Plant pathogenic fungi hijack phosphate signaling with conserved enzymatic effectors

Abstract

Inorganic phosphate (Pi) is essential for life, and plant cells monitor Pi availability by sensing inositol pyrophosphate (PP-InsP) levels. In this work, we describe the hijacking of plant phosphate sensing by a conserved family of Nudix hydrolase effectors from pathogenic Magnaporthe and Colletotrichum fungi. Structural and enzymatic analyses of the Nudix effector family demonstrate that they selectively hydrolyze PP-InsP. Gene deletion experiments of Nudix effectors in Magnaporthe oryzae, Colletotrichum higginsianum, and Colletotrichum graminicola indicate that PP-InsP hydrolysis substantially enhances disease symptoms in diverse pathosystems. Further, we show that this conserved effector family induces phosphate starvation signaling in plants. Our study elucidates a molecular mechanism, used by multiple phytopathogenic fungi, that manipulates the highly conserved plant phosphate sensing pathway to exacerbate disease.