Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice

Abstract

Many phytopathogens secrete cell wall degradation enzymes (CWDEs) to damage host cells and facilitate colonization. As the major components of the plant cell wall, cellulose and hemicellulose are the targets of CWDEs. Damaged plant cells often release damage-associated molecular patterns (DAMPs) to trigger plant immune responses. Here, we establish that the fungal pathogen Magnaporthe oryzae secretes the endoglucanases MoCel12A and MoCel12B during infection of rice (Oryza sativa). These endoglucanases target hemicellulose of the rice cell wall and release two specific oligosaccharides, namely the trisaccharide 31-β-D-Cellobiosyl-glucose and the tetrasaccharide 31-β-D-Cellotriosyl-glucose. 31-β-D-Cellobiosyl-glucose and 31-β-D-Cellotriosyl-glucose bind the immune receptor OsCERK1 but not the chitin binding protein OsCEBiP. However, they induce the dimerization of OsCERK1 and OsCEBiP. In addition, these Poaceae cell wall-specific oligosaccharides trigger a burst of reactive oxygen species (ROS) that is largely compromised in oscerk1 and oscebip mutants. We conclude that 31-β-D-Cellobiosyl-glucose and 31-β-D-Cellotriosyl-glucose are specific DAMPs released from the hemicellulose of rice cell wall, which are perceived by an OsCERK1 and OsCEBiP immune complex during M. oryzae infection in rice.

Secreted Glycoside Hydrolase Proteins as Effectors and Invasion Patterns of Plant-Associated Fungi and Oomycetes

“…Taken together, these results suggested that MoCel12A and/or MoCel12B negatively contribute to the virulence of M. oryzae . This is supported by the finding that the ectopic expression of MoCel12A in rice leads to enhanced resistance against this fungus, associated with the significant upregulation of immune-responsive genes, a dwarf phenotype, and the formation of spontaneous lesions on leaves of transgenic plants ( Yang et al, 2021 ).…”

“…Secreted GH12 proteins from plant-associated fungi and oomycetes also play an active role in DAMP release. Examples include MoCel12A and MoCel12B, two secreted GH12 proteins with β-glucanase (endoglucanase) activity from M. oryzae ( Takeda et al, 2010 ; Yang et al, 2021 ). The expression of both MoCel12A and MoCel12B is upregulated during the early stages of infection when the fungus is undergoing biotrophic growth.…”

“…The expression of both MoCel12A and MoCel12B is upregulated during the early stages of infection when the fungus is undergoing biotrophic growth. Here, expression is initiated at 8 h post-inoculation (hpi), around the time of primary infection hyphae formation, then peaks at 24 and 12 hpi, respectively ( Yang et al, 2021 ). While ∆mocel12a deletion mutants did not display reduced virulence on rice, ∆mocel12a/b double-mutants exhibited enhanced virulence, as measured by more severe disease symptoms and increased fungal biomass ( Yang et al, 2021 ).…”

“…Here, expression is initiated at 8 h post-inoculation (hpi), around the time of primary infection hyphae formation, then peaks at 24 and 12 hpi, respectively ( Yang et al, 2021 ). While ∆mocel12a deletion mutants did not display reduced virulence on rice, ∆mocel12a/b double-mutants exhibited enhanced virulence, as measured by more severe disease symptoms and increased fungal biomass ( Yang et al, 2021 ). Furthermore, strains overexpressing MoCel12A had reduced biomass during host infection ( Yang et al, 2021 ).…”

“…While ∆mocel12a deletion mutants did not display reduced virulence on rice, ∆mocel12a/b double-mutants exhibited enhanced virulence, as measured by more severe disease symptoms and increased fungal biomass ( Yang et al, 2021 ). Furthermore, strains overexpressing MoCel12A had reduced biomass during host infection ( Yang et al, 2021 ). Taken together, these results suggested that MoCel12A and/or MoCel12B negatively contribute to the virulence of M. oryzae .…”