Rice HMA proteins function as sensor receptors that detect the conserved MAX effector AvrPigm, form filament-like oligomers with nucleic acids to catalyze production of 2',3'-cAMP/cGMP signaling molecules, which are subsequently perceived by the LRR domains of executor CNL receptors such as PigmR to activate broad-spectrum blast resistance, establishing a previously unrecognized sensor-executor immunity mechanism in plants.

Plants deploy a sensor repertoire, usually NLRs, to perceive pathogen effectors and activate executor NLR-triggered immunity. Here we reveal that rice HMA proteins function as sensors detecting the Magnaporthe oryzae MAX effector AvrPigm to trigger broad-spectrum blast resistance mediated by the CNL PigmR. AvrPigm is conserved with multiple copies in blast genomes and targets HMA proteins, facilitating HMA translocation into the cytoplasm. Cryo-EM structure of the HPP04HMA reveals a filament-like oligomer with ssDNA/RNA bound inside the filament, which display cyclic nucleotide synthase activity to generate 2′,3′-cNMP in a CNL-dependent manner. We further discovered that the LRR domains of the executor CNLs perceive 2′,3′-cNMP to mount immunity. Our study thus establishes an unrecognized immunity mode with a distinct repertoire of sensor receptors that produce signaling molecules that are perceived by the LRR domains of executor NLRs to mediate immunity, shedding new light on the sensor-executor conception and immune activation in plants.

Highlights

HMA proteins and CNL receptors form a new sensor-executor mode in plant immunity

Cryo-EM reveals the filament-like structure of HMA-ssRNA/ssDNA

HMA proteins are cyclic nucleotide synthetases to generate 2′,3′-cNMP

LRR domains of CNLs perceive 2′,3′-cNMP to mediate immunity