CaSun1, a SUN family protein, governs the pathogenicity of Colletotrichum camelliae by recruiting CaAtg8 to promote mitophagy

Abstract

Camellia oleifera, a woody oilseed plant native to China, is highly susceptible to anthracnose, a fungal disease that poses a significant threat to its yield and quality. Mitophagy, a specialized form of autophagy that specifically targets dysfunctional mitochondria, is crucial for cellular homeostasis, stress response, and pathogenesis in fungi. The proteins that potentially participate in mitophagy in Colletotrichum camelliae were identified herein using immunoprecipitation-mass spectrometry (IP-MS) by screening for the potential protein interactors of the core autophagy-related protein, CaAtg8. Among the identified mitochondria-associated proteins, CaSun1 was selected for further investigation. Phenotypic analyses revealed that CaSun1 is a critical regulator of vegetative growth, conidiation, and pathogenicity. CaSun1 localized to the mitochondria, consistent with the conserved function of SUN family proteins. Notably, the findings revealed that CaSun1 was essential for mitophagy and colocalized with CaAtg8 during nitrogen starvation. Functional analyses demonstrated that CaSun1-mediated mitophagy is vital for the growth of invasive hyphae and pathogenicity in C. camelliae. In summary, our findings indicated that CaSun1 mediates mitophagy by facilitating the recruitment of CaAtg8 in C. camelliae, thereby contributing to the establishment of anthracnose. This study provided novel insights into the molecular mechanisms underlying the pathogenesis of fungal infections and identified a potential target for disease control.

Acknowledgements

This research was supported by the Zhejiang Provincial Natural Science Foundation of China (Grant no. LQ24C160010), the Agricultural Science and Technology Innovation Program, Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2023-ZFRI-03), and the ‘Pioneer’ and ‘Leading Goose’ R&D Program of Zhejiang (Grant no. 2023C02034). We are grateful for the editorial support provided by TopEdit (www.topeditsci.com) in terms of language use.

Author contributions

J.C. and C-L.L. planned and designed the research. S.M., S-F.C., and M.X. performed most experiments. L.W., L-J.C., and Y.C. analyzed the IP-MS data and measured the phenotype. S-J.J. provided the idea and revised the language. Y. S. prepared the necessary materials. S.M., S-F.C., and M.X. wrote and revised the manuscript.

Data availability

The data presented in this study are available in the article and in its online supplementary material.

Conflict of interest statement

The authors declare that there are no conflicts of interest related to this article.

Supplementary data

Supplementary data is available at Horticulture Research online.

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