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.

A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta

Abstract

The developmental basis for the generation of divergent leaf forms is largely unknown. Here we investigate this problem by studying processes that distinguish development of two related species: Arabidopsis thaliana, which has simple leaves, and Cardamine hirsuta, which has dissected leaves with individual leaflets. Using genetics, expression studies and cell lineage tracing, we show that lateral leaflet formation in C. hirsuta requires the establishment of growth foci that form after leaf initiation. These growth foci are recruited at the leaf margin in response to activity maxima of auxin, a hormone that polarizes growth in diverse developmental contexts. Class I KNOTTED1-like homeobox (KNOX) proteins also promote leaflet initiation in C. hirsuta, and here we provide evidence that this action of KNOX proteins is contingent on the ability to organize auxin maxima via the PINFORMED1 (PIN1) auxin efflux transporter. Thus, differential deployment of a fundamental mechanism polarizing cellular growth contributed to the diversification of leaf form during evolution.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: C. hirsuta PIN1 activity is required for leaf and leaflet formation.
Figure 2: PIN1-directed auxin activity maxima underpin leaflet formation.
Figure 3: Localized cell division underpins leaflet outgrowth in C. hirsuta.
Figure 4: KNOX-mediated leaf dissection requires C. hirsuta PIN1-directed auxin activity gradients.

References

  1. Gleissberg, S. Comparative Developmental and Molecular Genetic Aspects of Leaf Dissection (Taylor and Francis, New York, 2002).

    Book  Google Scholar 

  2. Hay, A. & Tsiantis, M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 38, 942–947 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Okada, K., Ueda, J., Komaki, M.K., Bell, C.J. & Shimura, Y. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677–684 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Galweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).

    Article  CAS  PubMed  Google Scholar 

  5. Heisler, M.G. et al. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15, 1899–1911 (2005).

    Article  CAS  PubMed  Google Scholar 

  6. Scarpella, E., Marcos, D., Friml, J. & Berleth, T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 20, 1015–1027 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Long, J.A., Moan, E.I., Medford, J.I. & Barton, M.K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69 (1996).

    Article  CAS  PubMed  Google Scholar 

  9. Hay, A., Barkoulas, M. & Tsiantis, M. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133, 3955–3961 (2006).

    Article  CAS  PubMed  Google Scholar 

  10. Chuck, G., Lincoln, C. & Hake, S. KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8, 1277–1289 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Langlade, N.B. et al. Evolution through genetically controlled allometry space. Proc. Natl. Acad. Sci. USA 102, 10221–10226 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Felix, M.A. Cryptic quantitative evolution of the vulva intercellular signaling network in Caenorhabditis. Curr. Biol. 17, 103–114 (2007).

    Article  CAS  PubMed  Google Scholar 

  13. McGregor, A.P. et al. Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448, 587–590 (2007).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  15. Hofer, J., Gourlay, C., Michael, A. & Ellis, T.H. Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol. Biol. 45, 387–398 (2001).

    Article  CAS  PubMed  Google Scholar 

  16. Kim, M., McCormick, S., Timmermans, M. & Sinha, N. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424, 438–443 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. DeMason, D.A. & Chawla, R. Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218, 435–448 (2004).

    Article  CAS  PubMed  Google Scholar 

  18. Wang, H. et al. The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17, 2676–2692 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tissier, A.F. et al. Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics. Plant Cell 11, 1841–1852 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Levy, A.A. & Walbot, V. Regulation of the timing of transposable element excision during maize development. Science 248, 1534–1537 (1990).

    Article  CAS  PubMed  Google Scholar 

  21. Poethig, R.S. & Sussex, I.M. The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165, 170–184 (1985).

    Article  CAS  PubMed  Google Scholar 

  22. Poethig, R.S. Clonal analysis of cell lineage patterns in plant development. Am. J. Bot. 74, 581–594 (1987).

    Article  Google Scholar 

  23. Ori, N. et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 39, 787–791 (2007).

    Article  CAS  PubMed  Google Scholar 

  24. Fletcher, J.C., Brand, U., Running, M.P., Simon, R. & Meyerowitz, E.M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911–1914 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. Kenrick, P. & Crane, P.R. The Origin and Early Diversification of Land Plants: a Cladistic Study (Smithsonian Institution Press, London, 1997).

    Google Scholar 

  26. Arber, A. The Natural Philosophy of Plant Form (Cambridge Univ. Press, Cambridge, 1950).

    Google Scholar 

  27. 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  PubMed  Google Scholar 

  28. Moore, I., Galweiler, L., Grosskopf, D., Schell, J. & Palme, K. A transcription activation system for regulated gene expression in transgenic plants. Proc. Natl. Acad. Sci. USA 95, 376–381 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Eshed, Y., Baum, S.F., Perea, J.V. & Bowman, J.L. Establishment of polarity in lateral organs of plants. Curr. Biol. 11, 1251–1260 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Bowman, J.L., Smyth, D.R. & Meyerowitz, E.M. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1–20 (1991).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank S. Hake (Plant Gene Expression Center, University of California Berkeley), M.G. Heisler, E.M. Meyerowitz (California Institute of Technology), R. Swarup, M. Bennett (University of Nottingham), J. Friml (Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), Ghent) and J. Jones (John Innes Centre, Norwich) for seed stocks and reagents. We also thank A. Hudson and J. Langdale for comments on the manuscript, I. Moore for assistance with confocal microscopy, R. Mueller and R. Simon (Heinrich-Heine University, Duesseldorf) for sharing sequences to design CLV3 primers, S. Langer for technical assistance and J. Baker for photography. This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) and EU NEST idea project NEST 120878. M.T. is a recipient of an EMBO Young Investigator Award and a Royal Society Wolfson Merit award, A.H. is a recipient of a Royal Society University Research Fellowship and a Junior Research Fellowship at Balliol College, and M.B. of a Bodossakis foundation award. We also acknowledge the support of the Gatsby Charitable foundation.

Author information

Authors and Affiliations

Authors

Contributions

M.B. performed the majority of the experiments and contributed to experimental design and writing. A.H. produced the cSTMGUS lines and contributed Figures 2c,m,n and 3a. E.K. contributed Figure 4g. M.T. and A.H. wrote the manuscript. M.T. designed and directed the study.

Corresponding author

Correspondence to Miltos Tsiantis.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7, Supplementary Table 1 (PDF 1127 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Barkoulas, M., Hay, A., Kougioumoutzi, E. et al. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40, 1136–1141 (2008). https://doi.org/10.1038/ng.189

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.189

This article is cited by

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