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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.

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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.

References

  1. 1

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

    CAS  Article  Google Scholar 

  2. 2

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

    CAS  ADS  Article  Google Scholar 

  3. 3

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

    CAS  Article  Google Scholar 

  4. 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. 5

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

    CAS  ADS  Article  Google Scholar 

  6. 6

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

    CAS  ADS  Article  Google Scholar 

  7. 7

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

    CAS  ADS  Article  Google Scholar 

  8. 8

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

    CAS  Article  Google Scholar 

  9. 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)

    CAS  Article  Google Scholar 

  10. 10

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

    CAS  ADS  Article  Google Scholar 

  11. 11

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

    CAS  ADS  Article  Google Scholar 

  12. 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)

    CAS  Article  Google Scholar 

  13. 13

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

    CAS  Article  Google Scholar 

  14. 14

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

    CAS  Article  Google Scholar 

  15. 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)

    CAS  Article  Google Scholar 

  16. 16

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

    CAS  Article  Google Scholar 

  17. 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. 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)

    CAS  Article  Google Scholar 

  19. 19

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

    CAS  Article  Google Scholar 

  20. 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)

    CAS  Article  Google Scholar 

  21. 21

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

    CAS  Article  Google Scholar 

  22. 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)

    CAS  Article  Google Scholar 

  23. 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. 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)

    CAS  Article  Google Scholar 

  25. 25

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

    CAS  Article  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.

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Correspondence to Ben Scheres.

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The authors declare no competing financial interests.

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

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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

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