Abstract

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 Spitzenkörper (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.

Highlights

  • Magnaporthe oryzae is a filamentous fungus and the causal agent of rice blast disease

  • 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 accumulated at the narrow penetration site where the hypha invaded the plant cell

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Summary

Introduction

Magnaporthe oryzae is a filamentous fungus and the causal agent of rice blast disease. Hyphae generally extend by tip growth [5, 6]. This process is thought to be associated with the polarized trafficking of secretory vesicles to the Spitzenkorper (Spk), the organizing center for hyphal growth and development [7]. The exocyst complex in M. oryzae is located at the hyphal tip, ahead of the Spk, indicating that a successive protein secretion pathway is required for fungal infection [12]. Even though the Spk plays critical roles in the development and pathogenesis of filamentous fungi, how the Spk is maintained and moves in a polar manner in fungal cells is not well understood

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