A plant RNA-binding protein senses 2′,3′-cNMP produced by insect effectors

RNA-derived 2′,3′-cyclophosphate-terminated nucleotides act as immune signalling molecules in prokaryotes and eukaryotes1–3, but how plants perceive them remains unknown. Sucking insects inject digestive enzymes including RNases into the host plant to acquire nutrients. Here we demonstrate that NIB1, a glycine-rich RNA-binding protein in rice, senses 2′,3′-cyclic nucleotide monophosphates (2′,3′-cNMPs; 2′,3′-cAMP and 2′,3′-cGMP) and adenylyl-(3′→5′)-guanosine 2′,3′-cyclic phosphate (ApG>p) produced by a salivary T2 ribonuclease of green stink bug during feeding. Binding of the RNase products promotes formation of nuclear condensates containing NIB1, which recruit the core immune regulator Enhanced Disease Susceptibility 1 (EDS1) and activate defence, potentially contributing to the immune signalling of Toll/interleukin-1 receptor (TIR) proteins that also produce the nuclease products. Exogenous application of 2′,3′-cAMP, 2′,3′-cGMP or ApG>p elicits NIB1 and EDS1-mediated immune responses. Our findings unveil a conserved pathway in plants, in which glycine-rich RNA-binding proteins perceive the nuclease-generated second messengers to launch defence and point to a potential link between plant TIR nuclease activity and EDS1 signalling. The rice RNA-binding protein NIB1 detects 2′,3′-cyclic nucleotide products from insect saliva RNase, forming nuclear condensates that recruit EDS1 to activate defence, revealing a conserved messenger-based immune pathway in plants.