A fungal nuclease effector subverts the chloroplast genome and triggers cell death to promote infection.

The hemibiotrophic fungus Magnaporthe oryzae causes rice blast, a devastating plant disease, by transitioning from biotrophic to necrotrophic growth, which triggers host cell death. This trophic shift is essential for nutrient acquisition and disease progression, culminating in conidiation. However, the molecular mechanisms underlying this transition are not well understood. Here, by screening 298 candidate effector proteins upregulated during late infection stages, we identified six necrotrophic effectors (NEEs) from M. oryzae, with MoNee6 exhibiting a particularly important role in virulence. MoNee6 functions as a nuclease that specifically localizes to rice chloroplasts and degrades chloroplast DNA, directly inducing host cell death. Nevertheless, MoNee6 is unstable within the chloroplast and is degraded by the rice chloroplast caseinolytic protease (Clp). To improve host resistance, we engineered OsClpP1 as a nuclear-encoded, chloroplast-targeted protein by fusing it to a chloroplast transit peptide, thereby enabling its expression independent of the native chloroplast-genome-encoded function. This modification enhanced Clp-mediated degradation of MoNee6 and substantially reduced the severity of rice blast. Our findings reveal a previously unrecognized interaction between an effector and the chloroplast that drives the biotrophic-to-necrotrophic transition, and they demonstrate an effective strategy for engineering chloroplast-targeted defence mechanisms against M. oryzae.