Abstract
As much as 10% of plant immune receptors from the nucleotide-binding domain leucine-rich repeat (NLR) family carry integrated domains (IDs) that can directly bind pathogen effectors. However, it remains unclear whether direct binding to effectors is a universal feature of ID-containing NLRs given that only a few NLR-IDs have been functionally characterized. Here we show that the rice (Oryza sativa) sensor NLR-ID Pii2 confers resistance to strains of the rice blast fungus Magnaporthe oryzae that carry the effector AVR-Pii without directly binding this protein. First, we show that AVR-Pii binds the exocyst subunit OsExo70F2 in rice (Oryza sativa) to dissociate preformed complexes of OsExo70F2 with host RPM1 INTERACTING PROTEIN4 (RIN4) at the conserved NOI motif, facilitating a possible virulence function. Second, we show that in its resting state, Pii2 binds OsExo70F2 and OsExo70F3, essential components of Pii-mediated resistance, through its integrated NOI domain. Remarkably, AVR-Pii binding to OsExo70F2/F3 leads to dissociation of the Pii2–OsExo70F2 and Pii2–OsExo70F3 complexes, destabilization of Pii2, and activation of immunity. These findings support a novel conceptual model in which an NLR-ID monitors alterations of tethered host proteins targeted by pathogen effectors, providing insight into pathogen recognition mechanisms.
Significance statement Plant diseases diminish crop yields by over 20% each year, and deploying resistant crops is the most effective way to combat them. Nucleotide-binding domain leucine-rich repeat (NLR)-type receptors are the major player in plant resistance against pathogens, with a subset of NLRs containing unconventional domains called integrated domains (ID) derived from host proteins. Previous studies suggest that pathogen avirulence (AVR) effectors directly bind or modify NLR-IDs before they are recognized by the host. Here, we reveal that the rice NLR-ID receptor Pii2 indirectly recognizes AVR-Pii when the effector dissociates Pii2 from the host Exo70 proteins tethered to Pii2. We propose a new model of how NLRs can recognize pathogens, expanding our understanding of plant immunity.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
This version was thoroughly revised with new results of gene knockout of OsExo70F2 and F3 (Fig. 1), interactions among AVR-Pii/Exo70/Pii2 (Fig.2), importance of NOI domain in Pii2 for its function and stability (Fig. 3), effect of Exo70 on stabilization of Pii2, and effect of AVR-Pii on dissociation of Exo70 and Pii2. A new model of interaction between pathogen AVR and plant NLR is proposed.
