The Role of the Arabidopsis E2FB Transcription Factor in Regulating Auxin-Dependent Cell Divisionw⃞

The molecular mechanisms by which the phytohormone auxin coordinates cell division with cell growth and differentiation are largely unknown. Here, we show that in Arabidopsis thaliana E2FB, accumulation and stability are positively regulated by auxin. Coexpression of E2FB, but not of E2FA, with its dimerization partner A, stimulated cell proliferation in the absence of auxin in tobacco (Nicotiana tabacum) Bright Yellow-2 cells. E2FB regulated the entry into both S- and M-phases, the latter corresponding to the activation of a plant-specific mitotic regulator, CDKB1;1. Increased E2FB levels led to shortened cell cycle duration, elevated cell numbers, and extremely small cell sizes. In the absence of auxin, cells elongated with concomitant increase in their ploidy level, but both were strongly inhibited by E2FB. We conclude that E2FB is one of the key targets for auxin to determine whether cells proliferate or whether they exit the cell cycle, enlarge, and endoreduplicate their DNA.

[1]  M. Estelle,et al.  The F-box protein TIR1 is an auxin receptor , 2005, Nature.

[2]  Ottoline Leyser,et al.  The Arabidopsis F-box protein TIR1 is an auxin receptor , 2005, Nature.

[3]  W. Kim,et al.  Retinoblastoma protein regulates cell proliferation, differentiation, and endoreduplication in plants. , 2005, The Plant journal : for cell and molecular biology.

[4]  Peter Nick,et al.  Auxin-Dependent Cell Division and Cell Elongation. 1-Naphthaleneacetic Acid and 2,4-Dichlorophenoxyacetic Acid Activate Different Pathways1 , 2005, Plant Physiology.

[5]  D. Inzé,et al.  The Plant-Specific Cyclin-Dependent Kinase CDKB1;1 and Transcription Factor E2Fa-DPa Control the Balance of Mitotically Dividing and Endoreduplicating Cells in Arabidopsis , 2004, The Plant Cell Online.

[6]  W. Gerald,et al.  Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control , 2004, Nature.

[7]  W. Gruissem,et al.  Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte , 2004, Nature.

[8]  R. Bhalerao,et al.  Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen. , 2004, The Plant journal : for cell and molecular biology.

[9]  B. Edgar,et al.  Negative Regulation of dE2F1 by Cyclin-Dependent Kinases Controls Cell Cycle Timing , 2004, Cell.

[10]  T. Mészáros,et al.  A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis , 2004, The EMBO journal.

[11]  Dirk Inzé,et al.  Plant cell cycle transitions. , 2003, Current opinion in plant biology.

[12]  Keith Roberts,et al.  "Big it up": endoreduplication and cell-size control in plants. , 2003, Current opinion in plant biology.

[13]  M. Bennett,et al.  The case for morphogens in plants , 2003, Nature Cell Biology.

[14]  B. Blasius,et al.  Auxin Transport Synchronizes the Pattern of Cell Division in a Tobacco Cell Line1 , 2003, Plant Physiology.

[15]  S. Kosugi,et al.  Constitutive E2F Expression in Tobacco Plants Exhibits Altered Cell Cycle Control and Morphological Change in a Cell Type-Specific Manner , 2003, Plant Physiology.

[16]  Balázs Melikant,et al.  A plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2-phase and alleviates the DNA-damage checkpoint , 2003, Journal of Cell Science.

[17]  H. Tsukaya.  Organ shape and size: a lesson from studies of leaf morphogenesis. , 2003, Current opinion in plant biology.

[18]  J. Murray,et al.  Altered Cell Cycle Distribution, Hyperplasia, and Inhibited Differentiation in Arabidopsis Caused by the D-Type Cyclin CYCD3 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004838. , 2003, The Plant Cell Online.

[19]  C. Gutiérrez,et al.  Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. , 2002, The Plant Cell.

[20]  W. Shen.  The plant E2F-Rb pathway and epigenetic control. , 2002, Trends in plant science.

[21]  H. Nakagami,et al.  Phosphorylation of Retinoblastoma-Related Protein by the Cyclin D/Cyclin-Dependent Kinase Complex Is Activated at the G1/S-Phase Transition in Tobacco Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.0025 , 2002, The Plant Cell Online.

[22]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[23]  J. Bryant,et al.  Endoreduplication is not inhibited but induced by aphidicolin in cultured cells of tobacco. , 2002, Journal of experimental botany.

[24]  M. Menges,et al.  Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. , 2002, The Plant journal : for cell and molecular biology.

[25]  C. Bergounioux,et al.  The E2F Family of Transcription Factors from Arabidopsis thaliana , 2002, The Journal of Biological Chemistry.

[26]  D. Inzé,et al.  Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa–DPa transcription factor , 2002, The EMBO journal.

[27]  S. Kosugi,et al.  Interaction of the Arabidopsis E2F and DP Proteins Confers Their Concomitant Nuclear Translocation and Transactivation , 2002, Plant Physiology.

[28]  G. Sandberg,et al.  The role of auxin-binding protein 1 in the expansion of tobacco leaf cells. , 2002, The Plant journal : for cell and molecular biology.

[29]  D. Inzé,et al.  A bright future for the bright yellow-2 cell culture. , 2001, Plant physiology.

[30]  Y. Mizukami,et al.  A matter of size: developmental control of organ size in plants. , 2001, Current opinion in plant biology.

[31]  R. Spang,et al.  Role for E2F in Control of Both DNA Replication and Mitotic Functions as Revealed from DNA Microarray Analysis , 2001, Molecular and Cellular Biology.

[32]  U. Goodenough,et al.  Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. , 2001, Genes & development.

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

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

[35]  M. Sussman,et al.  ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. , 2001, Genes & development.

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

[37]  E. A. Deakin,et al.  The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation , 2000, Plant Molecular Biology.

[38]  R. Huntley,et al.  The plant cell cycle. , 1999, Current opinion in plant biology.

[39]  T. P. Neufeld,et al.  Coordination of Growth and Cell Division in the Drosophila Wing , 1998, Cell.

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

[41]  D. Inzé,et al.  Levels of endogenous cytokinins, indole‐3‐acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY‐2 cells , 1996, FEBS letters.

[42]  J. Nevins,et al.  Expression of transcription factor E2F1 induces quiescent cells to enter S phase , 1993, Nature.

[43]  G. An,et al.  High efficiency transformation of cultured tobacco cells. , 1985, Plant physiology.

[44]  J. Torrey.  Plant Cell Biology , 1969, Nature.

[45]  A. Murphy,et al.  Auxin transport. , 2005, Current opinion in plant biology.

[46]  A. Steinmetz,et al.  The Tobacco A-Type Cyclin , Nicta ; CYCA 3 ; 2 , at the Nexus of Cell Division and Differentiation , 2003 .

[47]  Jeffrey M. Trimarchi,et al.  Transcription: Sibling rivalry in the E2F family , 2002, Nature Reviews Molecular Cell Biology.

[48]  S. D. de Jager,et al.  © 2001 Kluwer Academic Publishers. Printed in the Netherlands. , 2000 .

[49]  J. Zuo,et al.  Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. , 2000, The Plant journal : for cell and molecular biology.

[50]  T. Nagata,et al.  Plant cell biology through the window of the highly synchronized tobacco BY-2 cell line. , 1999, Methods in cell science : an official journal of the Society for In Vitro Biology.