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Independent recruitment of a conserved developmental mechanism during leaf evolution

Nature volume 434, pages 509–514 (2005)Cite this article

Abstract

Vascular plants evolved in the Middle to Late Silurian period, about 420 million years ago1. The fossil record indicates that these primitive plants had branched stems with sporangia but no leaves. Leaf-like lateral outgrowths subsequently evolved on at least two independent occasions2,3,4. In extant plants, these events are represented by microphyllous leaves in lycophytes (clubmosses, spikemosses and quillworts) and megaphyllous leaves in euphyllophytes (ferns, gymnosperms and angiosperms). Our current understanding of how leaves develop is restricted to processes that operate during megaphyll formation. Because microphylls and megaphylls evolved independently, different mechanisms might be required for leaf formation. Here we show that this is not so. Gene expression data from a microphyllous lycophyte, phylogenetic analyses, and a cross-species complementation experiment all show that a common developmental mechanism can underpin both microphyll and megaphyll formation. We propose that this mechanism might have operated originally in the context of primitive plant apices to facilitate bifurcation. Recruitment of this pathway to form leaves occurred independently and in parallel in different plant lineages.

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Figure 1: KNOX–ARP relationships in S. kraussiana.
Figure 2: KNOX–ARP relationships in O. regalis.
Figure 3: KNOX–ARP relationships across land plants.
Figure 4: Complementation of Arabidopsis as1-1 mutants by SkARP1.

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References

  1. Edwards, D., Feehan, J. & Smith, D. G. A late Wenlock flora from County Tipperary, Ireland. Bot. J. Linn. Soc. 86, 19–36 (1983)

    Article  Google Scholar 

  2. Gifford, E. M. & Foster, A. S. Morphology and Evolution of Vascular Plants (Freeman, New York, 1989)

    Google Scholar 

  3. Boyce, C. K. & Knoll, A. H. Evolution of developmental potential and the multiple independent origin of leaves in Paleozoic vascular plants. Paleobiology 28, 70–100 (2002)

    Article  Google Scholar 

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

    Google Scholar 

  5. Jackson, D., Veit, B. & Hake, S. Expression of maize Knotted1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 404–413 (1994)

    Google Scholar 

  6. Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K. & Hake, S. A. Knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6, 1859–1876 (1994)

    Article  CAS  Google Scholar 

  7. Nishimura, A., Tamaoki, M., Sato, Y. & Matsuoka, M. The expression of tobacco Knotted1-type class1 homeobox genes correspond to regions predicted by the cytohistological zonation model. Plant J. 18, 337–347 (1999)

    Article  CAS  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  ADS  CAS  Google Scholar 

  9. Sentoku, N. et al. Regional expression of the rice KN1-type homeobox gene family during embryo, shoot and flower development. Plant Cell 11, 1651–1663 (1999)

    Article  CAS  Google Scholar 

  10. Hofer, J. M., Gourlay, C. W., 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  Google Scholar 

  11. Hareven, D., Gutfinger, T., Parnis, A., Eshed, Y. & Lifschitz, E. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84, 735–744 (1996)

    Article  CAS  Google Scholar 

  12. Muller, J. et al. In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. Plant J. 27, 13–23 (2001)

    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. Schneeberger, R., Tsiantis, M., Freeling, M. & Langdale, J. A. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125, 2857–2865 (1998)

    CAS  PubMed  Google Scholar 

  15. Tsiantis, M., Schneeberger, R., Golz, J. F., Freeling, M. & Langdale, J. A. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284, 154–156 (1999)

    Article  ADS  CAS  Google Scholar 

  16. 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 

  17. Smith, L. G., Greene, B., Veit, B. & Hake, S. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116, 21–30 (1992)

    CAS  PubMed  Google Scholar 

  18. McHale, N. A. & Koning, R. E. PHANTASTICA regulates development of the adaxial mesophyll in Nicotiana leaves. Plant Cell 16, 1251–1262 (2004)

    Article  CAS  Google Scholar 

  19. Wikstrom, N., Savolainen, V. & Chase, M. W. Evolution of the angiosperms: calibrating the family tree. Proc. R. Soc. Lond. B 268, 2211–2220 (2001)

    Article  CAS  Google Scholar 

  20. Tsiantis, M. & Hay, A. Comparative plant development: the time of the leaf? Nature Rev. Genet. 4, 169–180 (2003)

    Article  CAS  Google Scholar 

  21. Steeves, T. A. & Sussex, I. M. Studies on the development of excised leaves in sterile culture. Am. J. Bot. 44, 665–673 (1957)

    Article  Google Scholar 

  22. Bierhorst, D. W. On the stem apex, leaf initiation and early leaf ontogeny in filicalean ferns. Am. J. Bot. 64, 125–152 (1977)

    Article  Google Scholar 

  23. 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 

  24. 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  ADS  CAS  Google Scholar 

  25. Kim, M. et al. Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 130, 4405–4415 (2003)

    Article  CAS  Google Scholar 

  26. Theodoris, G., Inada, N. & Freeling, M. Conservation and molecular dissection of ROUGH SHEATH2 and ASYMMETRIC LEAVES1 function in leaf development. Proc. Natl Acad. Sci. USA 100, 6837–6842 (2003)

    Article  ADS  CAS  Google Scholar 

  27. Pautot, V. et al. KNAT2: evidence for a link between Knotted-like genes and carpel development. Plant Cell 13, 1719–1734 (2001)

    Article  CAS  Google Scholar 

  28. Golz, J. F., Keck, E. J. & Hudson, A. Spontaneous mutations in KNOX genes give rise to a novel floral structure in antirrhinum. Curr. Biol. 12, 515–522 (2002)

    Article  CAS  Google Scholar 

  29. Parnis, A. et al. The dominant developmental mutants of tomato, Mouse-Ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9, 2143–2158 (1997)

    Article  CAS  Google Scholar 

  30. Janssen, B.-J., Lund, L. & Sinha, N. Overexpression of a homeobox gene LeT6 reveals indeterminate features in the tomato compound leaf. Plant Physiol. 117, 771–786 (1998)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Stork for technical help; C. Hammond and T. Gardner for help during their undergraduate degrees (funded by the Wellcome Trust and a Nuffield Bursary, respectively); M. Tsiantis and G. Theodoris for rs2 fusion constructs; M. Tsiantis and M. Knight for criticizing our manuscript; M. Tsiantis, D. Barker and the Oxford Systematics Discussion Group for discussions; and J. Hofer, A. Hudson and N. McHale for the use of unpublished data presented in Fig. 3. D.L.A. was the recipient of a Sainsbury PhD studentship. The work was funded by a grant to J.A.L. and R.W.S. from the Biotechnology and Biological Sciences Research Council.

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Author notes

  1. Elizabeth C. Moylan

    Present address: BioMed Central, Middlesex House, 32–42 Cleveland Street, London, W1T 4LB, UK

  2. Debbie L. Alexander

    Present address: Carnegie Institution of Washington, Department of Plant Biology, 260 Panama Street, Stanford, California, 94305, USA

  3. C. Jill Harrison and Susie B. Corley: These authors contributed equally to this work

Authors and Affiliations

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

    C. Jill Harrison, Susie B. Corley, Elizabeth C. Moylan, Debbie L. Alexander, Robert W. Scotland & Jane A. Langdale

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Corresponding author

Correspondence to Jane A. Langdale.

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Supplementary information

Supplementary Figure S1

Hybridization analysis of KNOX and ARP gene families in S. kraussiana. (PPT 280 kb)

Supplementary Figure S2

Sequence alignment and phylogenetic relationships of Selaginella class I KNOX and ARP genes. (PPT 1684 kb)

Supplementary Figure S3

Phylogenetic relationships in the KNOX gene family. (PPT 619 kb)

Supplementary Figure S4

Phylogenetic relationships within the MYB gene super-family. (PPT 77 kb)

Supplementary Figure Legends

Legends to accompany the above Supplementary Figures. This file also contains additional references. (DOC 98 kb)

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Harrison, C., Corley, S., Moylan, E. et al. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434, 509–514 (2005). https://doi.org/10.1038/nature03410

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