Magnaporthe oryzae SMO1 encodes a Ras GTPase-activating protein required for spore morphology, appressorium function and rice blast disease

Abstract

The pathogenic life cycle of the rice blast fungus Magnaporthe oryzae involves a series of morphogenetic changes, essential for its ability to cause disease. The smo mutation was identified more than twenty-five years ago and affects the shape and development of diverse cell types in M. oryzae, including conidia, appressoria and asci. All attempts to clone the SMO1 gene by map-based cloning and/or complementation, have failed over many years. Here, we report the identification of SMO1 by a combination of bulk segregant analysis and comparative genome analysis. SMO1 encodes a GTPase-activating protein (GAP), which regulates Ras signalling during infection-related development. Targeted deletion of SMO1 results in abnormal, non-adherent conidia, impaired in their production of spore tip mucilage. Smo1 mutants also develop smaller appressoria, with a severely reduced capacity to infect rice plants. SMO1 is necessary for organisation of microtubules and for septin-dependent remodelling of the F-actin cytoskeleton at the appressorium pore. Smo1 physically interacts with components of the Ras2 signaling complex, and a range of other signalling and cytoskeletal components, including the four core septins. SMO1 is therefore necessary for regulation of RAS activation required for conidial morphogenesis and septin-mediated plant infection.