Metarhizium robertsii is a versatile fungus with multifactorial lifestyles, and it is an emerging fungal model for investigating the mechanisms of multiple lifestyle transitions that involve trans-kingdom host jumping. Penetration of the insect cuticle is the necessary step for the transition from saprophytic or symbiotic to pathogenic lifestyle. Previously, we found the transcription factor AFTF1 plays an important role in cuticle penetration, which is precisely regulated by Fus3-MAPK, Slt2-MAPK, and the membrane protein Mr-OPY2. Here, we identified a transcription factor (MrSt12) that directly regulated the transcription of Aftf1 by physically interacting with the cis-acting element (ATGAAACA) in the promoter of Aftf1. The deletion mutant of MrSt12 failed to form the infection structure appressorium and was thus nonpathogenic. We further found that the regulation of Aftf1 by MrSt12 was directly controlled by the Fus3-MAPK. In conclusion, we found a new signaling cascade containing Fus3-MAPK, MrSt12, and AFTF1, which regulates cuticle penetration by M. robertsii.
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