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The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins

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Abstract

Recent discoveries of plant retinoblastoma (Rb) protein homologues and D-type cyclins suggest that control of the onset of cell division in plants may have stronger parallels with mammalian G1/S controls than with yeasts. In mammals, the Rb protein interacts specifically with D-type cyclins and regulates cell proliferation by binding and inhibiting E2F transcription factors. However, the developmental role of Rb in plants and its potential interaction with cell cycle regulators is unknown. We show that the maize Rb homologue ZmRb-1 is temporally and spatially regulated during maize leaf development. ZmRb-1 is highly expressed in differentiating cells, but almost undetectable in proliferating cells. In vitro, both ZmRb-1 and human Rb bind all classes of plant D-type cyclins with the involvement of a conserved N-terminal Leu-x-Cys-x-Glu (LxCxE) Rb-interaction motif. This binding is strongly reduced by mutation of the conserved Cys-470 of ZmRb-1. ZmRb-1 binds human and Drosophila E2F, and inhibits transcriptional activation of human E2F. We also show that ZmRb-1 is a good in vitro substrate for all human G1/S protein kinases. The functional conservation of proteins that control the G1/S transition in mammals and plants points to the existence of plant E2F homologues. We conclude that evolution of Rb and cyclin D proteins occurred after separation of the fungi from the higher eukaryotic lineage, but preceded the divergence of plant and animal kingdoms.

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Author notes

  1. Donna Freeman & Judith Greenwood

    Present address: Peptide Therapeutics Ltd, 321 Cambridge Science Park, Milton Road, Cambridge, CB4 4WG, UK

  2. Joe Makker

    Present address: Joint Diseases Laboratory, McGill University, Shriners Hospital for Children, 1529 Cedar Avenue, Montreal, Quebec, Canada, H3G 1A6

  3. Edward Walker

    Present address: MRC Laboratory of Molecular Biology, Hills Road, Cambridge, CB2 2QH, UK

Authors and Affiliations

  1. Institute of Biotechnology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QT, UK

    Rachael Huntley, Sandra Healy, Donna Freeman, Sarah de Jager, Judith Greenwood, Joe Makker, Edward Walker & James A.H. Murray

  2. Wellcome/CRC Institute, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QR, UK

    Paul Lavender, Mark Jackman, Andrew J. Bannister & Tony Kouzarides

  3. Centro de Biología Molecular ‘Severo Ochoa’ (CSIC-UAM), Universidad Autónoma, Cantoblanco, 28049, Madrid, Spain

    Qi Xie & Crisanto Gutiérrez

  4. Department of Cell Biology, John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK; present addresses

    John H. Doonan

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  1. Rachael Huntley
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Huntley, R., Healy, S., Freeman, D. et al. The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol Biol 37, 155–169 (1998). https://doi.org/10.1023/A:1005902226256

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