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

Nature Genetics volume 40, pages 1136–1141 (2008)Cite this article

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.

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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.

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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.

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Authors and Affiliations

  1. Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK

    Michalis Barkoulas, Angela Hay, Evagelia Kougioumoutzi & Miltos Tsiantis

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  1. Michalis Barkoulas
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  2. Angela Hay
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  3. Evagelia Kougioumoutzi
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  4. Miltos Tsiantis
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Contributions

M.B. performed the majority of the experiments and contributed to experimental design and writing. A.H. produced the cSTM≫GUS 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.

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Correspondence to Miltos Tsiantis.

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

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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

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