Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus.

IMPORTANCE: The interplay between plant and pathogen is a dynamic process, with the host's innate defense mechanisms serving a crucial role in preventing infection. In response to many plant pathogen infections, host cells generate the key regulatory molecule, reactive oxygen species (ROS), to limit the spread of the invading organism. In this study, we reveal the effects of fungal peroxisome dynamics on host ROS homeostasis, during the rice blast fungus Magnaporthe oryzae infection. The elongation of the peroxisome appears contingent upon ROS and links to the accumulation of ROS within the host and the infectious growth of the pathogen. Importantly, we identify a peroxisomal 3-ketoacyl-CoA thiolase, MoKat2, responsible for the elongation of the peroxisome during the infection. In response to host-derived ROS, the homodimer of MoKat2 undergoes dissociation to bind peroxisome membranes for peroxisome elongation. This process, in turn, inhibits the accumulation of host ROS, which is necessary for successful infection. Overall, our study is the first to highlight the intricate relationship between fungal organelle dynamics and ROS-mediated host immunity, extending the fundamental knowledge of pathogen-host interaction.

The Peroxisomal-CoA Synthetase MoPcs60 Is Important for Fatty Acid Metabolism and Infectious Growth of the Rice Blast Fungus.

Fatty acid metabolism is important for the maintenance of fatty acid homeostasis. Free fatty acids, which are toxic in excess, are activated by esterification with coenzyme A (CoA) and then subjected to ß-oxidization. Fatty acid ß-oxidation-related genes play critical roles in the development and virulence of several phytopathogens. In this study, we identified and characterized a peroxisomal-CoA synthetase in the rice blast fungus Magnaporthe oryzae, MoPCS60, which is a homolog of PCS60 in budding yeast. MoPCS60 was highly expressed during the conidial and early infectious stages and was induced under oleate treatment. Targeted deletion of MoPCS60 resulted in a significant reduction in growth rate when oleate and olive oil were used as the sole carbon sources. Compared with the wild-type strain Guy11, the ΔMopcs60 mutant exhibited fewer peroxisomes, more lipid droplets, and decreased pathogenicity. The distribution of MoPcs60 varied among developmental stages and was mainly localized to peroxisomes in the hyphae, conidia, and appressoria when treated with oleate. Our results suggest that MoPcs60 is a key peroxisomal-CoA synthetase involved in fatty acid ß-oxidation and pathogenicity in rice blast fungi.