, Zhang C, Dante RA, Carneiro NP, Lowe KS, Jung R, Gordon-Kamm WJ, Larkins BA (1999) Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc Natl Acad Sci USA 96:4180–4185
Tardieu F, Reymond M, Hamard P, Granier C, Muller B (2000) Spatial distributions of expansion rate, cell division rate and cell size in maize leaves: a synthesis of the effects of soil water status, evaporative demand and temperature. J Exp Bot 51:1505–1514
Torres Acosta JA, Fowke LC, Wang H (2011) Analyses of phylogeny, evolution, conserved sequences and genome-wide expression of the ICK/KRP family of plant CDK inhibitors. Ann Bot 107:1141–1157
Umeda M, Umeda-Hara C, Yamaguchi M, Hashimoto J, Uchimiya H (1999a) Differential expression of genes for cyclin-dependent protein kinases in rice plants. Plant Physiol 119:31–40
Umeda M, Iwamoto N, Umeda-Hara C, Yamaguchi M, Hashimoto J, Uchimiya H (1999b) Molecular characterization of mitotic cyclins in rice plants. Mol Gen Genet 262:230–238
Umeda M, Shimotohno A, Yamaguchi M (2005) Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants. Plant Cell Physiol 46:1437–1442
Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916
Vandepoele K, Simillion C, Van de Peer Y (2003) Evidence that rice and other cereals are ancient aneuploids. Plant Cell 15:2192–2202
Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster GT, Gruissem W, Van de Peer Y, Inzé D, De Veylder L (2005) Genome-wide identification of potential plant E2F target genes. Plant Physiol 139:316–328
Verkest A, Weinl C, Inzé D, De Veylder L, Schnittger A (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol 139:1099–1106
Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis CW, Ma H (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135:1084–1099
Xu Y, McCouch SR, Zhang Q (2005) How can we use genomics to improve cereals with rice as a reference genome? Plant Mol Biol 59:7–26
Yamaguchi M, Fabian T, Sauter M, Bhalerao RP, Schrader J, Sandberg G, Umeda M, Uchimiya H (2000) Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants. Plant J 24:11–20
Yang R, Tang Q, Wang H, Zhang X, Pan G, Wang H, Tu J (2011) Analyses of two rice (Oryza sativa) cyclin-dependent kinase inhibitors and effects of transgenic expression of OsiICK6 on plant growth and development. Ann Botany 107:1087–1101
Zhang T, Wang X, Lu Y, Cai X, Ye Z, Zhang J (2013) Genome-wide analysis of the cyclin gene family in tomato. Int J Mol Sci 15:120–140
Zhiponova MK, Pettkó-Szandtner A, Stelkovics É, Neer Z, Bottka S, Krenács T, Fehér A, Dudits D, Szilák L (2006) Mitosis-specific promoter of the alfalfa cyclin-dependent kinase gene (Medsa;CDKB2;1) is activated by wounding, and ethylene, in a non-cell division dependent manner. Plant Physiol 2:693–703
Acknowledgments
The authors would like to thank Wim Van Caeneghem for skillful advice with real-time PCR analysis, Klaas Vandepoele for assistance in the annotation process of the rice cell cycle genes, Yves van de Peer and the members of the Bioinformatics group for providing appropriate infrastructure for the annotation process. This work was partly supported by a grant from the Institute for the Promotion of Innovation by Science and Technology in Flanders (postdoctoral fellowship to R.M.B.), A.P-Sz was supported by OTKA-68896 and the János Bolyai Research Scholarship of the Hungarian Academy of Sciences.
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A. Pettkó-Szandtner, M. Cserháti and R. M. Barrôco have contributed equally to this work.
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Pettkó-Szandtner, A., Cserháti, M., Barrôco, R.M. et al. Core cell cycle regulatory genes in rice and their expression profiles across the growth zone of the leaf. J Plant Res 128, 953–974 (2015). https://doi.org/10.1007/s10265-015-0754-3
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DOI: https://doi.org/10.1007/s10265-015-0754-3