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PMID: 15208425 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins.

Plant physiology ·Vol. 135 ·No. 2 ·2004-06-00 ·Pages 1084-99

Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis CW, Ma H

Abstract

Cyclins are primary regulators of the activity of cyclin-dependent kinases, which are known to play critical roles in controlling eukaryotic cell cycle progression. While there has been extensive research on cell cycle mechanisms and cyclin function in animals and yeasts, only a small number of plant cyclins have been characterized functionally. In this paper, we describe an exhaustive search for cyclin genes in the Arabidopsis genome and among available sequences from other vascular plants. Based on phylogenetic analysis, we define 10 classes of plant cyclins, four of which are plant-specific, and a fifth is shared between plants and protists but not animals. Microarray and reverse transcriptase-polymerase chain reaction analyses further provide expression profiles of cyclin genes in different tissues of wild-type Arabidopsis plants. Comparative phylogenetic studies of 174 plant cyclins were also performed. The phylogenetic results imply that the cyclin gene family in plants has experienced more gene duplication events than in animals. Expression patterns and phylogenetic analyses of Arabidopsis cyclin genes suggest potential gene redundancy among members belonging to the same group. We discuss possible divergence and conservation of some plant cyclins. Our study provides an opportunity to rapidly assess the position of plant cyclin genes in terms of evolution and classification, serving as a guide for further functional study of plant cyclins.

MeSH Terms
Arabidopsis/genetics Arabidopsis Proteins/genetics,metabolism Cyclin B/genetics,metabolism Cyclins/genetics,metabolism Gene Expression Profiling/methods Gene Expression Regulation, Plant Genome, Plant Multigene Family Phylogeny
Chemicals
Arabidopsis Proteins CycB1 protein, Arabidopsis Cyclin B Cyclins D-type cyclin CDCD4.1, Arabidopsis cyc1bAt protein, Arabidopsis
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Wang Guanfang
Department of Biology and the Huck Institutes of Life Sciences, Pennsylvania State University, University Park, Pennsylvania 16802, USA.
Kong Hongzhi
Sun Yujin
Zhang Xiaohong
Zhang Wei
Altman Naomi
DePamphilis Claude W
Ma Hong
References (66)
66 references, click to expand
  1. Cell cycle controls: genome-wide analysis in Arabidopsis.
    Curr Opin Plant Biol. 2001 Dec;4(6):501-6 PMID: 11641065
  2. Mitosis in plants: how far we have come at the molecular level?
    Curr Opin Plant Biol. 2002 Dec;5(6):487-93 PMID: 12393010
  3. Cyclin G1 and cyclin G2 comprise a new family of cyclins with contrasting tissue-specific and cell cycle-regulated expression.
    J Biol Chem. 1996 Mar 15;271(11):6050-61 PMID: 8626390
  4. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division.
    Cell. 1983 Jun;33(2):389-96 PMID: 6134587
  5. Analysis of cell division parameters and cell cycle gene expression during the cultivation of Arabidopsis thaliana cell suspensions.
    J Exp Bot. 2001 Aug;52(361):1625-33 PMID: 11479327
  6. Cip/Kip cyclin-dependent kinase inhibitors: brakes of the cell cycle engine during development.
    Bioessays. 1998 Dec;20(12):1020-9 PMID: 10048302
  7. Model scenarios for evolution of the eukaryotic cell cycle.
    Philos Trans R Soc Lond B Biol Sci. 1998 Dec 29;353(1378):2063-76 PMID: 10098216
  8. Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes.
    Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6410-5 PMID: 11983922
  9. Cell cycle controls and the development of plant form.
    Curr Opin Plant Biol. 2001 Feb;4(1):44-9 PMID: 11163167
  10. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
    Science. 2002 Apr 5;296(5565):92-100 PMID: 11935018
  11. Cyclins and cyclin-dependent kinases: a biochemical view.
    Biochem J. 1995 Jun 15;308 ( Pt 3):697-711 PMID: 8948422
  12. "Cross-talk" between cell division cycle and development in plants.
    Plant Cell. 2002 Jan;14(1):11-6 PMID: 11826295
  13. The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13603-10 PMID: 10570119
  14. The role and regulation of D-type cyclins in the plant cell cycle.
    Plant Mol Biol. 2000 Aug;43(5-6):621-33 PMID: 11089865
  15. Cell cycle control in fission yeast and mammals: identification of new regulatory mechanisms.
    Adv Cancer Res. 1996;69:17-62 PMID: 8791678
  16. A novel and highly divergent Arabidopsis cyclin isolated by complementation in budding yeast.
    Biochim Biophys Acta. 2001 May 28;1539(1-2):1-6 PMID: 11389963
  17. Genome-wide analysis of core cell cycle genes in Arabidopsis.
    Plant Cell. 2002 Apr;14(4):903-16 PMID: 11971144
  18. Cyclin specificity: how many wheels do you need on a unicycle?
    J Cell Sci. 2001 May;114(Pt 10):1811-20 PMID: 11329367
  19. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias.
    Bioinformatics. 2003 Jan 22;19(2):185-93 PMID: 12538238
  20. Isolation and characterization of cDNA clones for plant cyclins.
    EMBO J. 1991 Sep;10(9):2681-8 PMID: 1831125
  21. Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells.
    Plant Mol Biol. 2000 Aug;43(5-6):595-605 PMID: 11089863
  22. Amino acid substitution matrices from protein blocks.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10915-9 PMID: 1438297
  23. Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization.
    Plant Mol Biol. 1996 Dec;32(6):1003-18 PMID: 9002599
  24. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).
    Science. 2002 Apr 5;296(5565):79-92 PMID: 11935017
  25. Cyclin/Cdk complexes: their involvement in cell cycle progression and mitotic division.
    Protoplasma. 2001;216(3-4):119-42 PMID: 11732181
  26. Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1.
    Cell. 1996 Mar 22;84(6):863-74 PMID: 8601310
  27. Cyclin F is degraded during G2-M by mechanisms fundamentally different from other cyclins.
    J Biol Chem. 2002 Sep 20;277(38):35140-9 PMID: 12122006
  28. A- and B-type cyclins differentially modulate substrate specificity of cyclin-cdk complexes.
    EMBO J. 1993 May;12(5):1947-54 PMID: 8491188
  29. Regulation of cell division in plants: an Arabidopsis perspective.
    Prog Cell Cycle Res. 1997;3:29-41 PMID: 9552404
  30. Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants.
    Plant J. 2000 Oct;24(1):11-20 PMID: 11029700
  31. The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization.
    Cell. 1989 Aug 11;58(3):485-97 PMID: 2569363
  32. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis.
    Science. 1986 Oct 17;234(4774):364-8 PMID: 2876518
  33. Transcriptome analysis during cell division in plants.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14825-30 PMID: 12393816
  34. Cyclin is degraded by the ubiquitin pathway.
    Nature. 1991 Jan 10;349(6305):132-8 PMID: 1846030
  35. CDK-related protein kinases in plants.
    Plant Mol Biol. 2000 Aug;43(5-6):607-20 PMID: 11089864
  36. Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes.
    Curr Biol. 2002 Mar 5;12(5):415-20 PMID: 11882294
  37. The tobacco A-type cyclin, Nicta;CYCA3;2, at the nexus of cell division and differentiation.
    Plant Cell. 2003 Dec;15(12):2763-77 PMID: 14615597
  38. Whole-genome analysis of animal A- and B-type cyclins.
    Genome Biol. 2002;3(12):RESEARCH0070 PMID: 12537559
  39. Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein.
    Plant J. 1999 Nov;20(4):503-8 PMID: 10607302
  40. Developmental expression of the arabidopsis cyclin gene cyc1At.
    Plant Cell. 1994 Dec;6(12):1763-74 PMID: 7866022
  41. A survey of the molecular evolutionary dynamics of twenty-five multigene families from four grass taxa.
    J Mol Evol. 2001 Feb;52(2):144-56 PMID: 11231894
  42. SCF and APC: the Yin and Yang of cell cycle regulated proteolysis.
    Curr Opin Cell Biol. 1998 Dec;10(6):759-68 PMID: 9914180
  43. Cyclin D control of growth rate in plants.
    Nature. 2000 Jun 1;405(6786):575-9 PMID: 10850717
  44. Divide and conquer: cytokinesis in plant cells.
    Curr Opin Plant Biol. 1999 Dec;2(6):447-53 PMID: 10607656
  45. How proteolysis drives the cell cycle.
    Science. 1996 Dec 6;274(5293):1652-9 PMID: 8939846
  46. Targets of cyclin-dependent protein kinases.
    Curr Opin Cell Biol. 1993 Apr;5(2):187-93 PMID: 8507490
  47. The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana.
    Gene. 1994 Jun 10;143(2):211-6 PMID: 8206375
  48. Plant cell cycle transitions.
    Curr Opin Plant Biol. 2003 Dec;6(6):536-43 PMID: 14611951
  49. Kinetic analysis of a molecular model of the budding yeast cell cycle.
    Mol Biol Cell. 2000 Jan;11(1):369-91 PMID: 10637314
  50. Cyclin-dependent kinases and cell division in plants- the nexus
    Plant Cell. 1999 Apr;11(4):509-22 PMID: 10213774
  51. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  52. Cell cycle-regulated gene expression in Arabidopsis.
    J Biol Chem. 2002 Nov 1;277(44):41987-2002 PMID: 12169696
  53. PEST sequences and regulation by proteolysis.
    Trends Biochem Sci. 1996 Jul;21(7):267-71 PMID: 8755249
  54. Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein.
    EMBO J. 2002 Jun 17;21(12):3081-95 PMID: 12065421
  55. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  56. Organization of cortical microtubules in plant cells.
    Curr Opin Cell Biol. 1995 Feb;7(1):65-71 PMID: 7755991
  57. Insights into the G1/S transition in plants.
    Planta. 2002 Jul;215(3):345-56 PMID: 12111215
  58. At the heart of the budding yeast cell cycle.
    Trends Genet. 1996 Oct;12(10):405-12 PMID: 8909137
  59. Cyclin I: a new cyclin encoded by a gene isolated from human brain.
    Exp Cell Res. 1995 Dec;221(2):534-42 PMID: 7493655
  60. A gene expression map of the Arabidopsis root.
    Science. 2003 Dec 12;302(5652):1956-60 PMID: 14671301
  61. Factors controlling cyclin B expression.
    Plant Mol Biol. 2000 Aug;43(5-6):677-90 PMID: 11089869
  62. Principles of CDK regulation.
    Nature. 1995 Mar 9;374(6518):131-4 PMID: 7877684
  63. Developmental expression of the Arabidopsis thaliana CycA2;1 gene.
    Planta. 2000 Oct;211(5):623-31 PMID: 11089674
  64. 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. 2003 Feb;60(2):401-12 PMID: 12678503
  65. Conserved structural motifs in cyclins identified by sequence analysis.
    J Cell Sci. 1991 Jul;99 ( Pt 3):669-74 PMID: 1834684
  66. Plant A-type cyclins.
    Plant Mol Biol. 2000 Aug;43(5-6):659-75 PMID: 11089868
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2004-06-00
Pages
1084-99
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC514142
Subset
IM
Grants
NIGMS NIH HHS · R01 GM63871 · United States
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