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:

Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato

Nature Genetics volume 39, pages 787–791 (2007)Cite this article

Abstract

Plant leaves show pronounced plasticity of size and form. In the classical, partially dominant mutation Lanceolate (La)1, the large compound leaves of tomato (Solanum lycopersicum) are converted into small simple ones. We show that LA encodes a transcription factor from the TCP family2,3 containing an miR319-binding site4. Five independent La isolates are gain-of-function alleles that result from point mutations within the miR319-binding site and confer partial resistance of the La transcripts to microRNA (miRNA)-directed inhibition. The reduced sensitivity to miRNA regulation leads to elevated LA expression in very young La leaf primordia and to precocious differentiation of leaf margins. In contrast, downregulation of several LA-like genes using ectopic expression of miR319 resulted in larger leaflets and continuous growth of leaf margins. Our results imply that regulation of LA by miR319 defines a flexible window of morphogenetic competence along the developing leaf margin that is required for leaf elaboration.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: The molecular basis for the La syndrome.
Figure 2: Spatial distribution of LA and miR319.
Figure 3: Loss of LA-like activities results in delayed leaf differentiation.
Figure 4: Patterning tomato compound leaves.

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  1. Mathan, D.S. & Jenkins, J.A. Chemically induced phenocopy of a tomato mutant. Science 131, 36–87 (1960).

    Article  CAS  Google Scholar 

  2. Cubas, P., Lauter, N., Doebley, J. & Coen, E. The TCP domain: a motif found in proteins regulating plant growth and development. Plant J. 18, 215–222 (1999).

    Article  CAS  Google Scholar 

  3. Nath, U., Crawford, B.C., Carpenter, R. & Coen, E. Genetic control of surface curvature. Science 299, 1404–1407 (2003).

    Article  CAS  Google Scholar 

  4. Palatnik, J.F. et al. Control of leaf morphogenesis by microRNAs. Nature 425, 257–263 (2003).

    Article  CAS  Google Scholar 

  5. 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 

  6. Holtan, H.E. & Hake, S. Quantitative trait locus analysis of leaf dissection in tomato using Lycopersicon pennellii segmental introgression lines. Genetics 165, 1541–1550 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 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 

  8. Menda, N., Semel, Y., Peled, D., Eshed, Y. & Zamir, D. In silico screening of a saturated mutation library of tomato. Plant J. 38, 861–872 (2004).

    Article  CAS  Google Scholar 

  9. Caruso, J.L. Morphogenetic aspects of a leafless mutant in tomato. I. General patterns in development. Am. J. Bot. 55, 1169–1176 (1968).

    Article  Google Scholar 

  10. Dengler, N.G. Comparison of leaf development in Normal (+/+), Entire (E/E), and Lanceolate (La/+) plants of tomato, Lycopersicon esculentum 'Ailsa Craig'. Bot. Gaz. 145, 66–77 (1984).

    Article  Google Scholar 

  11. Mathan, D.S. & Jenkins, J.A. A morphogenetic study of Lanceolate, a leaf shape mutant in the tomato. Am. J. Bot. 49, 504–514 (1962).

    Article  CAS  Google Scholar 

  12. Stettler, R.F. Dosage effects of the Lanceolate gene in tomato. Am. J. Bot. 51, 253–264 (1964).

    Article  Google Scholar 

  13. Hagemann, W. & Gleissberg, S. Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst. Evol. 199, 121–152 (1996).

    Article  Google Scholar 

  14. Dengler, N.G. & Tsukaya, H. Leaf morphogenesis in dicotyledons: current issues. Int. J. Plant Sci. 162, 459–464 (2001).

    Article  Google Scholar 

  15. Boynton, J.E. & Rick, C.M. Linkage tests with mutants of Stubbe's groups I, II, III and IV. Rep. Tomato Genet. Coop. Tomato Genet. Coop. 15, 24–27 (1965).

    Google Scholar 

  16. Li, C., Potuschak, T., Colon-Carmona, A., Gutierrez, R.A. & Doerner, P. Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc. Natl. Acad. Sci. USA 102, 12978–12983 (2005).

    Article  CAS  Google Scholar 

  17. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P. & Burge, C.B. Prediction of mammalian microRNA targets. Cell 115, 787–798 (2003).

    Article  CAS  Google Scholar 

  18. Schwab, R. et al. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8, 517–527 (2005).

    Article  CAS  Google Scholar 

  19. Lifschitz, E. et al. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. USA 103, 6398–6403 (2006).

    Article  CAS  Google Scholar 

  20. Lifschytz, E. & Falk, R. A genetic analysis of the Killer-prune (K-pn) locus of Drosophila melanogaster. Genetics 62, 353–358 (1969).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Stadler, L.J. Some genetic effects of X rays in plants. J. Hered. 21, 3–19 (1930).

    Article  Google Scholar 

  22. Chen, J.-J., Janssen, B.-J., Williams, A. & Sinha, N. A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell 9, 1289–1304 (1997).

    Article  CAS  Google Scholar 

  23. 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 

  24. Alvarez, J.P. et al. Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18, 1134–1151 (2006).

    Article  CAS  Google Scholar 

  25. Baker, C.C., Sieber, P., Wellmer, F. & Meyerowitz, E.M. The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr. Biol. 15, 303–315 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Tang, G., Reinhart, B.J., Bartel, D.P. & Zamore, P.D. A biochemical framework for RNA silencing in plants. Genes Dev. 17, 49–63 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. 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  Google Scholar 

  30. Valoczi, A., Varallyay, E., Kauppinen, S., Burgyan, J. & Havelda, Z. Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J. 47, 140–151 (2006).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We wish to thank E. Lifschitz5 (Technion), the C.M. Rick Tomato Genetics Resource Center and Clemson University Genomics Institute for materials, Navot Ori for unearthing la-6, and R. Fluhr, E. Hornstein, Z. Lippman, D. Weigel, S. Hake, J. Bowman and members of our laboratories for discussions and criticism. The work was supported by grants from the US-Israel Binational Agricultural Research and Development Fund, the European Union (MechPlant project) and the Israel Science Foundation (ISF) to N.O.; from ISF, MINERVA, The US-Israel Binational Science Foundation and Lubin Center for Plant Biotechnology to Y.E.; from the German-Israeli Foundation for Scentific Research and Development to Y.E. and N.O.; and from the German-Israeli Project Cooperation to Y.E. and D.Z.

Author information

Authors and Affiliations

  1. The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture and The Otto Warburg Minerva Center for Agricultural Biotechnology, Faculty of Agriculture, Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel

    Naomi Ori, Aya Refael Cohen, Adi Etzioni, Arnon Brand, Osnat Yanai, Sharona Shleizer, Naama Menda & Dani Zamir

  2. Department of Plant Sciences, Weizmann Institute of Science, Rehovot, 76100, Israel

    Ziva Amsellem, Idan Efroni, Irena Pekker, John Paul Alvarez, Eyal Blum & Yuval Eshed

Authors
  1. Naomi Ori
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aya Refael Cohen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adi Etzioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arnon Brand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Osnat Yanai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sharona Shleizer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Naama Menda
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ziva Amsellem
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Idan Efroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Irena Pekker
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. John Paul Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Eyal Blum
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Dani Zamir
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yuval Eshed
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the experiments and their interpretation. N.O., D.Z. and Y.E. directed the experiments, and N.O. and Y.E. wrote the manuscript.

Corresponding authors

Correspondence to Naomi Ori or Yuval Eshed.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

The Lanceolate syndrome in leaves and flowers. (PDF 619 kb)

Supplementary Fig. 2

Genetic and molecular characterization of LA. (PDF 473 kb)

Supplementary Fig. 3

The LA-like protein family. (PDF 999 kb)

Supplementary Fig. 4

Quantification of LA and Tkn2/LeT6 expression in genotypes representing a gradient of LA activity. (PDF 358 kb)

Supplementary Fig. 5

Heterochronic differences in wild-type and la-6 leaf morphology. (PDF 564 kb)

Supplementary Fig. 6

Genetic interactions of La-2 with other leaf shape mutants. (PDF 291 kb)

Supplementary Table 1

Primers used in this study (PDF 19 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ori, N., Cohen, A., Etzioni, A. et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39, 787–791 (2007). https://doi.org/10.1038/ng2036

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng2036

This article is cited by

Search

Advanced 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