Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Cyclin D control of growth rate in plants

Nature volume 405, pages 575–579 (2000)Cite this article

Abstract

The mechanisms by which plants modulate their growth rate in response to environmental and developmental conditions are unknown, but are presumed to involve specialized regions called meristems where cell division is concentrated1,2,3,4,5. The possible role of cell division in influencing meristem activity and overall plant growth rate is controversial, with a prevailing view that cell division is secondary to higher order meristem controls1,2,6,7. Here we show that a reduction in the length of the cell-cycle G1 phase and faster cell cycling occur when the rate of cell division in transgenic tobacco plants is increased by the plant D-type cyclin CycD2 (ref. 8). The plants have normal cell and meristem sizes, but elevated overall growth rates, an increased rate of leaf initiation and accelerated development in all stages from seedling to maturity. We conclude that cell division is a principal determinant of meristem activity and overall growth rate, and propose that modulation of plant growth rate is achieved through regulation of G1.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Expression, activity and interaction of CycD2;At in tobacco.
Figure 2: Phenotypic characterization of CycD2;At-expressing tobacco plants.
Figure 3: Leaf expansion and initiation in wild-type and CycD2;At-expressing transgenic plants.
Figure 4: Cell-cycle analysis in wild-type and CycD2;At-expressing transgenic meristems.

Similar content being viewed by others

References

  1. Lyndon, R. F. The Shoot Apical Meristem (Cambridge Univ. Press, Cambridge, 1998).

    Google Scholar 

  2. Clark, S. E. & Schiefelbein, J. W. Expanding insights into the role of cell proliferation in plant development. Trends Cell Biol. 7, 454–458 (1997).

    Article  CAS  Google Scholar 

  3. Kinsman, E. A. et al. Elevated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata. Plant Cell Envir. 20, 1309–1316 (1997).

    Article  Google Scholar 

  4. Francis, D. in Inherent Variation in Plant Growth (eds Lambers, H. & Van Vuuren, M. M. I.) 5–20 (Backhuys, Leiden, 1998).

    Google Scholar 

  5. Francis, D. & Barlow, P. W. Temperature and the cell cycle. Symp. Soc. Exp. Biol. 42, 181–201 (1988).

    CAS  PubMed  Google Scholar 

  6. Hagemann, W. The relationship of anatomy to morphology in plants: A new theoretical perspective. Int. J. Plant Sci. 153, 538–548 (1992).

    Article  ADS  Google Scholar 

  7. Barlow, P. W. in Shape and Form in Plants and Fungi (eds Ingram, D. S. & Hudson, A.) 169–193 (Academic, London, 1995)

    Google Scholar 

  8. Soni, R., Carmichael, J. P., Shah, Z. H. & Murray, J. A. H. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7, 85–103 (1995).

    Article  CAS  Google Scholar 

  9. Bayliss, M. W. in The Cell Division Cycle in Plants (eds Bryant, J. A. & Francis, D.) 157–177 (Cambridge Univ. Press, Cambridge, 1985).

    Google Scholar 

  10. Pines, J. Cyclins and cyclin-dependent kinases: Theme and variations. Adv. Cancer Res. 66, 181–212 (1995).

    Article  CAS  Google Scholar 

  11. Murray, J. A. H. et al. in Plant Cell Division (eds Francis, D., Dudits, D. & Inzé, D.) 99–127 (Portland, London, 1998).

    Google Scholar 

  12. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. & Murray, J. A. H. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541–1544 (1999).

    Article  ADS  CAS  Google Scholar 

  13. Setiady, Y. Y., Sekine, M., Hariguchi, N., Kouchi, H. & Shinmyo, A. Molecular cloning and characterization of a cDNA clone that encodes a cdc2 homolog from Nicotiana tabacum. Plant Cell Physiol. 37, 369–376 (1996).

    Article  CAS  Google Scholar 

  14. Mironov, V., De Veylder, L., Van Montagu, M. & Inzé, D. Cyclin-dependent kinases and cell division in plants—the nexus. Plant Cell 11, 509–521 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Lyndon, R. F. Rates of cell division in the shoot apical meristem of Pisum. Ann. Bot. 34, 1–17 (1970).

    Article  Google Scholar 

  16. Galli, M. G. & Sala, F. Aphidicolin as synchronizing agent in root tip meristems of Haplopappus gracilis. Plant Cell Rep. 2, 156–159 (1983).

    Article  CAS  Google Scholar 

  17. Francis, D., Davis, M. S., Braybrook, C., James, N. C. & Herbert, R. J. An effect of zinc on M-phase and G1 of the plant cell cycle in the synchronous TBY-2 tobacco cell suspension. J. Exp. Bot. 46, 1887–1894 (1995).

    Article  CAS  Google Scholar 

  18. Polymenis, M. & Schmidt, E. V. Coordination of cell growth with cell division. Curr. Opin. Genet. Dev. 9, 76–80 (1999).

    Article  CAS  Google Scholar 

  19. Gonthier, R., Jacqmard, A. & Bernier, G. Occurrence of two cell subpopulations with different cell-cycle durations in the central and peripheral zones of the vegetative shoot apex of Sinapis alba L. Planta 165, 288–291 (1985).

    Article  CAS  Google Scholar 

  20. Clowes, F. A. L. in: Cell Division in Higher Plants (ed. Yeoman, M. M.) 253–284 (Academic, London, 1976).

    Google Scholar 

  21. Gonthier, R., Jacqmard, A. & Bernier, G. Changes in cell-cycle duration and growth fraction in the shoot meristem of Sinapis during floral transition. Planta 170, 55–59 (1987).

    Article  CAS  Google Scholar 

  22. Evans, H. J., Neary, G. J. & Tonkinson, S. M. The use of colchicine as an indicator of mitotic rate in broad bean root meristems. J. Genet. 55, 487–502 (1957).

    Article  Google Scholar 

  23. Neufeld, T. P., de la Cruz, A. F. A., Johnston, L. A. & Edgar, B. A. Coordination of growth and cell division in the Drosophila wing. Cell 93, 1183–1193 (1998).

    Article  CAS  Google Scholar 

  24. Nash, R., Tokiwa, G., Anand, S., Erickson, K. & Futcher, A. B. The WHI1+ gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog. EMBO J. 7, 4335–4346 (1988).

    Article  CAS  Google Scholar 

  25. Quelle, D. E. et al. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7, 1559–1571 (1993).

    Article  CAS  Google Scholar 

  26. Resnitzky, D., Gossen, M., Bujard, H. & Reed, S. I. Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14, 1669–1679 (1994).

    Article  CAS  Google Scholar 

  27. Doerner, P., Jorgensen, J-E., You, R., Steppuhn, J. & Lamb, C. Control of root growth and development by cyclin expression. Nature 380, 520–523 (1996).

    Article  ADS  CAS  Google Scholar 

  28. Hemerly, A. et al. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 14, 3925–3936 (1995).

    Article  CAS  Google Scholar 

  29. Gleave, A. P. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203–1207 (1992).

    Article  CAS  Google Scholar 

  30. Riou-Khamlichi, C., Menges, M., Healy, J. M. S. & Murray, J. A. H. Sugar control of the plant cell cycle: Differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell. Biol. (in the press).

Download references

Acknowledgements

We thank M. Sekine for permission to cite unpublished data; I. Furner for making possible the glasshouse experiments; R. Day and A. Mills for expert plant care and measurements; A. Inskip for technical support, T. Burgess and the Multi-Imaging Centre for help with scanning electron micrographs; and M. Cornelissen and M. De Block for invaluable discussions. This work was supported in part by the UK Biotechnology and Biological Sciences Research Council.

Author information

Author notes

  1. J. M. Sandra Healy

    Present address: Dipartimento di Genetica, Università di Milano, IV Piano, Torre A, Via Celoria, 26, 20133, Milano, Italy

Authors and Affiliations

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

    Claire E. Cockcroft, Bart G. W. den Boer, J. M. Sandra Healy & James A. H. Murray

  2. Aventis CropScience N.V., Jozef Plateaustraat 22, Gent, B-9000, Belgium

    Bart G. W. den Boer

Authors
  1. Claire E. Cockcroft
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bart G. W. den Boer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. M. Sandra Healy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James A. H. Murray
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James A. H. Murray.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cockcroft, C., den Boer, B., Healy, J. et al. Cyclin D control of growth rate in plants. Nature 405, 575–579 (2000). https://doi.org/10.1038/35014621

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35014621

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing