Magnaporthe oryzae fimbrin organizes actin networks in the hyphal tip during polar growth and pathogenesis.

Author summary The actin cytoskeleton plays crucial roles in M. oryzae growth and pathogenesis. However, the organizing principles and dynamic behavior of the cytoskeleton in M. oryzae growth and expansion in plant cells remain enigmatic. In this study, through super-resolution observation, we found a dense network of actin cables dynamically gathered near the Spitzenkorper, the organizing center for hyphal growth and development. The actin cytoskeleton also accumulated at the narrow penetration site where the hypha invaded the plant cell. Furthermore, the actin cross-linking protein MoFim1 contributes to organizing these actin cables, thus facilitating hyphal polarity, vesicle transport, and invasive expansion of hyphae in the host plant cell. In all, our results uncovered a mechanism by which M. oryzae organizes and relies on a unique actin distribution pattern in hyphae during cell growth and pathogenesis. Magnaporthe oryzae causes rice blast disease, but little is known about the dynamic restructuring of the actin cytoskeleton during its polarized tip growth and pathogenesis. Here, we used super-resolution live-cell imaging to investigate the dynamic organization of the actin cytoskeleton in M. oryzae during hyphal tip growth and pathogenesis. We observed a dense actin network at the apical region of the hyphae and actin filaments originating from the Spitzenkorper (Spk, the organizing center for hyphal growth and development) that formed branched actin bundles radiating to the cell membrane. The actin cross-linking protein Fimbrin (MoFim1) helps organize this actin distribution. MoFim1 localizes to the actin at the subapical collar, the actin bundles, and actin at the Spk. Knockout of MoFim1 resulted in impaired Spk maintenance and reduced actin bundle formation, preventing polar growth, vesicle transport, and the expansion of hyphae in plant cells. Finally, transgenic rice (Oryza sativa) expressing RNA hairpins targeting MoFim1 exhibited improved resistance to M. oryzae infection, indicating that MoFim1 represents an excellent candidate for M. oryzae control. These results reveal the dynamics of actin assembly in M. oryzae during hyphal tip development and pathogenesis, and they suggest a mechanism in which MoFim1 organizes such actin networks.