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

Julien Gronnier,Michelle Von Arx,Martin Stegmann,Kai Dünser,Zhenbiao Yang,Christina M Franck,Cyril Zipfel,Christoph Ringli,Alicia Abarca,Wenwei Lin,Jürgen Kleine-Vehn,Thomas A Defalco

doi:10.7554/elife.74162

Abstract

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.

Highlights

Multicellular organisms evolved sophisticated surveillance systems to monitor44 changes in their environment
Using this approach, we found that FLAGELLIN SENSING 2 (FLS2)-GFP fluorescence was maintained into well-defined and static structures in WT, while it appeared more disperse and more mobile in both fer mutants (Figure 1A, B and Figure 1 – figure supplement 2)
Flg22-induced reactive oxygen species (ROS) production was reduced in lrx3/4/5 174 similar to the levels observed in fer-4 (Figure 2B)

Summary

23 ABSTRACT

Spatial partitioning is a propensity of biological systems orchestrating cell activities in space and time. The receptor kinase FERONIA (FER) controls ligand[28] 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 31 (RALF23) by FER inhibits immunity. 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, regulate BAK1 nanoscale organization and immune signaling. RALF23 perception leads to rapid modulation 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

42 INTRODUCTION

104 RESULTS AND DISCUSSION

314 ACKNOWLEDGMENTS

856 MATERIALS AND METHODS

Col-0 Mock Col-0 RALF23