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

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, 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.

S-acylation stabilizes ligand-induced receptor kinase complex formation during plant pattern-triggered immune signalling

“…This process stabilises signalling active FLS2 molecular assemblies. These data therefore provide a mechanistic basis for the observed phenomenon of activation state dependent changes in membrane nanodomain content and organisation described for various RKs, including FLS2 [18, 20, 40, 42].…”

“…Live cell imaging of unstimulated FLS2 and BAK1 indicates that complex composition, specifically presence or absence of the RK FERONIA (FER), has marked effects on nanoscale organisation and mobility of in the plasma membrane. In addition, activation of the RK FERONIA (FER) by its ligand RALF23 alters BAK1 organisation and mobility [20]. This indicates that both complex composition, and the activation state of individual components, affects behaviour of the whole complex.…”

“…As part of this overall process, flg22 binding by FLS2 has been shown to dictate FLS2 phosphorylation, SUMOylation and ubiquitination state, indicating a high degree of post-translational regulation. FLS2 activation also alters overall complex composition [7][8][9][10][11][12][13][14][15][16][17], biophysical properties [18] and behaviour [19,20] of the complex. However, the underlying mechanisms and functional relevance of these changes remain unknown.…”

FERONIA Receptor Kinase Integrates with Hormone Signaling to Regulate Plant Growth, Development, and Responses to Environmental Stimuli

“…The leucine-rich repeat (LRR)-extensins (LRXs) are a class of cell wall-localized chimeric extensin proteins [ 48 ]. Recent findings reveal that the N-terminal LRR domain of LRXs interacts with both FER and RALFs [ 49 , 50 , 51 ]. FER is a well-known receptor of RALF peptides [ 27 , 52 , 53 , 54 ], and the LRXs–RALFs–FER module has been demonstrated to play pivotal roles in regulating plant growth and immunity [ 49 , 50 , 51 , 55 , 56 ].…”

“…Recent findings reveal that the N-terminal LRR domain of LRXs interacts with both FER and RALFs [ 49 , 50 , 51 ]. FER is a well-known receptor of RALF peptides [ 27 , 52 , 53 , 54 ], and the LRXs–RALFs–FER module has been demonstrated to play pivotal roles in regulating plant growth and immunity [ 49 , 50 , 51 , 55 , 56 ]. In the context of ABA responses, the ABA accumulation in Arabidopsis mutants lrx345 and fer-4 were dramatically increased, which contributed to the salt-hypersensitivity of these mutants [ 56 ].…”