OsBBI1-targeted OsSUI1 negatively regulates rice immunity through modulating the nonsense-mediated mRNA decay pathway.

E3 ubiquitin ligases, as key components of the protein ubiquitination process, play a crucial role in rice immunity. We previously demonstrated that the E3 ligase OsBBI1 modulates rice blast resistance. Here, we report the OsBBI1-OsSUI1-nonsense-mediated mRNA decay (NMD)-alternatively splicing (AS) network as a regulatory mechanism of OsBBI1 in rice immunity. OsBBI1 ubiquitinates the eukaryotic translation initiation factor OsSUI1 for degradation. Knockout mutant ossui1 exhibited enhanced resistance to blast and bacterial blight diseases and displayed over-accumulation of defense-related AS transcripts, which was also elevated in OsBBI1-OE plants, including OsDR11S that positively modulates blast resistance. The impaired chitin-triggered immune responses in osbbi1 mutants were partially rescued by OsSUI1 mutation. The NMD factors, for example OsUPF1, OsUPF3, and OsSMG7, were upregulated in ossui1 and OsBBI1-OE plants. Knockdown mutants osupf1, osupf3, and ossmg7 over-accumulated defense-related AS transcripts and enhanced disease resistance. The chitin-triggered immune responses in ossui1 depended on alterations in downstream genes, including the NMD genes and defense-related AS transcripts. OsBBI1 regulated OsSUI1 and OsSMG7 accumulation, while OsSUI1 influenced OsSMG7. Blast fungus infection and chitin treatment decreased OsSUI1 and OsSMG7 levels. These findings suggest that OsBBI1-mediated degradation of OsSUI1 modulates the NMD pathway, leading to the accumulation of defense-related AS transcripts and enhanced rice immunity.