Skip to main content

Thank you for visiting 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.

SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis


Leaves of flowering plants are determinate organs produced by pluripotent structures termed shoot apical meristems. Once specified, leaves differentiate an adaxial (upper) side specialized for light capture, and an abaxial (lower) side specialized for gas exchange. A functional relationship between meristem activity and the differentiation of adaxial leaf fate has been recognized for over fifty years, but the molecular basis of this interaction is unclear. In Arabidopsis thaliana, activity of the class I KNOX (KNOTTED1-like homeobox) genes SHOOTMERISTEMLESS (STM) and BREVIPEDICELLUS (BP) is required for meristem function but excluded from leaves1,2,3, whereas members of the HD-Zip III (class III homeodomain leucine zipper) protein family function to promote both meristem activity and adaxial leaf fate4,5,6. Here we show that the zinc-finger protein SERRATE acts in a microRNA (miRNA) gene-silencing pathway to regulate expression of the HD-Zip III gene PHABULOSA (PHB) while also limiting the competence of shoot tissue to respond to KNOX expression. Thus, SERRATE acts to coordinately regulate meristem activity and leaf axial patterning.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: se alleles condition defects in leaf axial patterning and increased meristem size.
Figure 2: SE regulates PHB expression.
Figure 3: SE functions in a miRNA gene-silencing pathway.
Figure 4: SE antagonises KNOX activity.


  1. 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)

    ADS  CAS  Article  PubMed  Google Scholar 

  2. 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)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Byrne, M. E., Simorowski, J. & Martienssen, R. A. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129, 1957–1965 (2002)

    CAS  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  6. Juarez, M. T., Kui, J. S., Thomas, J., Heller, B. A. & Timmermans, M. C. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84–88 (2004)

    ADS  CAS  Article  PubMed  Google Scholar 

  7. 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 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Gallois, J. L., Woodward, C., Reddy, G. V. & Sablowski, R. Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129, 3207–3217 (2002)

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  11. Bao, N., Lye, K. W. & Barton, M. K. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell 7, 653–662 (2004)

    CAS  Article  PubMed  Google Scholar 

  12. Prigge, M. J. & Wagner, D. R. The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13, 1263–1279 (2001)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Ori, N., Eshed, Y., Chuck, G., Bowman, J. L. & Hake, S. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127, 5523–5532 (2000)

    CAS  PubMed  Google Scholar 

  14. Englbrecht, C. C., Schoof, H. & Bohm, S. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5, 39 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

  15. Golling, G. et al. Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nature Genet. 31, 135–140 (2002)

    CAS  Article  PubMed  Google Scholar 

  16. Mallory, A. C. et al. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J. 23, 3356–3364 (2004)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Green, K. A., Prigge, M. J., Katzman, R. B. & Clark, S. E. CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17, 691–704 (2005)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Smith, H. M. & Hake, S. The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15, 1717–1727 (2003)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Hay, A. et al. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 12, 1557–1565 (2002)

    CAS  Article  PubMed  Google Scholar 

  20. Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657 (2003)

    ADS  Article  PubMed  Google Scholar 

  21. 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 

  22. Bougourd, S., Marrison, J. & Haseloff, J. Technical advance: an aniline blue staining procedure for confocal microscopy and 3D imaging of normal and perturbed cellular phenotypes in mature Arabidopsis embryos. Plant J. 24, 543–550 (2000)

    CAS  Article  PubMed  Google Scholar 

Download references


We are indebted to K. Barton and B. Reinhart for providing plasmids 35S::PHB (pJM2) and 35S::PHB-1D (pMKB2) and for sharing data before publication. For helpful discussions and seed storks we thank N. Ori and S. Hake (bp-9 seeds) and Y. Eshed and J. Bowman (phb-6; phv-5; rev-9/ + seeds). We also thank M. Prigge for se-1 Ler seeds, R. Sablowski for STMGR seeds and J. Langdale for comments on the manuscript, the Arabidopsis Biological Resource Center and Syngenta for se-3 and se-2 seeds respectively, and J. Baker for photography. Finally, we thank A. Bird and I. Henderson for advice on bisulphite sequencing. This work was funded by a BBSRC grant to M.T. S.P.G. is the recipient of a Sainsbury Studentship from the Gatsby Charitable Foundation and A.H. is the recipient of a University of Oxford Glasstone Research Fellowship.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Miltos Tsiantis.

Ethics declarations

Competing interests

Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplemntary Figure S1

A schematic of the SE genomic locus indicating the positions of lesions in se mutant alleles, and contains information regarding transcripts produced by these alleles. (DOC 31 kb)

Supplementary Figure S2

RT-PCR and RNA gel blot analysis of expression of various transcripts in se-3 and Col, and contains descriptions of PCR conditions and primer sequences. (DOC 302 kb)

Supplementary Figure S3

A histogram reflecting the cytosine methylation status of a region of the PHB genomic locus in se-3 and Col. Clones generated from se-3 show reduced levels of CpG methylation. (PDF 77 kb)

Supplementary Figure S4

Gene expression analysis of the gibberellic acid biosynthetic gene GA5, demonstrating that this gene is similarly regulated in a KNOX gain-of-function line, a dominant phb mutant, and se-1. (DOC 137 kb)

Supplementary Methods

Experimental procedures used in generation of the supporting online material not included in the main methods section. (DOC 28 kb)

Supplementary Table S1

A sequence alignment of all clones analysed for generating bisulphite sequencing data presented in Supplementary Figure S3. (DOC 39 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Grigg, S., Canales, C., Hay, A. et al. SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437, 1022–1026 (2005).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

Further reading


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.


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