Regulation of immune receptor kinases plasma membrane nanoscale landscape 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 unclear. The receptor kinase FERONIA (FER) controls complex formation of the immune receptor kinase FLAGELLIN SENSING 2 (FLS2) with its co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1), and this function is inhibited by the FER ligand RAPID ALKALANIZATION FACTOR 23 (RALF23). 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 (LRXs) proteins contribute to RALF23 responsiveness, regulate BAK1 nanoscale organization and immune signaling. Furthermore, 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 the plasma membrane nanoscale landscape to regulate cell surface signaling by other receptor kinases.

[1]  J. Chai,et al.  Pollen PCP-B peptides unlock a stigma peptide–receptor kinase gating mechanism for pollination , 2021, Science.

[2]  C. Ringli,et al.  Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis , 2020, PLoS genetics.

[3]  S. Mayor,et al.  The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity , 2020, Life Science Alliance.

[4]  T. Ott,et al.  The Nanoscale Organization of the Plasma Membrane and Its Importance in Signaling: A Proteolipid Perspective1[OPEN] , 2019, Plant Physiology.

[5]  K. Malínská,et al.  Cell wall contributes to the stability of plasma membrane nanodomain organization of Arabidopsis thaliana FLOTILLIN2 and HYPERSENSITIVE INDUCED REACTION1 proteins. , 2019, The Plant journal : for cell and molecular biology.

[6]  J. Chai,et al.  Mechanisms of RALF peptide perception by a heterotypic receptor complex , 2019, Nature.

[7]  S. Botchway,et al.  The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis , 2018, Proceedings of the National Academy of Sciences.

[8]  S. Mithoe,et al.  Regulation of pattern recognition receptor signalling by phosphorylation and ubiquitination. , 2018, Current opinion in plant biology.

[9]  Julien Gronnier,et al.  Divide and Rule: Plant Plasma Membrane Organization. , 2018, Trends in plant science.

[10]  S. Assmann,et al.  A kinase‐dead version of FERONIA receptor‐like kinase has dose‐dependent impacts on rosette morphology and RALF1‐mediated stomatal movements , 2018, FEBS letters.

[11]  R. Sormani,et al.  Receptor Kinase THESEUS1 Is a Rapid Alkalinization Factor 34 Receptor in Arabidopsis , 2018, Current Biology.

[12]  Artemis Perraki,et al.  Phosphocode-dependent functional dichotomy of a common co-receptor in plant signaling , 2018, Nature.

[13]  C. T. Anderson,et al.  FERONIA’s sensing of cell wall pectin activates ROP GTPase signaling in Arabidopsis , 2018, bioRxiv.

[14]  K. Mysore,et al.  Symbiotic root infections in Medicago truncatula require remorin-mediated receptor stabilization in membrane nanodomains , 2017, Proceedings of the National Academy of Sciences.

[15]  L. Lai,et al.  Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling , 2017, Science.

[16]  U. Grossniklaus,et al.  RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis , 2017, Science.

[17]  P. He,et al.  From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition. , 2017, Annual review of phytopathology.

[18]  E. Hosy,et al.  Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains , 2017, eLife.

[19]  U. Hohmann,et al.  The Structural Basis of Ligand Perception and Signal Activation by Receptor Kinases. , 2017, Annual review of plant biology.

[20]  D. MacLean,et al.  Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains , 2017, eLife.

[21]  Johannes Schindelin,et al.  TrackMate: An open and extensible platform for single-particle tracking. , 2017, Methods.

[22]  J. Hohlbein,et al.  Visualization of BRI1 and SERK3/BAK1 Nanoclusters in Arabidopsis Roots , 2017, PloS one.

[23]  Alexandra Kroll,et al.  Classification and Segmentation of Nanoparticle Diffusion Trajectories in Cellular Micro Environments , 2017, PloS one.

[24]  C. Zipfel,et al.  The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling , 2017, Science.

[25]  Jonathan D. G. Jones,et al.  Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. , 2014, Molecular cell.

[26]  M. Sussman,et al.  A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion , 2014, Science.

[27]  J. Borst,et al.  Visualization of BRI1 and BAK1(SERK3) Membrane Receptor Heterooligomers during Brassinosteroid Signaling1[W][OPEN] , 2013, Plant Physiology.

[28]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[29]  S. Botchway,et al.  Cell wall constrains lateral diffusion of plant plasma-membrane proteins , 2012, Proceedings of the National Academy of Sciences.

[30]  Alexandra M. E. Jones,et al.  The Arabidopsis Leucine-Rich Repeat Receptor–Like Kinases BAK1/SERK3 and BKK1/SERK4 Are Required for Innate Immunity to Hemibiotrophic and Biotrophic Pathogens[W] , 2011, Plant Cell.

[31]  Alexandra M. E. Jones,et al.  Phosphorylation-Dependent Differential Regulation of Plant Growth, Cell Death, and Innate Immunity by the Regulatory Receptor-Like Kinase BAK1 , 2011, PLoS genetics.

[32]  J. Friml,et al.  PIN Polarity Maintenance by the Cell Wall in Arabidopsis , 2011, Current Biology.

[33]  A. Cheung,et al.  FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development , 2010, Proceedings of the National Academy of Sciences.

[34]  Wendy Goucher,et al.  Walls have ears , 2010 .

[35]  T. Boller,et al.  Rapid Heteromerization and Phosphorylation of Ligand-activated Plant Transmembrane Receptors and Their Associated Kinase BAK1* , 2010, The Journal of Biological Chemistry.

[36]  W. Frommer,et al.  Plasma membrane microdomains regulate turnover of transport proteins in yeast , 2008, The Journal of cell biology.

[37]  Sophia Mersmann,et al.  Plant Pattern-Recognition Receptor FLS2 Is Directed for Degradation by the Bacterial Ubiquitin Ligase AvrPtoB , 2008, Current Biology.

[38]  K. Jaqaman,et al.  Robust single particle tracking in live cell time-lapse sequences , 2008, Nature Methods.

[39]  Jonathan D. G. Jones,et al.  A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence , 2007, Nature.

[40]  T. Boller,et al.  Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation , 2006, Cell.

[41]  B. Keller,et al.  The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. , 2001, Genes & development.

[42]  T. Boller,et al.  FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. , 2000, Molecular cell.

[43]  Leonie Steinhorst,et al.  The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca 2 + Signaling Graphical Abstract Highlights , 2018 .

[44]  P. Janssen,et al.  Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex , 2013 .