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

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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Fig. 1: The CLE9/10 peptide negatively regulates the formation of stomatal precursor cells by SPCH destabilization.
Fig. 2: Mutations in CLE9 increase the numbers of epidermal cells in cotyledons and leaves.
Fig. 3: The HSL1 receptor kinase is required for the action of CLE9/10 on stomatal lineage development.
Fig. 4: CLE9/10 directly binds to HSL1 and induces the recruitment of SERK1.
Fig. 5: CLE9/10 negatively regulates periclinal cell division in xylem files.
Fig. 6: The BAM family receptors are required for CLE9/10 regulation of xylem numbers.
Fig. 7: A model for the action of CLE9/10.

Data availability

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

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.

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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.

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Correspondence to Jijie Chai or Tatsuo Kakimoto.

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

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Supplementary Video 1

Periclinal cell divisions of xylem precursor cells in wild type.

Supplementary Video 2

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

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Qian, P., Song, W., Yokoo, T. et al. The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors. Nature Plants 4, 1071–1081 (2018). https://doi.org/10.1038/s41477-018-0317-4

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