Cargando…

Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors

Spatial partitioning is a propensity of biological systems orchestrating cell activities in space and time. The dynamic regulation of plasma membrane nano-environments has recently emerged as a key fundamental aspect of plant signaling, but the molecular components governing it are still mostly uncl...

Descripción completa

Detalles Bibliográficos
Autores principales: Gronnier, Julien, Franck, Christina M, Stegmann, Martin, DeFalco, Thomas A, Abarca, Alicia, von Arx, Michelle, Dünser, Kai, Lin, Wenwei, Yang, Zhenbiao, Kleine-Vehn, Jürgen, Ringli, Christoph, Zipfel, Cyril
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8791635/
https://www.ncbi.nlm.nih.gov/pubmed/34989334
http://dx.doi.org/10.7554/eLife.74162
_version_ 1784640226974498816
author Gronnier, Julien
Franck, Christina M
Stegmann, Martin
DeFalco, Thomas A
Abarca, Alicia
von Arx, Michelle
Dünser, Kai
Lin, Wenwei
Yang, Zhenbiao
Kleine-Vehn, Jürgen
Ringli, Christoph
Zipfel, Cyril
author_facet Gronnier, Julien
Franck, Christina M
Stegmann, Martin
DeFalco, Thomas A
Abarca, Alicia
von Arx, Michelle
Dünser, Kai
Lin, Wenwei
Yang, Zhenbiao
Kleine-Vehn, Jürgen
Ringli, Christoph
Zipfel, Cyril
author_sort Gronnier, Julien
collection PubMed
description Spatial partitioning is a propensity of biological systems orchestrating cell activities in space and time. The dynamic regulation of plasma membrane nano-environments has recently emerged as a key fundamental aspect of plant signaling, but the molecular components governing it are still mostly unclear. The receptor kinase FERONIA (FER) controls ligand-induced complex formation of the immune receptor kinase FLAGELLIN SENSING 2 (FLS2) with its co-receptor BRASSINOSTEROID-INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1), and perception of the endogenous peptide hormone RAPID ALKALANIZATION FACTOR 23 (RALF23) by FER inhibits immunity. Here, we show that FER regulates the plasma membrane nanoscale organization of FLS2 and BAK1. Our study demonstrates that akin to FER, leucine-rich repeat (LRR) extensin proteins (LRXs) contribute to RALF23 responsiveness and regulate BAK1 nanoscale organization and immune signaling. Furthermore, RALF23 perception leads to rapid modification of FLS2 and BAK1 nanoscale organization, and its inhibitory activity on immune signaling relies on FER kinase activity. Our results suggest that perception of RALF peptides by FER and LRXs actively modulates plasma membrane nanoscale organization to regulate cell surface signaling by other ligand-binding receptor kinases.
format Online
Article
Text
id pubmed-8791635
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-87916352022-01-27 Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors Gronnier, Julien Franck, Christina M Stegmann, Martin DeFalco, Thomas A Abarca, Alicia von Arx, Michelle Dünser, Kai Lin, Wenwei Yang, Zhenbiao Kleine-Vehn, Jürgen Ringli, Christoph Zipfel, Cyril eLife Cell Biology Spatial partitioning is a propensity of biological systems orchestrating cell activities in space and time. The dynamic regulation of plasma membrane nano-environments has recently emerged as a key fundamental aspect of plant signaling, but the molecular components governing it are still mostly unclear. The receptor kinase FERONIA (FER) controls ligand-induced complex formation of the immune receptor kinase FLAGELLIN SENSING 2 (FLS2) with its co-receptor BRASSINOSTEROID-INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1), and perception of the endogenous peptide hormone RAPID ALKALANIZATION FACTOR 23 (RALF23) by FER inhibits immunity. Here, we show that FER regulates the plasma membrane nanoscale organization of FLS2 and BAK1. Our study demonstrates that akin to FER, leucine-rich repeat (LRR) extensin proteins (LRXs) contribute to RALF23 responsiveness and regulate BAK1 nanoscale organization and immune signaling. Furthermore, RALF23 perception leads to rapid modification of FLS2 and BAK1 nanoscale organization, and its inhibitory activity on immune signaling relies on FER kinase activity. Our results suggest that perception of RALF peptides by FER and LRXs actively modulates plasma membrane nanoscale organization to regulate cell surface signaling by other ligand-binding receptor kinases. eLife Sciences Publications, Ltd 2022-01-06 /pmc/articles/PMC8791635/ /pubmed/34989334 http://dx.doi.org/10.7554/eLife.74162 Text en © 2022, Gronnier et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Gronnier, Julien
Franck, Christina M
Stegmann, Martin
DeFalco, Thomas A
Abarca, Alicia
von Arx, Michelle
Dünser, Kai
Lin, Wenwei
Yang, Zhenbiao
Kleine-Vehn, Jürgen
Ringli, Christoph
Zipfel, Cyril
Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
title Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
title_full Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
title_fullStr Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
title_full_unstemmed Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
title_short Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
title_sort regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8791635/
https://www.ncbi.nlm.nih.gov/pubmed/34989334
http://dx.doi.org/10.7554/eLife.74162
work_keys_str_mv AT gronnierjulien regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT franckchristinam regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT stegmannmartin regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT defalcothomasa regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT abarcaalicia regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT vonarxmichelle regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT dunserkai regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT linwenwei regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT yangzhenbiao regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT kleinevehnjurgen regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT ringlichristoph regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors
AT zipfelcyril regulationofimmunereceptorkinaseplasmamembranenanoscaleorganizationbyaplantpeptidehormoneanditsreceptors