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The epidermis both drives and restricts plant shoot growth

Abstract

The size of an organism is genetically determined, yet how a plant or animal achieves its final size is largely unknown. The shoot of higher plants has a simple conserved body plan based on three major tissue systems: the epidermal (L1), sub-epidermal (L2) and inner ground and vascular (L3) tissues. Which tissue system drives or restricts growth has been a subject of debate for over a century1,2,3,4. Here, we use dwarf, brassinosteroid biosynthesis and brassinosteroid response mutants in conjunction with tissue-specific expression of these components as tools to examine the role of the epidermis in shoot growth. We show that expression of the brassinosteroid receptor or a brassinosteroid biosynthetic enzyme in the epidermis, but not in the vasculature, of null mutants is sufficient to rescue their dwarf phenotypes. Brassinosteroid signalling from the epidermis is not sufficient to establish normal vascular organization. Moreover, shoot growth is restricted when brassinosteroids are depleted from the epidermis and brassinosteroids act locally within a leaf. We conclude that the epidermis both promotes and restricts shoot growth by providing a non-autonomous signal to the ground tissues.

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Figure 1: Brassinosteroid biosynthesis and perception in the epidermis is sufficient to rescue dwarfism.
Figure 2: Brassinosteroid signalling from the epidermis restores the number of vascular bundles but not their radial organization.
Figure 3: Brassinosteroids act locally and make a small contribution to growth from the inner layers.
Figure 4: The stabilized form of BES1 or BZR1 can mediate growth responses from the epidermis in bri1.

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References

  1. Peters, W. S. & Tomos, D. The epidermis still in control? Bot. Acta 109, 264–267 (1996)

    Article  Google Scholar 

  2. Kutschera, U. Stem elongation and cell wall proteins in flowering plants. Plant Biol. 3, 466–480 (2001)

    Article  CAS  Google Scholar 

  3. Green, P. B. Connecting gene and hormone action to form, pattern and organogenesis: biophysical transductions. J. Exp. Bot. 45, 1775–1788 (1994)

    Article  CAS  Google Scholar 

  4. Dale, J. E. The control of leaf expansion. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 267–295 (1988)

    Article  Google Scholar 

  5. Tsukaya, H. Mechanism of leaf-shape determination. Annu. Rev. Plant Biol. 57, 477–496 (2006)

    Article  CAS  Google Scholar 

  6. Gendreau, E. et al. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295–305 (1997)

    Article  CAS  Google Scholar 

  7. Szekeres, M. et al. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85, 171–182 (1996)

    Article  CAS  Google Scholar 

  8. Nakamura, A. et al. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 140, 580–590 (2006)

    Article  CAS  Google Scholar 

  9. Nakaya, M., Tsukaya, H., Murakami, N. & Kato, M. Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol. 43, 239–244 (2002)

    Article  CAS  Google Scholar 

  10. Vert, G., Nemhauser, J. L., Geldner, N., Hong, F. & Chory, J. Molecular mechanisms of steroid hormone signaling in plants. Annu. Rev. Cell Dev. Biol. 21, 177–201 (2005)

    Article  CAS  Google Scholar 

  11. Fujioka, S. & Yokota, T. Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137–164 (2003)

    Article  CAS  Google Scholar 

  12. Sessions, A., Weigel, D. & Yanofsky, M. F. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20, 259–263 (1999)

    Article  CAS  Google Scholar 

  13. Choe, S. et al. The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11, 207–221 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Cano-Delgado, A. et al. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341–5351 (2004)

    Article  CAS  Google Scholar 

  15. Turner, S. & Sieburth, L. E. Vascular Patterning. In The Arabidopsis Book (eds Somerville, C. R. & Meyerowitz, E. M.) (Am. Soc. Plant Biol., Rockville, Maryland, 2003)

    Google Scholar 

  16. Turk, E. M. et al. CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol. 133, 1643–1653 (2003)

    Article  CAS  Google Scholar 

  17. Neff, M. M. et al. BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc. Natl Acad. Sci. USA 96, 15316–15323 (1999)

    Article  ADS  CAS  Google Scholar 

  18. Symons, G. M. & Reid, J. B. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 2196–2206 (2004)

    Article  CAS  Google Scholar 

  19. Bishop, G. J., Harrison, K. & Jones, J. D. The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell 8, 959–969 (1996)

    Article  CAS  Google Scholar 

  20. Baima, S. et al. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121, 4171–4182 (1995)

    CAS  PubMed  Google Scholar 

  21. Kurata, T., Okada, K. & Wada, T. Intercellular movement of transcription factors. Curr. Opin. Plant Biol. 8, 600–605 (2005)

    Article  CAS  Google Scholar 

  22. Gallagher, K. L. & Benfey, P. N. Not just another hole in the wall: understanding intercellular protein trafficking. Genes Dev. 19, 189–195 (2005)

    Article  CAS  Google Scholar 

  23. Yin, Y. et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181–191 (2002)

    Article  CAS  Google Scholar 

  24. Wang, Z. Y. et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505–513 (2002)

    Article  CAS  Google Scholar 

  25. Pien, S., Wyrzykowska, J., McQueen-Mason, S., Smart, C. & Fleming, A. Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc. Natl Acad. Sci. USA 98, 11812–11817 (2001)

    Article  ADS  CAS  Google Scholar 

  26. 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 

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Acknowledgements

We thank Y. Belkhadir, M. Chen, N. Geldner and X. Wu for many thoughtful discussions and critical comments on the manuscript. We thank P. Sawchenko, LNSF, for access to microtomy, S. Mora-Garcia for help at the initial stage of the project and T. Gabi, S. Kim, E. Ballon-Landa, C. Butterfield and Z. Smith for technical assistance. This work was supported by grants from the National Science Foundation and the USDA to J.C. and by The Salk Institute and a Vaadia-BARD Postdoctoral Fellowship from BARD, The United States–Israel Binational Agricultural Research and Development Fund to S.S.-G. J.C. is an investigator of the Howard Hughes Medical Institute.

Author Contributions S.S.-G. and J.C. conceived and designed the experiments. S.S.-G. performed the experiments. C.P. performed plant anatomical sections. S.S.-G. and J.C. analysed the data and wrote the paper.

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Correspondence to Joanne Chory.

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Savaldi-Goldstein, S., Peto, C. & Chory, J. The epidermis both drives and restricts plant shoot growth. Nature 446, 199–202 (2007). https://doi.org/10.1038/nature05618

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