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

eLife ◽  
2022 ◽  
Vol 11 ◽  
Author(s):  
Julien Gronnier ◽  
Christina M Franck ◽  
Martin Stegmann ◽  
Thomas A DeFalco ◽  
Alicia Abarca ◽  
...  
Keyword(s):  
Plasma Membrane ◽  
Peptide Hormone ◽  
Fundamental Aspect ◽  
Receptor Kinase ◽  
Plant Signaling ◽  
Immune Signaling ◽  
Dynamic Regulation ◽  
Immune Receptor ◽  
Rapid Modulation ◽  
Cell Surface Signaling

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, 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 plasma membrane nanoscale organization to regulate cell surface signaling by other ligand-binding receptor kinases.

scholarly journals FERONIA regulates FLS2 plasma membrane nanoscale dynamics to modulate plant immune signaling

2020 ◽  
Author(s):  
Julien Gronnier ◽  
Christina M. Franck ◽  
Martin Stegmann ◽  
Thomas A. DeFalco ◽  
Alicia Abarca Cifuentes ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Complex Formation ◽  
Cell Surface ◽  
Single Particle Tracking ◽  
Receptor Kinase ◽  
Leucine Rich Repeat ◽  
Immune Signaling ◽  
Receptor Complexes ◽  
Nanoscale Dynamics

ABSTRACTCell surface receptors survey and relay information to ensure the development and survival of multicellular organisms. In the model plant Arabidopsis thaliana, the Catharanthus roseus RLK1-like receptor kinase FERONIA (FER) regulates myriad of biological processes to coordinate development, growth and responses to the environment. We recently showed that FER positively regulates immune signaling by controlling the ligand-induced complex formation between the leucine-rich repeat receptor kinase (LRR-RK) FLAGELLIN SENSING 2 (FLS2) and its co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3 (BAK1/SERK3). In this context, FER function is inhibited by binding of its peptide ligand RAPID ALKALINIZATION FACTOR 23 (RALF23). However, the mechanisms by which FER regulates FLS2-BAK1 complex formation remain unclear. Here, we show that FER-dependent regulation of immune signaling is independent of its kinase activity, indicating that FER rather plays a structural role. FER has been proposed to bind directly to the plant cell wall, but we found that a FER mutant unable to bind pectin is still functional in regulating immune signaling. Instead, FER- and cell wall-associated LEUCINE RICH REPEAT-EXTENSIN proteins are required for this regulation. Using high-resolution live-imaging and single-particle tracking, we observed that FER regulates FLS2 plasma membrane nanoscale dynamics, which may explain its role in controlling ligand-induced FLS2-BAK1 association. We propose that FER acts as an anchoring point connecting cell wall and plasma membrane nano-environments to enable the nucleation of pre-formed receptor/co-receptor complexes at the cell surface.

scholarly journals Dynamic Regulation of Caveolin-1 Trafficking in the Germ Line and Embryo of Caenorhabditis elegans

2006 ◽  
Vol 17 (7) ◽  
pp. 3085-3094 ◽  
Author(s):  
Ken Sato ◽  
Miyuki Sato ◽  
Anjon Audhya ◽  
Karen Oegema ◽  
Peter Schweinsberg ◽  
...  
Keyword(s):  
Cell Cycle ◽  
Plasma Membrane ◽  
Caenorhabditis Elegans ◽  
Fluorescent Protein ◽  
Germ Line ◽  
Cortical Granule ◽  
Major Protein ◽  
Dynamic Regulation ◽  
Caveolin 1 ◽  
Green Fluorescent

Caveolin is the major protein component required for the formation of caveolae on the plasma membrane. Here we show that trafficking of Caenorhabditis elegans caveolin-1 (CAV-1) is dynamically regulated during development of the germ line and embryo. In oocytes a CAV-1-green fluorescent protein (GFP) fusion protein is found on the plasma membrane and in large vesicles (CAV-1 bodies). After ovulation and fertilization the CAV-1 bodies fuse with the plasma membrane in a manner reminiscent of cortical granule exocytosis as described in other species. Fusion of CAV-1 bodies with the plasma membrane appears to be regulated by the advancing cell cycle, and not fertilization per se, because fusion can proceed in spe-9 fertilization mutants but is blocked by RNA interference–mediated knockdown of an anaphase-promoting complex component (EMB-27). After exocytosis, most CAV-1-GFP is rapidly endocytosed and degraded within one cell cycle. CAV-1 bodies in oocytes appear to be produced by the Golgi apparatus in an ARF-1–dependent, clathrin-independent, mechanism. Conversely endocytosis and degradation of CAV-1-GFP in embryos requires clathrin, dynamin, and RAB-5. Our results demonstrate that the distribution of CAV-1 is highly dynamic during development and provides new insights into the sorting mechanisms that regulate CAV-1 localization.

scholarly journals The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling

Science ◽  
2017 ◽  
Vol 355 (6322) ◽  
pp. 287-289 ◽  
Author(s):  
Martin Stegmann ◽  
Jacqueline Monaghan ◽  
Elwira Smakowska-Luzan ◽  
Hanna Rovenich ◽  
Anita Lehner ◽  
...  
Keyword(s):  
Receptor Kinase ◽  
Immune Signaling

scholarly journals Comprehensive Analysis of Human Cytomegalovirus- and HIV-Mediated Plasma Membrane Remodeling in Macrophages

mBio ◽  
2021 ◽  
Author(s):  
Ramona Businger ◽  
Saima Kivimäki ◽  
Stefan Simeonov ◽  
Georgios Vavouras Syrigos ◽  
Justus Pohlmann ◽  
...  
Keyword(s):  
Plasma Membrane ◽  
Human Cytomegalovirus ◽  
Comprehensive Analysis ◽  
Membrane Remodeling ◽  
Immune Signaling

The PM is a key component that viruses have to cope with. It is a barrier for infection and egress and is critically involved in antiviral immune signaling.

scholarly journals An XA21-Associated Kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors

2013 ◽  
Author(s):  
Xuewei Chen ◽  
Shimin Zuo ◽  
Benjamin Schwessinger ◽  
Mawsheng Chern ◽  
Patrick Canlas ◽  
...  
Keyword(s):  
Direct Interaction ◽  
Dependent Manner ◽  
Receptor Kinase ◽  
Immune Receptor ◽  
Immune Receptors ◽  
Yeast Two Hybrid System ◽  
Intracellular Domains ◽  
Activity Dependent

The rice XA21 immune receptor kinase and the structurally related XA3 receptor, confer immunity to Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial leaf blight. Here we report the isolation of OsSERK2 (rice somatic embryogenesis receptor kinase 2) and demonstrate that OsSERK2 positively regulates immunity mediated by XA21 and XA3 as well as the rice immune receptor FLS2 (OsFLS2). Rice plants silenced for OsSerk2 display altered morphology and reduced sensitivity to the hormone brassinolide. OsSERK2 interacts with the intracellular domains of each immune receptor in the yeast-two-hybrid system in a kinase activity dependent manner. OsSERK2 undergoes bidirectional trans-phosphorylation with XA21 in vitro and forms a constitutive complex with XA21 in vivo. Taken together, these results demonstrate an essential role for OsSERK2 in the function of three rice immune receptors and suggest that direct interaction with the rice immune receptors is critical for their function.

scholarly journals Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor

2019 ◽  
Vol 116 (17) ◽  
pp. 8525-8534 ◽  
Author(s):  
Dee Dee Luu ◽  
Anna Joe ◽  
Yan Chen ◽  
Katarzyna Parys ◽  
Ofir Bahar ◽  
...  
Keyword(s):  
Immune Response ◽  
Biological Process ◽  
Peptide Hormone ◽  
Xanthomonas Oryzae ◽  
Targeted Proteomics ◽  
Mature Peptide ◽  
Immune Receptor ◽  
High Affinity ◽  
Precursor Peptide ◽  
Modified Peptides

The rice immune receptor XA21 is activated by the sulfated microbial peptide required for activation of XA21-mediated immunity X (RaxX) produced byXanthomonas oryzaepv.oryzae(Xoo). Mutational studies and targeted proteomics revealed that the RaxX precursor peptide (proRaxX) is processed and secreted by the protease/transporter RaxB, the function of which can be partially fulfilled by a noncognate peptidase-containing transporter component B (PctB). proRaxX is cleaved at a Gly–Gly motif, yielding a mature peptide that retains the necessary elements for RaxX function as an immunogen and host peptide hormone mimic. These results indicate that RaxX is a prokaryotic member of a previously unclassified and understudied group of eukaryotic tyrosine sulfated ribosomally synthesized, posttranslationally modified peptides (RiPPs). We further demonstrate that sulfated RaxX directly binds XA21 with high affinity. This work reveals a complete, previously uncharacterized biological process: bacterial RiPP biosynthesis, secretion, binding to a eukaryotic receptor, and triggering of a robust host immune response.

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