Article | Published:

Competitive binding of antagonistic peptides fine-tunes stomatal patterning

Nature volume 522, pages 439443 (25 June 2015) | Download Citation

Abstract

During development, cells interpret complex and often conflicting signals to make optimal decisions. Plant stomata, the cellular interface between a plant and the atmosphere, develop according to positional cues, which include a family of secreted peptides called epidermal patterning factors (EPFs). How these signalling peptides orchestrate pattern formation at a molecular level remains unclear. Here we report in Arabidopsis that Stomagen (also called EPF-LIKE9) peptide, which promotes stomatal development, requires ERECTA (ER)-family receptor kinases and interferes with the inhibition of stomatal development by the EPIDERMAL PATTERNING FACTOR 2 (EPF2)–ER module. Both EPF2 and Stomagen directly bind to ER and its co-receptor TOO MANY MOUTHS. Stomagen peptide competitively replaced EPF2 binding to ER. Furthermore, application of EPF2, but not Stomagen, elicited rapid phosphorylation of downstream signalling components in vivo. Our findings demonstrate how a plant receptor agonist and antagonist define inhibitory and inductive cues to fine-tune tissue patterning on the plant epidermis.

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Acknowledgements

We thank I. Hara-Nishimura for STOMAGEN-ami lines and anti-Stomagen antibody; K. Peterson for iSTOMAGEN construct and transgenic lines; M. Kanaoka and N. Kamiya for LURE2 peptides; D. Baulcombe for p19 plasmid; C. Tamerler and M. Sarikaya for use of the HPLC, QCM and MALDI-ToF equipment; A. Hofstetter for technical assistance; and J. McAbee, K. Peterson, T. Imaizumi, B. Wakimoto, S. Di Rubbo and R. Horst for comments. K.U.T. is an HHMI-GBMF Investigator and an Endowed Distinguished Professor of Biology; J.S.L. was an NSERC Postdoctoral Fellow. Y.-C.L.L. was a Mary Gates Undergraduate Research Fellow of the University of Washington.

Author information

Affiliations

  1. Howard Hughes Medical Institute, University of Washington, Seattle, Washington 98195, USA

    • Jin Suk Lee
    • , Ya-Chen Lisa Lin
    • , Soon-Ki Han
    • , Julian Avila
    •  & Keiko U. Torii
  2. Department of Biology, University of Washington, Seattle, Washington 98195, USA

    • Jin Suk Lee
    • , Michal Maes
    • , Ya-Chen Lisa Lin
    • , Aarthi Putarjunan
    • , Soon-Ki Han
    • , Julian Avila
    •  & Keiko U. Torii
  3. Department of Materials Science and Engineering, University of Washington, Seattle, Washington 98195, USA

    • Marketa Hnilova

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Contributions

J.S.L. and K.U.T. conceived the project. J.S.L., M.H., M.M., J.A. and Y.-C.L.L. purified peptides and performed ligand−receptor binding and bioassays. J.S.L and S.-K.H. performed RT–PCR. J.S.L. and A.P. performed MAPK assays. J.S.L. and Y.-C.L.L. performed quantitative analysis of stomatal phenotypes. K.U.T. constructed STOMAGEN cDNA plasmid. K.U.T., J.S.L., M.H., M.M., Y.-C.L.L., A.P. and S.-K.H. analysed the data. K.U.T. wrote the manuscript with inputs from all co-authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Keiko U. Torii.

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https://doi.org/10.1038/nature14561

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