The Bifunctional Plant Receptor, OsCERK1, Regulates Both Chitin-Triggered Immunity and Arbuscular Mycorrhizal Symbiosis in Rice

Abstract

Plants are constantly exposed to threats from pathogenic microbes and thus developed an innate immune system to protect themselves. On the other hand, many plants also have the ability to establish endosymbiosis with beneficial microbes such as arbuscular mycorrhizal (AM) fungi or rhizobial bacteria, which improves the growth of host plants. How plants evolved these systems managing such opposite plant-microbe interactions is unclear. We show here that knockout (KO) mutants of OsCERK1, a rice receptor kinase essential for chitin signaling, were impaired not only for chitin-triggered defense responses but also for AM symbiosis, indicating the bifunctionality of OsCERK1 in defense and symbiosis. On the other hand, a KO mutant of OsCEBiP, which forms a receptor complex with OsCERK1 and is essential for chitin-triggered immunity, established mycorrhizal symbiosis normally. Therefore, OsCERK1 but not chitin-triggered immunity is required for AM symbiosis. Furthermore, experiments with chimeric receptors showed that the kinase domains of OsCERK1 and homologs from non-leguminous, mycorrhizal plants could trigger nodulation signaling in legume-rhizobium interactions as the kinase domain of Nod factor receptor1 (NFR1), which is essential for triggering the nodulation program in leguminous plants, did. Because leguminous plants are believed to have developed the rhizobial symbiosis on the basis of AM symbiosis, our results suggest that the symbiotic function of ancestral CERK1 in AM symbiosis enabled the molecular evolution to leguminous NFR1 and resulted in the establishment of legume-rhizobia symbiosis. These results also suggest that OsCERK1 and homologs serve as a molecular switch that activates defense or symbiotic responses depending on the infecting microbes.

The Nod factor-independent nodulation in Aeschynomene evenia required the common plant-microbe symbiotic "toolkit"

“…However, this border has been crossed through the identification of the mycorrhizal lipochitooligosaccharide, whose structure appears very close to that of the NFs (Maillet et al, 2011), and the discovery in P. andersonii of a LysM-RLK receptor involved in both rhizobial and mycorrhizal recognition (Op den Camp et al, 2011). Another member of the LysM-RLK family, Chitin Elicitor Receptor Kinase1 (CERK1), was recently shown to be involved in the perception of pathogenic and symbiotic microbial patterns (Miyata et al, 2014). These data support the hypothesis of a role for LysM-RLKs in the perception of a broad range of microbial patterns, and our next goal is to identify their role in legume-rhizobium NF-independent symbioses.…”

Algal ancestor of land plants was preadapted for symbiosis

“…Genetic and transcriptomic analyses in angiosperms led to the characterization of genes controlling these steps (19,20). At the plasma membrane, a receptor complex composed of lysin motif receptor-like kinase (LysM-RLK) proteins and a malectinlike domain (MLD)-RLK (DMI2) perceives the Myc factor signals (17,21,22) and activates a nuclear envelope-localized potassium channel (DMI1) that initiates and maintains rapid oscillations of calcium within and around the nucleus (23). These calcium "spikes" are decoded by a calcium-and calmodulindependent protein kinase (CCaMK), a specific calcium-dependent protein kinase (CDPK) also regulated by calmodulin (24).…”

Chitin and chitin-related compounds in plant–fungal interactions

“…The perception of shorter oligosaccharides such as chitotetraose could instead rely on monomeric receptors (Miyata et al 2014; Shinya et al 2015) as into each receptor’s LysM domain, half of this oligomer molecule (C4) fits (Liu et al 2012; Shinya et al 2015). …”

“…From OsCERK1/CEBiP receptor dimer, knock-out mutants of OsCERK1 receptor kinase was found to be essential for chitin signalling in rice, where not only chitin-triggered defence responses but also arbuscular mycorrhizal symbiosis was impaired, indicating the bifunctionality of CERK1 in defence and symbiosis (Miyata et al 2014). On the other hand, a knock-out mutant of CEBiP, which forms receptor complex with CERK1 and was essential for chitin-triggered immunity, established mycorrhizal symbiosis.…”

“…On the other hand, a knock-out mutant of CEBiP, which forms receptor complex with CERK1 and was essential for chitin-triggered immunity, established mycorrhizal symbiosis. Therefore, OsCERK1 but not chitin-triggered immunity was required for arbuscular mycorrhizal symbiosis (Miyata et al 2014). Sánchez-Vallet et al (2015) proposed that CERK1 has a dual function in symbiosis and immunity, and acts as an adaptor in multiple receptor complexes, rather than as a receptor for a specific ligand.…”