Article | Published:

The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors

Nature Plantsvolume 4pages10711081 (2018) | Download Citation

Abstract

The frequency and orientation of cell division are regulated by intercellular signalling molecules; however, tissue-specific regulatory systems for cell divisions are only partially understood. Here, we report that the peptide hormone CLAVATA3/ESR-RELATED 9/10 (CLE9/10) regulates two different developmental processes, stomatal lineage development and xylem development, through two distinct receptor systems in Arabidopsis thaliana. We show that the receptor kinase HAESA-LIKE 1 (HSL1) is a CLE9/10 receptor that regulates stomatal lineage cell division, and BARELY NO MERISTEM (BAM) class receptor kinases are CLE9/10 receptors that regulate periclinal cell division of xylem precursor cells. Both HSL1 and BAM1 bind to CLE9/10, but only HSL1 recruits SOMATIC EMBRYOGENESIS RECEPTOR KINASES as co-receptors in the presence of CLE9/10, suggesting different signalling modes for these receptor systems.

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The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Change history

  • 26 December 2018

    In the version of this Article originally published, the authors incorrectly stated that the work was supported by Innovative Areas grant number 25003006; the correct number is 25113006. This statement has now been amended in all online versions of the Article.

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Acknowledgements

Special thanks to H. Fukuda and Y. Kondo for providing us with all of the synthetic CLE peptides, Q.-J. Chen for the CRISPR vector (pHEE401E), K. Torii, D. Bergmann, S. Hou and the Arabidopsis Biological Resource Center seed stock centre for mutant seeds, and H. Deng and Y. Xu for mass spectrometry analysis. We thank K. Tsujimura for making vectors containing histone H2BsfGFP and mNEONGREEN optimized for A.thaliana. We thank Y. Matsubayashi and H. Shinohara for providing us with bam1-4 and bam1-4clv1-101 mutants, discussions and preliminary experiments, and B. Morris and A. Deneve for advice on English usage. This work was supported by Grant-in-Aid for Scientific Research (B) number 25291060, Innovative Areas grant numbers 25113006 and 18H04837 to T.K. and the Ministry of Science and Technology of China (2015CB910200) to J.C.

Author information

Author notes

  1. These authors contributed equally: Pingping Qian, Wen Song.

Affiliations

  1. Graduate School of Science, Osaka University, Osaka, Japan

    • Pingping Qian
    • , Toshiya Yokoo
    • , Ayako Minobe
    • , Guodong Wang
    •  & Tatsuo Kakimoto
  2. Innovation Center for Structural Biology, Tsinghua-Peking Joint Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, China

    • Wen Song
    •  & Jijie Chai
  3. Max-Planck Institute for Plant Breeding Research, Cologne, Germany

    • Wen Song
    •  & Jijie Chai
  4. Institute of Biochemistry, University of Cologne, Cologne, Germany

    • Wen Song
    •  & Jijie Chai
  5. Key Laboratory of MOE for Medicinal Plant Resource and Natural Pharmaceutical Chemistry, National Engineering Laboratory for Resource Developing of Endangered Chinese Crude Drugs in Northwest of China, College of Life Sciences, Shaanxi Normal University, Xi’an, China

    • Guodong Wang
  6. International Research Organization for Advanced Science and Technology (IROAST) Kumamoto University, Kumamoto, Japan

    • Takashi Ishida
  7. Graduate School of Science and Technology, Kumamoto University, Kumamoto, Japan

    • Shinichiro Sawa

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Contributions

P.Q., W.S., T.Y., A.M., G.W. and T.I. performed the experiments. P.Q., T.I., S.S., J.C. and T.K. designed the research. P.Q., W.S., J.C. and T.K. wrote the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Jijie Chai or Tatsuo Kakimoto.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–21 and Supplementary Tables 1–3.

  2. Reporting Summary

  3. Supplementary Video 1

    Periclinal cell divisions of xylem precursor cells in wild type.

  4. Supplementary Video 2

    Periclinal cell divisions of xylem precursor cells in cle9-c1.

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DOI

https://doi.org/10.1038/s41477-018-0317-4