Differential roles of three subclass III C6 transcription factors in the insect-pathogenic lifecycle of Beauveria bassiana.

Abstract

Six subclass III C6 transcription factors (TFs) with unique Zn(II)2Cys6 binuclear cluster DNA-binding (C6 or GAL4) domain not locating at N-terminus are underexplored in Beauveria bassiana, a wide-spectrum mycoinsecticide. Here, we report that three C6 TFs with the GAL4 domain locating at C-terminus (TF1), between C-terminal and central regions (TF2) and between central and N-terminal regions (TF3) are largely differentiated in function. TF1 was proven to localize in both nucleus and cytoplasm and regulate host immune repression in the course of host hemocoel colonization instead of cuticular penetration. The deletion of tf1 resulted in much greater virulence loss via normal cuticle infection (77%) than cuticle-bypassing infection (25%) for direct hemocoel colonization by intrahemocoel injection. The deletion also led to severe defects in radial growth, multiple stress tolerances, aerial conidiation, and submerged blastospore production as well as resistance to host immune defense after invasion into host hemocoel, unveiling pleiotropic effects of TF1 in the fungal lifecycle. TF3 was similar to TF1 in subcellular feature and exhibited lesser role than TF1 in mediating conidiation and blastospore production but no other role. TF2 looks like a typical subclass III C6 TF but proved functionally null perhaps due to its localization in neither nucleus nor cytoplasm under normal culture conditions. These findings add knowledge to subclass III C6 TFs and unveil a significance of host immune suppression for the insecticidal activity of B. bassiana after hyphal invasion into insect hemocoel through cuticular penetration.