The 24-kDa subunit of mitochondrial complex I regulates growth, microsclerotia development, stress tolerance, and virulence in Verticillium dahliae

Authors: LI, HUAN - Chinese Academy Of Agricultural Sciences; LIU, YING - Nanjing Forestry University; WANG, DAN - Zhejiang A & F University; WANG, YA-HONG - Nanjing Forestry University; SHENG, RUO-CHENG - Chinese Academy Of Agricultural Sciences; KONG, ZHIQIANG - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences; SUBBARAO, KRISHNA - University Of California; CHEN, FENG-MAO - Nanjing Forestry University; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/29/2024
Publication Date: 12/18/2024
Citation: Li, H., Liu, Y., Wang, D., Wang, Y.H., Sheng, R.C., Kong, Z.Q., Klosterman, S.J., Chen, J.Y., Subbarao, K.V., Chen, F.M., Zhang, D.D. 2024. The 24-kDa subunit of mitochondrial complex I regulates growth, microsclerotia development, stress tolerance, and virulence in Verticillium dahliae. BMC Biology. 22. Article 289. https://doi.org/10.1186/s12915-024-02084-9.
DOI: https://doi.org/10.1186/s12915-024-02084-9

Interpretive Summary: Verticillium dahliae is a soilborne plant pathogenic fungus and a cause of Verticillium wilt diseases of plants. Verticillium dahliae causes disease on over 200 plant species worldwide, including many agriculturally important crops. In addition to having a very broad host range, one of the reasons that V. dahliae is so difficult to control is because the fungus produces pigmented (melanized) resting structures that can survive in the soil for years. In this study, we examined the role of a mitochondrial gene of V. dahliae in pathogenicity, response to stress, and microsclerotia production. This gene product, named VdNuo1, is localized in the mitochondria and is involved in energy production and metabolism. VdNuo1 was deleted in V. dahliae and analyses of the VdNuo1 mutant strain revealed that it is necessary in resistance to stress, hyphal growth, and melanized microsclerotia development. Furthermore the strain displayed reduced virulence. Insights into the genes necessary for resistance to stress and pigment synthesis and microsclerotia formation in V. dahliae may lead to alternative control approaches to combat this fungus in the soil.

Technical Abstract: The complete mitochondrial respiratory chain is a precondition for maintaining cellular energy supply, development, and metabolic balance. Due to the evolutionary differentiation of complexes and the semi-autonomy of mitochondria, respiratory chain subunits have become critical targets for crop improvement and fungal control. In fungi, mitochondrial complex I mediates growth and metabolism. However, the role of this complex in the pathogenesis of phytopathogenic fungi is largely unknown. In this study, we identified the NADH: ubiquinone oxidoreductase 24-kDa subunit (VdNuo1) of complex in vascular wilt pathogen, Verticillium dahliae, and examined its functional conservation in phytopathogenic fungi. Based on the treatments with respiratory chain inhibitors, the mitochondria-localized VdNuo1 was confirmed to regulate mitochondrial morphogenesis and homeostasis. VdNuo1 was induced during the different developmental stages in V. dahliae, including hyphal growth, conidiation, and melanized microsclerotia development. The VdNuo1 mutants displayed variable sensitivity to stress factors and decreased pathogenicity in multiple hosts, indicating that VdNuo1 is necessary in stress tolerance and full virulence. Comparative transcriptome analysis demonstrated that VdNuo1 mediates global transcriptional effects, including oxidation and reduction processes, fatty acid, sugar, and energy metabolism. These defects are partly attributed to impairments of mitochondrial morphological integrity, complex assembly, and related functions. Its homologue (CgNuo1) functions in the vegetative growth, melanin biosynthesis, and pathogenicity of Colletotrichum gloeosporioides; however, CgNuo1 does not restore the VdNuo1 mutant to normal phenotypes. Our results revealed that VdNuo1 plays important roles in growth, metabolism, microsclerotia development, stress tolerance, and virulence of V. dahliae, sharing novel insight into the function of complex I and a potential fungicide target for pathogenic fungi.