Plant Molecular Biology

, Volume 51, Issue 3, pp 415–425 | Cite as

The ArabidopsisCLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins

  • Vijay K. Sharma
  • Julio Ramirez
  • Jennifer C. Fletcher


Members of the receptor-like kinase gene family play crucial regulatory roles in many aspects of plant development, but the ligands to which they bind are largely unknown. In Arabidopsis, the receptor kinase CLAVATA1 (CLV1) binds to the small secreted polypeptide CLV3, and three proteins act as key elements of a signal transduction pathway that regulates shoot apical meristem maintenance. To better understand the signal transduction mechanisms involving small polypeptides, we are studying 25 Arabidopsis CLV3/ESR (CLE) proteins that share a conserved C-terminal domain with CLV3 and three maize ESR proteins. Members of the CLE gene family were identified in database searches and only a few are known to be expressed. We have identified an additional member of the CLE gene family in Arabidopsis, which is more similar in gene structure to CLV3 than the other CLE genes. Phylogenetic analysis reveals that few of the putative CLE gene products are closely related, suggesting there may be little functional overlap between them. We show that 24 of the 25 ArabidopsisCLE genes are transcribed in one or more tissues during development, indicating that they do encode functional products. Many are widely expressed, but others are restricted to one or a few tissue types. We have also determined the sub-cellular localization of several CLE proteins, and find that they are exported to the plasma membrane or extracellular space. Our results suggest that the Arabidopsis CLE proteins, like CLV3, may function as secreted signaling molecules that act in diverse pathways during growth and development.

Arabidopsis plant development polypeptides signal transduction 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Blanc, G., Barakat, A., Guyot, R., Cooke, R. and Delseny, M. 2000. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12: 1093–1101.Google Scholar
  2. Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M. and Simon, R. 2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617–619.Google Scholar
  3. Clark, S.E., Williams, R.W. and Meyerowitz, E.M. 1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575–585.Google Scholar
  4. Cock, J.M. and McCormick, S. 2001. A large family of genes that share homology with CLAVATA3. Plant Physiol. 126: 939–942.Google Scholar
  5. Fletcher, J.C., Brand, U., Running, M.P., Simon, R. and Meyerowitz, E.M. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911–1914.Google Scholar
  6. Gomez-Gomez, L. and Boller, T. 2000. FLS2: a LRR receptorlike kinase involved in recognition of the flagellin elicitor in Arabidopsis. Mol. Cell 5: 1–20.Google Scholar
  7. Hecht V., Vielle-Calzada, J.-P., Hartog, M.V., Schmidt, E.D.L., Boutilier, K., Grossniklaus, U. and de Vries, S.C. 2001. The Arabidopsis somatic embryogenesis receptor kinase1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 127: 803–816.Google Scholar
  8. Initiative, A.G. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–814.Google Scholar
  9. Jinn, T.-L., Stone, J.M. and Walker, J.C. 2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abcission. Genes Dev. 14: 108–117.Google Scholar
  10. Li, J. and Chory, J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929–938.Google Scholar
  11. Lucas, W.J., Ding, B. and van der Schoot, C. 1993. Plasmodesmata and the supracellular nature of plants. New Phytol. 125: 435–476.Google Scholar
  12. Lucas, W.J., Bouche-Pillon, S., Jackson, D.P., Nguyen, L., Baker, L., Ding, B. and Hake, S. 1995. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270: 1980–dy1983.Google Scholar
  13. Nadeau, J.A. and Sack, F.D. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296: 1697–1700.Google Scholar
  14. Ni, M., Tepperman, J.M. and Quail, P.H. 1998. PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95: 657–667.Google Scholar
  15. Ohtake, Y., Takahashi, T. and Komeda, Y. 2000. Salicylic acid induces the expression of a number of receptor-like kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 41: 1038–1044.Google Scholar
  16. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V. and Fletcher, J.C. 2002. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14: 969–977.Google Scholar
  17. Sanford, J.C., Smith, F.D. and Russell, J.A. 1993. Optimizing the biolistic process for different biological applications. Meth. Enzymol. 217: 483–509.Google Scholar
  18. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F.X., Jurgens, G. and Laux, T. 2000. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635–644.Google Scholar
  19. Sessions, A., Yanofsky, M.F. and Weigel, D. 2002. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289: 779–781.Google Scholar
  20. Shiu, S.H. and Bleecker, A.B. 2001. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98: 10763–10768.Google Scholar
  21. Torii, K.U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R.F. and Komeda, Y. 1996. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735–746.Google Scholar
  22. Trotochaud, A., Jeong, S. and Clark, S.E. 2000. CLAVATA3, a multimeric ligand for the CLAVATA1 receptor-kinase. Science 289: 613–617.Google Scholar
  23. von Armin, A.G., Deng, X.W. and Stacey, M.G. 1998. Cloning vectors for the expression of green fluorescent proteins in transgenic plants. Gene 221: 35–43.Google Scholar
  24. Wagner, T.A. and Kohorn, B.D. 2001. Wall-associated kinases are expressed throughout plant development and required for cell expansion. Plant Cell 13: 303–318.Google Scholar
  25. Walker, J.C. 1993. Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J. 3: 451–456.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Vijay K. Sharma
    • 1
  • Julio Ramirez
    • 1
  • Jennifer C. Fletcher
    • 1
    • 2
  1. 1.Department of Plant and Microbial BiologyUniversity of CaliforniaBerkeleyUSA
  2. 2.USDA Plant Gene Expression CenterAlbanyUSA

Personalised recommendations