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:

microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity

Abstract

In both animals and plants, many developmentally important regulatory genes have complementary microRNAs (miRNAs), which suggests that these miRNAs constitute a class of developmental signalling molecules1. Leaves of higher plants exhibit a varying degree of asymmetry along the adaxial/abaxial (upper/lower) axis. This asymmetry is specified through the polarized expression of class III homeodomain/leucine zipper (HD-ZIPIII) genes2,3,4. In Arabidopsis, three such genes, PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV), are expressed throughout the incipient leaf, but become adaxially localized after primordium emergence. Downregulation of the HD-ZIPIII genes allows expression of the KANADI and YABBY genes, which specify abaxial fate5,6,7,8. PHB, PHV and REV transcripts contain a complementary site for miRNA165 and miRNA166, which can direct their cleavage in vitro9,10,11. Here we show that miRNA166 constitutes a highly conserved polarizing signal whose expression pattern spatially defines the expression domain of the maize hd-zipIII family member rolled leaf1 (rld1). Moreover, the progressively expanding expression pattern of miRNA166 during leaf development and its accumulation in phloem suggests that miRNA166 may form a movable signal that emanates from a signalling centre below the incipient leaf.

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: Effects of Rld1-O on leaf polarity.
Figure 2: Dominant Rld1 mutations affect the miRNA166 complementary site.
Figure 3: rld1 and phb expression in the wild type and Rld1-O.
Figure 4: Complementary hd-zipIII and miRNA166 expression.

Similar content being viewed by others

References

  1. Carrington, J. C. & Ambros, V. Role of microRNAs in plant and animal development. Science 301, 336–338 (2003)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  3. Emery, J. F. et al. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13, 1768–1774 (2003)

    Article  CAS  Google Scholar 

  4. Otsuga, D., DeGuzman, B., Prigge, M. J., Drews, G. N. & Clark, S. E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 25, 223–236 (2001)

    Article  CAS  Google Scholar 

  5. 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  Google Scholar 

  6. Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. & Poethig, R. S. KANADI regulates organ polarity in Arabidopsis. Nature 411, 706–709 (2001)

    Article  ADS  CAS  Google Scholar 

  7. Sawa, S. et al. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079–1088 (1999)

    Article  CAS  Google Scholar 

  8. Siegfried, K. R. et al. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117–4128 (1999)

    CAS  PubMed  Google Scholar 

  9. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B. & Bartel, D. P. MicroRNAs in plants. Genes Dev. 16, 1616–1626 (2002)

    Article  CAS  Google Scholar 

  10. Rhoades, M. W. et al. Prediction of plant microRNA targets. Cell 110, 513–520 (2002)

    Article  CAS  Google Scholar 

  11. 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 

  12. McConnell, J. R. & Barton, M. K. Leaf polarity and meristem formation in Arabidopsis. Development 125, 2935–2942 (1998)

    CAS  Google Scholar 

  13. Nelson, J. M., Lane, B. & Freeling, M. Expression of a mutant maize gene in the ventral leaf epidermis is sufficient to signal a switch of the leaf's dorsoventral axis. Development 129, 4581–4589 (2002)

    CAS  PubMed  Google Scholar 

  14. Llave, C., Kasschau, K. D., Rector, M. A. & Carrington, J. C. Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605–1619 (2002)

    Article  CAS  Google Scholar 

  15. Park, W., Li, J., Song, R., Messing, J. & Chen, X. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12, 1484–1495 (2002)

    Article  CAS  Google Scholar 

  16. Aukerman, M. J. & Sakai, H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730–2741 (2003)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  18. Zhong, R. & Ye, Z. H. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11, 2139–2152 (1999)

    Article  CAS  Google Scholar 

  19. Ratcliffe, O. J., Riechmann, J. L. & Zhang, J. Z. INTERFASCICULAR FIBERLESS1 is the same gene as REVOLUTA. Plant Cell 12, 315–317 (2000)

    Article  CAS  Google Scholar 

  20. Llave, C., Xie, Z., Kasschau, K. D. & Carrington, J. C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053–2056 (2002)

    Article  ADS  CAS  Google Scholar 

  21. Timmermans, M. C. P., Schultes, N. P., Jankovsky, J. P. & Nelson, T. Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125, 2813–2823 (1998)

    CAS  PubMed  Google Scholar 

  22. Sussex, I. M. Morphogenesis in Solanum tuberosum L.: Experimental investigation of leaf dorsiventrality and orientation in the juvenile shoot. Phytomorphology 5, 286–300 (1955)

    Google Scholar 

  23. Snow, M. & Snow, R. The dorsiventrality of leaf primordia. New Phytol. 58, 188–207 (1959)

    Article  Google Scholar 

  24. Foster, T. M. et al. A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14, 1479–1508 (2002)

    Article  Google Scholar 

  25. Burr, B., Burr, F. A., Thompson, K. H., Albertson, M. C. & Stuber, C. W. Gene mapping with recombinant inbreds in maize. Genetics 118, 519–526 (1988)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Timmermans, M. C. P., Das, O. P. & Messing, J. Characterization of a meiotic crossover in maize identified by a restriction fragment length polymorphism-based method. Genetics 143, 1771–1783 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Jackson, D. in Molecular Plant Pathology: A Practical Approach (eds Bowles, D. J., Gurr, S. J. & McPherson, M.) 163–174 (Oxford Univ. Press, Oxford, 1991)

    Google Scholar 

Download references

Acknowledgements

We thank T. Phelps-Durr, C. Kidner, T. Volpe and G. Hannon for discussions and comments on the manuscript. We also thank T. Mulligan for plant care. This work was supported by grants from the USDA. and the NSF (to M.C.P.T.). M.T.J. is funded in part by a W. Burghardt Turner Fellowship, and J.S.K. is an Alfred Hershey Fellow of the Watson School of Biological Sciences and is supported by a grant from the National Institute of General Medical Sciences, NIH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marja C. P. Timmermans.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Juarez, M., Kui, J., Thomas, J. et al. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84–88 (2004). https://doi.org/10.1038/nature02363

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02363

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