Recycling of trans-Golgi SNAREs is essential for apoplastic effector secretion and effective pathogenicity of Magnaporthe oryzae
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Vesicle transport is an essential process that mediates the growth, development and virulence of pathogenic fungi. However, the intricate mechanisms underlying how vesicle transport regulates the secretion of effector proteins remain to be fully elucidated. Here, we unveiled a novel pathway in which retromer and trans-Golgi (TGN) SNARE proteins co-regulate the proper secretion of apoplastic effectors in the rice blast fungus Magnaporthe oryzae. A TGN-associated SNARE complex consisting of MoSnc1, MoTlg1, MoTlg2, and MoVti1 was found to be essential for growth, development and pathogenicity in the fungus. Moreover, the TGN-associated SNARE complex is indispensable for accurate secretion of apoplastic effectors. Furthermore, we have elucidated that the dynamin-like protein MoVps1, an upstream regulator of the retromer complex, regulates the fission of MoVps35-coated vesicle and the proper localization of the TGN-associated SNARE complex. Additionally, we employed prochlorperazine, which identified as a potent dynamin inhibitor, elicits a developmental response in M. oryzae akin to MoVPS1 disruption, highlighting the pivotal regulatory role of dynamin and its potential as a therapeutic target for rice blast disease management. In conclusion, the study uncovered a specific mechanism by which MoVps1 and the retromer complex regulate the positioning of TGN-associated SNARE proteins to effectively promote effector secretion. It provides a deeper understanding of the molecular mechanisms of effector secretion in fungi and underscores the importance of vesicle transport in fungal pathogenesis.
Importance
Vesicle transport is essential for pathogenic fungi as it controls the secretion of effectors that modulate interactions with the host and infection processes. The detailed mechanisms of effector secretion via vesicular pathways in these fungi are not yet fully understood. In this study, we have discovered a new regulatory pathway involving the retromer complex and trans-Golgi SNARE proteins that is critical for the proper secretion of apoplast effectors in M. oryzae. We have identified an important TGN-associated SNARE complex, consisting of MoSnc1, MoTlg1, MoTlg2 and MoVti1, which is required for the development and pathogenicity of M. oryzae. Our results emphasize the importance of this SNARE complex for the precise secretion of effectors into the apoplast, a key step in pathogenesis. Additionally, we demonstrated that the dynamin-like protein MoVps1, a protein acting upstream of the retromer complex, is vital for the correct localization of the TGN-associated SNARE complex. Furthermore, our research underscores the critical regulatory role of dynamin in M. oryzae pathogenesis, with prochlorperazine serving as an inhibitor that mimics the phenotypic effects of MoVps1 disruption, thereby highlighting its potential as a biopesticide candidate for rice blast disease management. Our study has uncovered a specific regulatory mechanism in which MoVps1 and the retromer complex control the positioning and function of TGN-associated SNARE proteins, thereby facilitating effector secretion. This work not only advances our understanding of the molecular basis of effector secretion in fungi, but also has implications for the development of novel strategies to control fungal diseases.
