Li Huan, Sheng Ruo-Cheng, Wang Ya-Hong, Zhang Chen-Ning, Wang Dan, Klosterman Steven J, Zhang Dan-Dan, Subbarao Krishna V, Chen Feng-Mao, Chen Jie-Yin
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China.
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
Mol Plant Pathol. 2025 Sep;26(9):e70149. doi: 10.1111/mpp.70149.
During oxidative phosphorylation, the leaked electrons generate superoxide anions to attack the mitochondrial inner membrane and impair mitochondrial activity. Three superoxide dismutases (SODs) are secreted to degrade host superoxide anions in Verticillium dahliae. However, the roles of mitochondrial SODs (mtSODs) in superoxide anion detoxification and in virulence are unknown in this fungus. We had previously shown that complex I VdNuo1 subunit mediates multiple biological functions and mitochondrial morphogenesis in V. dahliae. Here, we demonstrate that among the seven VdSODs of V. dahliae, only VdSOD2 and VdSOD4 were localised in the mitochondria and interact directly with VdNuo1. The VdNuo1 mutants, which exhibited mitochondrial inactivation in response to the superoxide anion inducer menadione, also displayed aberrant VdSODs transcription and SOD activity. VdSOD2 acted as a positive regulator of mitochondrial superoxide anion detoxification, and thus, its overexpression rescued the menadione-sensitive phenotypes of VdNuo1 mutants. In contrast, the increased tolerance of VdSOD2/VdSOD4 double mutants highlights that VdSOD4 negatively affects superoxide anion degradation. Thus, VdSOD2 and VdSOD4 cooperate with VdNuo1 to maintain SOD homeostasis for growth, mitochondrial superoxide anion detoxification, and virulence in V. dahliae. The two active superoxide anion scavengers CgSOD2 and CgSOD4 shared the same localisation and interaction model with CgNuo1 in Colletotrichum gloeosporioides. These results not only demonstrate the roles of mtSODs in V. dahliae and a novel conserved mechanism in which the respiratory chain couples with mtSODs to regulate superoxide anion metabolism in filamentous fungi, but also provide insights for the development of multisite fungicides to control phytopathogenic pathogens.
在氧化磷酸化过程中，泄漏的电子会产生超氧阴离子，攻击线粒体内膜并损害线粒体活性。大丽轮枝菌分泌三种超氧化物歧化酶（SOD）来降解宿主超氧阴离子。然而，线粒体SOD（mtSOD）在该真菌中超氧阴离子解毒和毒力方面的作用尚不清楚。我们之前已经表明，复合体I的VdNuo1亚基介导大丽轮枝菌的多种生物学功能和线粒体形态发生。在这里，我们证明，在大丽轮枝菌的七种VdSOD中，只有VdSOD2和VdSOD4定位于线粒体，并直接与VdNuo1相互作用。VdNuo1突变体在超氧阴离子诱导剂甲萘醌作用下表现出线粒体失活，同时也表现出异常的VdSOD转录和SOD活性。VdSOD2作为线粒体超氧阴离子解毒的正调控因子，因此，其过表达挽救了VdNuo1突变体对甲萘醌敏感的表型。相反，VdSOD2/VdSOD4双突变体耐受性的增加表明VdSOD4对超氧阴离子降解有负面影响。因此，VdSOD2和VdSOD4与VdNuo1协同作用，维持SOD稳态，以促进大丽轮枝菌的生长、线粒体超氧阴离子解毒和毒力。两种活性超氧阴离子清除剂CgSOD2和CgSOD4在胶孢炭疽菌中与CgNuo1具有相同的定位和相互作用模式。这些结果不仅证明了mtSOD在大丽轮枝菌中的作用以及呼吸链与mtSOD耦合以调节丝状真菌中超氧阴离子代谢的一种新的保守机制，而且为开发多靶点杀菌剂来控制植物病原真菌提供了思路。
