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:

The expression domain of PHANTASTICA determines leaflet placement in compound leaves

An Erratum to this article was published on 04 September 2003

Abstract

Diverse leaf forms in nature can be categorized as simple or compound. Simple leaves, such as those of petunia, have a single unit of blade, whereas compound leaves, such as those of tomato, have several units of blades called leaflets. Compound leaves can be pinnate, with leaflets arranged in succession on a rachis, or palmate, with leaflets clustered together at the leaf tip. The mechanisms that generate these various leaf forms are largely unknown. The upper (adaxial) surface is usually different from the bottom (abaxial) surface in both simple and compound leaves. In species with simple leaves, the specification of adaxial and abaxial cells is important for formation of the leaf blade1,2, and the MYB transcription factor gene PHANTASTICA (PHAN) is involved in maintaining the leaf adaxial (upper) domain3,4. Here we show that downregulation of PHAN is sufficient to reduce the adaxial domain of leaf primordia and to change pinnate compound leaves into palmate compound leaves. Furthermore, this mechanism seems to be shared among compound leaves that arose independently.

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

Access options

Buy this article

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

Figure 1: Leaf morphology.
Figure 2: Adaxial domain in compound leaves from various plant species.
Figure 3: PHAN and compound leaf development.
Figure 4: Compound leaf development in pinnate, peltately palmate and non-peltately palmate leaves.

Similar content being viewed by others

References

  1. McConnell, J. R. et al. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411, 709–713 (2001)

    Article  ADS  CAS  PubMed Central  Google Scholar 

  2. Waites, R. & Hudson, A. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121, 2143–2154 (1995)

    CAS  Google Scholar 

  3. Sun, Y., Zhou, Q., Zhang, W., Fu, Y. & Huang, H. ASYMMETRIC LEAVES1, an Arabidopsis gene that is involved in the control of cell differentiation in leaves. Planta 214, 694–702 (2002)

    Article  CAS  Google Scholar 

  4. Waites, R., Selvadurai, H. R. N., Oliver, I. R. & Hudson, A. The Phantastica gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93, 779–789 (1998)

    Article  CAS  Google Scholar 

  5. Pien, S., Wyrzykowska, J. & Fleming, A. J. Novel marker genes for early leaf development indicate spatial regulation of carbohydrate metabolism within the apical meristem. Plant J. 25, 663–674 (2001)

    Article  CAS  Google Scholar 

  6. Koltai, H. & Bird, D. M. Epistatic repression of PHANTASTICA and class 1 KNOTTED genes is uncoupled in tomato. Plant J. 22, 455–459 (2000)

    Article  CAS  Google Scholar 

  7. Bharathan, G. et al. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296, 1858–1860 (2002)

    Article  ADS  CAS  Google Scholar 

  8. Gleissberg, S. & Kadereit, J. W. Evolution of leaf morphogenesis: evidence from developmental and phylogenetic data in Papaveraceae. Int. J. Plant Sci. 160, 787–794 (1999)

    Article  Google Scholar 

  9. Averof, M. & Patel, N. H. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388, 682–686 (1997)

    Article  ADS  CAS  PubMed Central  Google Scholar 

  10. Carroll, S. B. Endless forms: the evolution of gene regulation and morphological diversity. Cell 101, 577–580 (2000)

    Article  CAS  Google Scholar 

  11. Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999)

    Article  ADS  CAS  Google Scholar 

  12. Gellon, G. & McGinnis, W. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20, 116–125 (1998)

    Article  CAS  Google Scholar 

  13. Byrne, M. E. et al. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967–971 (2000)

    Article  ADS  CAS  Google Scholar 

  14. Timmermans, M. C. P., Hudson, A., Becraft, P. W. & Nelson, T. Rough sheath2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284, 151–153 (1999)

    Article  ADS  CAS  Google Scholar 

  15. Tsiantis, M., Schneeberger, R., Golz, J. F., Freeling, M. & Langdale, J. A. The maize roughsheath2 gene and leaf development programs in monocot and dicot plants. Science 284, 154–156 (1999)

    Article  ADS  CAS  Google Scholar 

  16. McCormick, S. in Plant Tissue Culture Manual, Fundamentals and Applications, Vol. B6 (ed. Lindsey, K.) 1–9 (Kluwer, Dordrecht, 1991)

    Google Scholar 

  17. Ruiz-Medrano, R., Xoconostle-Cazares, B. & Lucas, W. J. Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126, 4405–4419 (1999)

    CAS  PubMed  Google Scholar 

  18. Jackson, D., Veit, B. & Hake, S. Expression of maize KNOTTED 1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 405–413 (1994)

    CAS  Google Scholar 

  19. Kessler, S., Kim, M., Pham, T., Weber, N. & Sinha, N. Mutations altering leaf morphology in tomato. Int. J. Plant Sci. 162, 475–492 (2001)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Harada, T. Kellogg, B. Reinhart and members of the Sinha lab for comments on the manuscript; T. Metcalf and E. Sandoval for plant materials; and E. Dean and the UC Davis John Tucker herbarium. This work was supported by Jastro Shields and Elsie Stocking fellowships to M.K., and by awards from the NSF to N.R.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Neelima Sinha.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, M., McCormick, S., Timmermans, M. et al. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424, 438–443 (2003). https://doi.org/10.1038/nature01820

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01820

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