HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Andra-Octavia Roman
  • Pedro Jimenez-Sandoval
  • Sebastian Augustin
  • Caroline Broyart
  • Ludwig A. Hothorn
  • Julia Santiago

Research Organisations

External Research Organisations

  • University of Lausanne (UNIL)
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Details

Original languageEnglish
Article number876
Number of pages13
JournalNature Communications
Volume13
Issue number1
Early online date15 Feb 2022
Publication statusPublished - Dec 2022

Abstract

The membrane receptor kinases HAESA and HSL2 recognize a family of IDA/IDL signaling peptides to control cell separation processes in different plant organs. The homologous HSL1 has been reported to regulate epidermal cell patterning by interacting with a different class of signaling peptides from the CLE family. Here we demonstrate that HSL1 binds IDA/IDL peptides with high, and CLE peptides with lower affinity, respectively. Ligand sensing capability and receptor activation of HSL1 require a SERK co-receptor kinase. Crystal structures with IDA/IDLs or with CLE9 reveal that HSL1-SERK1 complex recognizes the entire IDA/IDL signaling peptide, while only parts of CLE9 are bound to the receptor. In contrast, the receptor kinase BAM1 interacts with the entire CLE9 peptide with high affinity and specificity. Furthermore, the receptor tandem BAM1/BAM2 regulates epidermal cell division homeostasis. Consequently, HSL1-IDLs and BAM1/BAM2-CLEs independently regulate cell patterning in the leaf epidermal tissue.

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Cite this

HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides. / Roman, Andra-Octavia; Jimenez-Sandoval, Pedro; Augustin, Sebastian et al.
In: Nature Communications, Vol. 13, No. 1, 876, 12.2022.

Research output: Contribution to journalArticleResearchpeer review

Roman, A-O, Jimenez-Sandoval, P, Augustin, S, Broyart, C, Hothorn, LA & Santiago, J 2022, 'HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides', Nature Communications, vol. 13, no. 1, 876. https://doi.org/10.1038/s41467-022-28558-4
Roman, A.-O., Jimenez-Sandoval, P., Augustin, S., Broyart, C., Hothorn, L. A., & Santiago, J. (2022). HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides. Nature Communications, 13(1), Article 876. https://doi.org/10.1038/s41467-022-28558-4
Roman AO, Jimenez-Sandoval P, Augustin S, Broyart C, Hothorn LA, Santiago J. HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides. Nature Communications. 2022 Dec;13(1):876. Epub 2022 Feb 15. doi: 10.1038/s41467-022-28558-4
Roman, Andra-Octavia ; Jimenez-Sandoval, Pedro ; Augustin, Sebastian et al. / HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides. In: Nature Communications. 2022 ; Vol. 13, No. 1.
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title = "HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides",
abstract = "The membrane receptor kinases HAESA and HSL2 recognize a family of IDA/IDL signaling peptides to control cell separation processes in different plant organs. The homologous HSL1 has been reported to regulate epidermal cell patterning by interacting with a different class of signaling peptides from the CLE family. Here we demonstrate that HSL1 binds IDA/IDL peptides with high, and CLE peptides with lower affinity, respectively. Ligand sensing capability and receptor activation of HSL1 require a SERK co-receptor kinase. Crystal structures with IDA/IDLs or with CLE9 reveal that HSL1-SERK1 complex recognizes the entire IDA/IDL signaling peptide, while only parts of CLE9 are bound to the receptor. In contrast, the receptor kinase BAM1 interacts with the entire CLE9 peptide with high affinity and specificity. Furthermore, the receptor tandem BAM1/BAM2 regulates epidermal cell division homeostasis. Consequently, HSL1-IDLs and BAM1/BAM2-CLEs independently regulate cell patterning in the leaf epidermal tissue.",
author = "Andra-Octavia Roman and Pedro Jimenez-Sandoval and Sebastian Augustin and Caroline Broyart and Hothorn, {Ludwig A.} and Julia Santiago",
note = "Funding Information: The authors thank V. Olieric for providing beam-time and the staff at beam-line PXIII of the Swiss Light Source (SLS), Villigen, for technical assistance during data collection. Special thanks to Zachary Nimchuck (University of North Carolina) for providing us with bam1-4 bam2-4 mutant and Christian Hardtke (University of Lausanne) for the pBAM1::3xNLS::YFP reporter line. We would also like to thank Anaxi Houbaert for his input and help to set up the epidermal cell quantification, and to Yan Ma for helping us with R functions. Supported by the University of Lausanne, Swiss National Science Foundation grants no. 31003A_173101, the European Research Council (ERC) grant agreement no. 716358 and the Fondation Philanthropique Famille Sandoz. ",
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N1 - Funding Information: The authors thank V. Olieric for providing beam-time and the staff at beam-line PXIII of the Swiss Light Source (SLS), Villigen, for technical assistance during data collection. Special thanks to Zachary Nimchuck (University of North Carolina) for providing us with bam1-4 bam2-4 mutant and Christian Hardtke (University of Lausanne) for the pBAM1::3xNLS::YFP reporter line. We would also like to thank Anaxi Houbaert for his input and help to set up the epidermal cell quantification, and to Yan Ma for helping us with R functions. Supported by the University of Lausanne, Swiss National Science Foundation grants no. 31003A_173101, the European Research Council (ERC) grant agreement no. 716358 and the Fondation Philanthropique Famille Sandoz.

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N2 - The membrane receptor kinases HAESA and HSL2 recognize a family of IDA/IDL signaling peptides to control cell separation processes in different plant organs. The homologous HSL1 has been reported to regulate epidermal cell patterning by interacting with a different class of signaling peptides from the CLE family. Here we demonstrate that HSL1 binds IDA/IDL peptides with high, and CLE peptides with lower affinity, respectively. Ligand sensing capability and receptor activation of HSL1 require a SERK co-receptor kinase. Crystal structures with IDA/IDLs or with CLE9 reveal that HSL1-SERK1 complex recognizes the entire IDA/IDL signaling peptide, while only parts of CLE9 are bound to the receptor. In contrast, the receptor kinase BAM1 interacts with the entire CLE9 peptide with high affinity and specificity. Furthermore, the receptor tandem BAM1/BAM2 regulates epidermal cell division homeostasis. Consequently, HSL1-IDLs and BAM1/BAM2-CLEs independently regulate cell patterning in the leaf epidermal tissue.

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