Chitin perception in plasmodesmata characterizes submembrane immune-signaling specificity in plants

Abstract

The plasma membrane (PM) is composed of heterogeneous subdomains, characterized by differences in protein and lipid composition. PM receptors can be dynamically sorted into membrane domains to underpin signaling in response to extracellular stimuli. In plants, the plasmodesmal PM is a discrete microdomain that hosts specific receptors and responses. We exploited the independence of this PM domain to investigate how membrane domains can independently integrate a signal that triggers responses across the cell. Focusing on chitin signaling, we found that responses in the plasmodesmal PM require the LysM receptor kinases LYK4 and LYK5 in addition to LYM2. Chitin induces dynamic changes in the localization, association, or mobility of these receptors, but only LYM2 and LYK4 are detected in the plasmodesmal PM. We further uncovered that chitin-induced production of reactive oxygen species and callose depends on specific signaling events that lead to plasmodesmata closure. Our results demonstrate that distinct membrane domains can integrate a common signal with specific machinery that initiates discrete signaling cascades to produce a localized response.

Functional and structural characterization of LysM proteins in interactions between fungi and plants

“…Rather, this response relies on the OsCEBiP orthologue AtLYM2 (Faulkner et al, 2013). Recently, it was demonstrated that, besides AlLYM2, these responses in the plasmodesmal plasma membrane require AtLYK4 and AtLYK5 as well, although only AtLYM2 and AtLYK4 could be detected in the plasmodesmal plasma membrane (Faulkner et al, 2013;Narusaka et al, 2013;Cheval et al, 2020). Collectively, these observations point towards the existence of dynamic changes in the localization, association, or mobility of these receptors in chitin perception complexes, and furthermore that different receptor complexes may exist at different subcellular localizations.…”

“…Although this receptor generally does not seem to act on the cell membrane, it was shown to mediate molecular fluxes in response to chitin in an AtCERK1-independent manner in plasmodesmata (Faulkner et al, 2013;Narusaka et al, 2013). Although the regulation of these molecular fluxes furthermore requires both AtLYK4 and AtLYK5, only AtLYM2 and AtLYK4 could be detected in the plasmodesmal plasma membrane (Cheval et al, 2020). Collectively, these findings underpin the occurrence of differentially composed chitin receptor complexes at different cellular locations in Arabidopsis.…”

“…This LysM-containing protein binds chitin oligosaccharides and mediates plasmodesmal fluxes between cells in the presence of chitin (Fernandez-Calvino et al, 2011;Shinya et al, 2012;Faulkner et al, 2013). Moreover, it was recently demonstrated that chitin-induced closure of plasmodesmata requires LYK4 and LYK5 in addition to LYM2, and chitin induces dynamic changes in the localization, association, and mobility of these receptors at distinct membrane domains (Cheval et al, 2020).…”

“…It has become evident that within the same plant several chitin receptors can operate, belonging either to the LysM-RLKs or the LysM-RLPs, and that assemble into dynamic receptor complexes upon chitin perception, the composition of which may depend on its localization (Miya et al, 2007;Faulkner et al, 2013;Cao et al, 2014;Cheval et al, 2020). For example, in Arabidopsis, the LysM-RLK AtLYK5 binds chitin with high affinity and acts as the primary chitin receptor (Cao et al, 2014).…”

“…Interestingly, these two receptor proteins also form a ligand-induced protein complex with OsCERK1 in response to bacterial cell wall peptidoglycan (PGN) (Liu et al, 2012a;Ao et al, 2014;Miyata et al, 2014). One of the three OsCEBiP orthologues in Arabidopsis, AtLYM2, controls the chitin-induced molecular fluxes across plasmodesmata and resistance to fungal pathogens independent of AtCERK1 (Faulkner et al, 2013;Narusaka et al, 2013;Cheval et al, 2020). Like OsCERK1, AtCERK1 has been shown to be required for peptidoglycan-triggered immunity (Willmann et al, 2011).…”