Discriminating symbiosis and immunity signals by receptor competition in rice

Abstract

Plants encounter various microbes in nature and must respond appropriately to symbiotic or pathogenic ones. In rice, the receptor-like kinase OsCERK1 is involved in recognizing both symbiotic and immune signals. However, how these opposing signals are discerned via OsCERK1 remains unknown. Here, we found that receptor competition enables the discrimination of symbiosis and immunity signals in rice. On the one hand, the symbiotic receptor OsMYR1 and its short-length chitooligosaccharide ligand inhibit complex formation between OsCERK1 and OsCEBiP and suppress OsCERK1 phosphorylating the downstream substrate OsGEF1, which reduces the sensitivity of rice to microbe-associated molecular patterns. Indeed, OsMYR1 overexpression lines are more susceptible to the fungal pathogen Magnaporthe oryzae, whereas Osmyr1 mutants show higher resistance. On the other hand, OsCEBiP can bind OsCERK1 and thus block OsMYR1–OsCERK1 heteromer formation. Consistently, the Oscebip mutant displayed a higher rate of mycorrhizal colonization at early stages of infection. Our results indicate that OsMYR1 and OsCEBiP receptors compete for OsCERK1 to determine the outcome of symbiosis and immunity signals.

Associations of Pantoea with Rice Plants: As Friends or Foes?

“…Then, a LysM receptor heteromer OsMYR1/OsLYK2 and OsCERK1 in rice plants recognized the Myc factors secreted by mycorrhiza. However, a recent study by Zhang et al [83] reported that CO4 and its receptor OsMYR1 were not only involved in initiating symbiotic signalling but also involved in reducing rice immunity by decreasing immune signalling induced by CO8, a bioactive immunity signal secreted by mycorrhiza. This study further indicates that a balanced perception of multiple symbiotic receptors in rice is important for the establishment of a successful mutualistic rice plant association with microbes (including Pantoea).…”

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

“…For example, lipochitooligosaccharide Nod Factors are perceived by legumes (Radutoiu et al, 2003;Bozsoki et al, 2020). In rice, shortchained chitotetraose triggers symbiotic signal transduction with the symbiotic complex receptor MYR1-CERK1, and this suppresses the formation of the CEBiP-CERK1 heteromer (Chiu and Paszkowski, 2021;Zhang et al, 2021). Besides, symbionts are also capable of colonizing hosts while overcoming the response to damage-associated molecular patterns (DAMPs) and MAMPs, while a response against pathogens is possible in the presence of non-pathogenic microbes (Zhou et al, 2020).…”

Rhizosphere Microbiome: The Emerging Barrier in Plant-Pathogen Interactions

“…In plants, innate immune systems can prevent most pathogens, while allowing colonization of symbiosis and beneficial microbes (Bozsoki et al, 2020;Zhou et al, 2020;Fröschel et al, 2021;Zhang et al, 2021). For example, after inoculation with the vascular pathogen Verticillium longisporum, pathogenic oomycete Phytophthora parasitica, or mutualistic endophyte Serendipita indica, plant root cell-layer responses were different, as revealed by cell-layer translatomes analysis, reflecting the fundamentally different colonization strategies of these microbes (Fröschel et al, 2021).…”

“…Though the protein structures of CERK6 and NFR1 are very similar, plants use regions II and IV of LysM1 to specifically recognize pathogens (chitin) or symbiotic signaling molecules (Nod factor) and initiate differential signaling of immunity or root nodule symbiosis (Bozsoki et al, 2020). Another recent advance revealed that the CO4 (Chitotetraose) symbiotic receptor OsMYR1 can initiate symbiotic signaling as well as repress rice immunity by depleting the receptor-like kinase OsCERK1, thereby preventing the formation of the immunity complex OsCERK1-OsCEBiP in rice (Zhang et al, 2021), suggesting that OsMYR1 and OsCEBiP receptors compete to bind OsCERK1 to determine the specific response outcomes of symbiosis and immunity signals. Therefore, these lines of evidence suggest plants encountering various microbes in nature could respond appropriately to pathogenic or symbiotic microbes (Figure 2), and the exploration of plant distinguishing pathogen from rhizosphere microbiome is likely to be revealed.…”

“…Studies suggest that plants affect and recruit soil beneficial microbial community in response to pathogenic microorganism attack, without activating a strong immune response to support its growth and fitness (Hacquard et al, 2017;Yin et al, 2021). Moreover, substantial work has revealed that plants could distinguish pathogenic and beneficial microbes accurately and maintain the dynamic balance between plant growth and defenses (Hacquard et al, 2017;Bozsoki et al, 2020;Zhou et al, 2020;Buscaill and van der Hoorn, 2021;Emonet et al, 2021;Ma et al, 2021;Zhang et al, 2021). Here we review and discuss (i) the current status of rhizosphere microbiome; (ii) emphasizing on its role in the context of plant-pathogen interactions, by acting as a barrier to pathogen invasion; (iii) showing the possibility of engineering diseasesuppressive microbes in response to pathogen attack.…”