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:

PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development

Abstract

Factors with a graded distribution can program fields of cells in a dose-dependent manner1,2, but no evidence has hitherto surfaced for such mechanisms in plants. In the Arabidopsis thaliana root, two PLETHORA (PLT) genes encoding AP2-domain transcription factors have been shown to maintain the activity of stem cells3. Here we show that a clade of four PLT homologues is necessary for root formation. Promoter activity and protein fusions of PLT homologues display gradient distributions with maxima in the stem cell area. PLT activities are largely additive and dosage dependent. High levels of PLT activity promote stem cell identity and maintenance; lower levels promote mitotic activity of stem cell daughters; and further reduction in levels is required for cell differentiation. Our findings indicate that PLT protein dosage is translated into distinct cellular responses.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Four PLT genes promote root formation.
Figure 2: PLT promoter activity and PLT protein fusions display gradients.
Figure 3: PLT expression regulates stem cell maintenance and meristem boundary.
Figure 4: Inducible expansion of meristem and stem cell area with PLT2–GR fusions.

Similar content being viewed by others

References

  1. Tabata, T. & Takei, Y. Morphogens, their identification and regulation. Development 131, 703–712 (2004)

    Article  CAS  Google Scholar 

  2. Gurdon, J. B. & Bourillot, P. Y. Morphogen gradient interpretation. Nature 413, 797–803 (2001)

    Article  CAS  ADS  Google Scholar 

  3. Aida, M. et al. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120 (2004)

    Article  CAS  Google Scholar 

  4. Skoog, F. & Miller, C. O. Chemical regulation of growth and organ formation in plant tissues cultured in vitro . Symp. Soc. Exp. Biol. 54, 118–130 (1957)

    Google Scholar 

  5. Weigel, D. & Jurgens, G. Stem cells that make stems. Nature 415, 751–754 (2002)

    Article  CAS  ADS  Google Scholar 

  6. Spradling, A., Drummond-Barbosa, D. & Kai, T. Stem cells find their niche. Nature 414, 98–104 (2001)

    Article  CAS  ADS  Google Scholar 

  7. Xu, J. et al. A molecular framework for plant regeneration. Science 311, 385–388 (2006)

    Article  CAS  ADS  Google Scholar 

  8. Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999)

    Article  CAS  Google Scholar 

  9. Nole-Wilson, S., Tranby, T. L. & Krizek, B. A. AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol. Biol. 57, 613–628 (2005)

    Article  CAS  Google Scholar 

  10. Birnbaum, K. et al. A gene expression map of the Arabidopsis root. Science 302, 1956–1960 (2003)

    Article  CAS  ADS  Google Scholar 

  11. Blilou, I. et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44 (2005)

    Article  CAS  ADS  Google Scholar 

  12. Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411 (1998)

    Article  CAS  Google Scholar 

  13. Hellmann, H. et al. Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J. 22, 3314–3325 (2003)

    Article  CAS  Google Scholar 

  14. Dharmasiri, N. et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109–119 (2005)

    Article  CAS  Google Scholar 

  15. Srinivasan, C. et al. Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta 225, 341–351 (2007)

    Article  CAS  Google Scholar 

  16. Wildwater, M. et al. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337–1349 (2005)

    Article  CAS  Google Scholar 

  17. Grieneisen, V. A., Xu, J., Marée, A. F. M., Hogeweg, P. & Scheres, B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature doi:10.1038/nature06215 (this issue).

  18. O'Connor, M. B., Umulis, D., Othmer, H. G. & Blair, S. S. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133, 183–193 (2006)

    Article  CAS  Google Scholar 

  19. Jaeger, J. & Reinitz, J. On the dynamic nature of positional information. Bioessays 28, 1102–1111 (2006)

    Article  CAS  Google Scholar 

  20. Hellens, R. P., Edwards, E. A., Leyland, N. R., Bean, S. & Mullineaux, P. M. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819–832 (2000)

    Article  CAS  Google Scholar 

  21. Aoyama, T. & Chua, N. H. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605–612 (1997)

    Article  CAS  Google Scholar 

  22. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998)

    Article  CAS  Google Scholar 

  23. Willemsen, V., Wolkenfelt, H., deVries, G., Weisbeek, P. & Scheres, B. The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125, 521–531 (1998)

    CAS  PubMed  Google Scholar 

  24. Bougourd, S., Marrison, J. & Haseloff, J. Technical advance: an aniline blue staining procedure for confocal microscopy and 3D imaging of normal and perturbed cellular phenotypes in mature Arabidopsis embryos. Plant J. 24, 543–550 (2000)

    Article  CAS  Google Scholar 

  25. Friml, J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis . Cell 108, 661–673 (2002)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Netherlands Genomics Initiative (M.L.) and the Portuguese Foundation for Science and Technology (C.G.) for funding, A. Shimotohno and J. M. Perez-Perez for sharing data and Frits Kindt for photography.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ben Scheres.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-9 with Legends and Supplementary Tables 1-3. (PDF 6235 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Galinha, C., Hofhuis, H., Luijten, M. et al. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053–1057 (2007). https://doi.org/10.1038/nature06206

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06206

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

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