Two histidine kinases can sense different stress cues for activation of the MAPK Hog1 in a fungal insect pathogen.

Filamentous fungi possess a large family of histidine kinases (HKs) classified to 11 distinct groups. Of those, only Group III (HK3) homologues in some fungi can sense osmotic, fungicidal and/or oxidative cues upstream of the signalling MAPK Hog1 cascade that usually governs two hallmark phenotypes, i.e., osmotolerance and dicarboximide/phenylpyrrole fungicide resistance. Here we examined functions of all eight HK groups with each possessing a single member in Beauveria bassiana. HK3 and HK8 (Group VIII) were evidently localized at hyphal cell periphery and had more functions in aerial conidiation and multiple stress responses than six other HKs. Increased osmosensitivity occurred uniquely in Δhk8 while high resistance to fludioxonil (phenylpyrrole) or iprodione (dicarboximide) fungicide appeared only in Δhk3. Phosphorylation of Hog1 was inhibited only in the Δhk3 cells triggered with fludioxonil cue and reduced only in the Δhk8 cells triggered with osmotic cue. However, an oxidative cue resulted in no signal change of phosphorylated Hog1 in either Δhk3 or Δhk8. Other Δhk mutants showed minor changes in some non-hallmark phenotypes. Altogether, HK3 and HK8 act as unique sensors of fungicidal and hyperosmotic cues respectively, upstream of the Hog1 cascade that regulates fungicidal resistance negatively and osmotolerance positively in B. bassiana.