Genome-Wide Analysis of Core Cell Cycle Genes in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010445.

Cyclin-dependent kinases and cyclins regulate with the help of different interacting proteins the progression through the eukaryotic cell cycle. A high-quality, homology-based annotation protocol was applied to determine the core cell cycle genes in the recently completed Arabidopsis genome sequence. In total, 61 genes were identified belonging to seven selected families of cell cycle regulators, for which 30 are new or corrections of the existing annotation. A new class of putative cell cycle regulators was found that probably are competitors of E2F/DP transcription factors, which mediate the G1-to-S progression. In addition, the existing nomenclature for cell cycle genes of Arabidopsis was updated, and the physical positions of all genes were compared with segmentally duplicated blocks in the genome, showing that 22 core cell cycle genes emerged through block duplications. This genome-wide analysis illustrates the complexity of the plant cell cycle machinery and provides a tool for elucidating the function of new family members in the future.

[1]  S. Pongor,et al.  Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. , 1997, The Plant Cell.

[2]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[3]  Ramana V. Davuluri,et al.  Evaluation of gene prediction software using a genomic data set: application to <$O_SSF>Arabidopsis thaliana<$C_SSF>sequences , 1999, Bioinform..

[4]  J. M. González,et al.  A fluorimetric method for the estimation of G+C mol% content in microorganisms by thermal denaturation temperature. , 2002, Environmental microbiology.

[5]  M. Hirano,et al.  Cloning and functional expression of a degradation-resistant novel isoform of p 27 Kip 1 , 2022 .

[6]  M. Menges,et al.  Cell cycle regulation of cyclin-dependent kinases in tobacco cultivar Bright Yellow-2 cells. , 2001, Plant physiology.

[7]  R. Müller,et al.  Cyclin ET, a new splice variant of human cyclin E with a unique expression pattern during cell cycle progression and differentiation. , 1997, Nucleic acids research.

[8]  Yves Van de Peer,et al.  TREECON: a software package for the construction and drawing of evolutionary trees , 1993, Comput. Appl. Biosci..

[9]  M. Milla,et al.  DP-2, a heterodimeric partner of E2F: identification and characterization of DP-2 proteins expressed in vivo. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D. Inzé,et al.  CDK-related protein kinases in plants , 2000, Plant Molecular Biology.

[11]  H. Schaller,et al.  Alternative splicing in the regulatory region of the human phosphatases CDC25A and CDC25C. , 2000, European journal of cell biology.

[12]  D. Inzé,et al.  The Arabidopsis Cks1At protein binds the cyclin‐dependent kinases Cdc2aAt and Cdc2bAt , 1997, FEBS letters.

[13]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[14]  Donna J. Freeman,et al.  Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization , 1996, Plant Molecular Biology.

[15]  Axel Meyer,et al.  Dealing with saturation at the amino acid level: a case study based on anciently duplicated zebrafish genes. , 2002, Gene.

[16]  P. John,et al.  Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like H1 histone kinase , 2004, Planta.

[17]  M. Umeda,et al.  A rice homolog of Cdk7/MO15 phosphorylates both cyclin-dependent protein kinases and the carboxy-terminal domain of RNA polymerase II. , 1998, The Plant journal : for cell and molecular biology.

[18]  K. Keyomarsi,et al.  Novel splice variants of cyclin E with altered substrate specificity. , 2000, Nucleic acids research.

[19]  Thomas Schiex,et al.  EUGÈNE: An Eukaryotic Gene Finder That Combines Several Sources of Evidence , 2000, JOBIM.

[20]  S Henikoff,et al.  Performance evaluation of amino acid substitution matrices , 1993, Proteins.

[21]  M. Mancini,et al.  The Cdk9 and cyclin T subunits of TAK/P-TEFb localize to splicing factor-rich nuclear speckle regions. , 2001, Journal of cell science.

[22]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[23]  K. Helin,et al.  DcE2F, a Functional Plant E2F-like Transcriptional Activator from Daucus carota * , 2000, The Journal of Biological Chemistry.

[24]  P. Raymond,et al.  A new C-type cyclin-dependent kinase from tomato expressed in dividing tissues does not interact with mitotic and G1 cyclins. , 2001, Plant physiology.

[25]  N. Grotz,et al.  An enhancer trap line associated with a D-class cyclin gene in Arabidopsis. , 2000, Plant physiology.

[26]  J. Murray,et al.  A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. , 1995, The Plant cell.

[27]  D. Inzé,et al.  A Plant-specific Cyclin-dependent Kinase Is Involved in the Control of G2/M Progression in Plants* , 2001, The Journal of Biological Chemistry.

[28]  Masaki Ito,et al.  Isolation and characterization of the E2F‐like gene in plants , 1999, FEBS letters.

[29]  J. T. Madison,et al.  Alternative splicing of cyclin transcripts in maize endosperm. , 1997, Gene.

[30]  D. Inzé,et al.  Identification of novel cyclin-dependent kinases interacting with the CKS1 protein of Arabidopsis. , 2001, Journal of experimental botany.

[31]  D. G. Brown,et al.  The origins of genomic duplications in Arabidopsis. , 2000, Science.

[32]  D. Inzé,et al.  A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation , 1999, Planta.

[33]  D. Inzé,et al.  Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. , 1995, The EMBO journal.

[34]  B. Larkins,et al.  Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  S. Hata cDNA cloning of a novel cdc2+/CDC28‐related protein kinase from rice , 1991, FEBS letters.

[36]  R. Bhalerao,et al.  A distinct cyclin-dependent kinase-activating kinase of Arabidopsis thaliana. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  V. Brendel,et al.  Prediction of locally optimal splice sites in plant pre-mRNA with applications to gene identification in Arabidopsis thaliana genomic DNA. , 1998, Nucleic acids research.

[38]  Anders Gorm Pedersen,et al.  Neural Network Prediction of Translation Initiation Sites in Eukaryotes: Perspectives for EST and Genome Analysis , 1997, ISMB.

[39]  A. Sali,et al.  Homology-based annotation yields 1,042 new candidate genes in the Drosophila melanogaster genome , 2001, Nature Genetics.

[40]  P. Rouzé,et al.  Genome annotation: which tools do we have for it? , 1999, Current opinion in plant biology.

[41]  Sean R. Eddy,et al.  Profile hidden Markov models , 1998, Bioinform..

[42]  Richard Hughey,et al.  Hidden Markov models for detecting remote protein homologies , 1998, Bioinform..

[43]  M. Delseny,et al.  Extensive Duplication and Reshuffling in the Arabidopsis Genome , 2000, Plant Cell.

[44]  M. Kreis,et al.  Identification of cdc2cAt: a new cyclin-dependent kinase expressed in Arabidopsis thaliana flowers. , 1999, Biochimica et biophysica acta.

[45]  D. Inzé,et al.  When plant cells decide to divide. , 2001, Trends in plant science.

[46]  P. O’Farrell,et al.  E2F-induced S phase requires cyclin E. , 1996, Genes & development.

[47]  D T Jones,et al.  Protein secondary structure prediction based on position-specific scoring matrices. , 1999, Journal of molecular biology.

[48]  M. Borodovsky,et al.  GeneMark.hmm: new solutions for gene finding. , 1998, Nucleic acids research.

[49]  Franky R. G. Terras,et al.  Functional Analysis of Cyclin-Dependent Kinase Inhibitors of Arabidopsis , 2001, The Plant Cell Online.

[50]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[51]  Jeroen Raes,et al.  ForCon : a software tool for the conversion of sequence alignments , 1999 .

[52]  D. Inzé,et al.  Characterization of two distinct DP‐related genes from Arabidopsis thaliana 1 , 2000, FEBS letters.

[53]  S Brunak,et al.  A branch point consensus from Arabidopsis found by non-circular analysis allows for better prediction of acceptor sites. , 1997, Nucleic acids research.

[54]  A. Valencia,et al.  Intrinsic errors in genome annotation. , 2001, Trends in genetics : TIG.

[55]  A. Hughes,et al.  Gene duplication and the structure of eukaryotic genomes. , 2001, Genome research.

[56]  Kim Rutherford,et al.  Artemis: sequence visualization and annotation , 2000, Bioinform..

[57]  E. Fraenkel,et al.  Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP. , 1999, Genes & development.

[58]  C. W. Lee,et al.  Nuclear accumulation of the E2F heterodimer regulated by subunit composition and alternative splicing of a nuclear localization signal. , 1996, Journal of cell science.

[59]  C. Gutiérrez,et al.  The cloning of plant E2F, a retinoblastoma-binding protein, reveals unique and conserved features with animal G(1)/S regulators. , 1999, Nucleic acids research.

[60]  Yves Van de Peer,et al.  TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment , 1994, Comput. Appl. Biosci..