Metarhizium acridum transcription factor MaFTF1 negatively regulates virulence of the entomopathogenic fungus by controlling cuticle penetration of locusts

Abstract BACKGROUND The entomopathogenic fungus (EPF) Metarhizium acridum , a typical filamentous fungus, has been utilized for the biological control of migratory locusts ( Locusta migratoria manilensis ). Fungal‐specific transcription factors (TFs) play a crucial role in governing various cellular processes in fungi, although TFs with only the Fungal_trans domain remain poorly understood. RESULTS In this study, we identified a unique fungal‐specific TF in M. acridum , named MaFTF1, which contains only a Fungal_trans domain and functions as a negative regulator of M. acridum virulence by influencing cuticle penetration. The virulence of the MaFTF1 knockout strain (Δ MaFTF1 ) against L. migratoria was increased, with a median lethal time (LT 50 ) ~0.91 days shorter than that of the wild‐type (WT) strain when inoculated topically, mimicking natural infection conditions. Correspondingly, Δ MaFTF1 penetrated the cuticle earlier than did the WT strain. Our investigation revealed that the development of appressoria was accelerated in Δ MaFTF1 compared with the WT strain. Furthermore, the appressoria of the Δ MaFTF1 displayed higher turgor pressure and an upregulated expression of fungal hydrolases active toward the insect cuticle. RNA sequencing analysis indicated that the differences in appressorium behavior between the strains were due to MaFTF1 regulating a complex metabolism pathway. CONCLUSION This study revealed that MaFTF1 acts as a negative regulator of virulence, impacting the process of cuticle penetration by slowing the formation of appressoria, decreasing their turgor pressure, and reducing the expression of hydrolases in appressoria, revealing an unexpected strategy in the EPFs. © 2024 Society of Chemical Industry.