Microsclerotia (MS) are highly sturdy and stable dormant structures produced by most filamentous fungi in response to various adversities. Owing to the robust regeneration, MS are also considered an ideal succedaneum to insecticidal conidia for entomopathogenic fungi application. Iron plays a regulatory role in the formation of MS, as reactive oxygen species (ROS) generated under conditions of iron overload are critically involved in driving this process. To explore the regulatory role of iron in the formation and virulence of MS in Metarhizium rileyi, functional analyses were conducted on two homologs of vacuolar iron transporter-like coding genes, designated MrCcc1 and MrCcc2, through expression analysis, gene knockout, phenotypic characterization, and toxicity assessment. Here we show that the expression of MrCcc1 and MrCcc2 is induced by iron, and that gene disruption of MrCcc1, but not MrCcc2, leads to reduced tolerance to multiple metal salts. MrCcc2 likely serves as a compensatory component, fulfilling the role typically performed by MrCcc1. Most importantly, all the deletion variants exhibited not only a significant reduction in MS production yield but also a decrease in viability, leading to impaired germination, growth, conidia production upon rehydration, and even conidial insecticidal activity against Spodoptera litura larvae. Our findings suggest that the vacuolar iron transporters MrCcc1 and MrCcc2 in M. rileyi function as positive regulators of fungal growth and reproduction, as well as of MS yield and activity. These findings highlight the importance of normal iron metabolism, as well as the critical role of iron-induced ROS in the formation of MS-based insecticides, and provide molecular targets for the engineered development of highly virulent strains.
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