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

Abstract

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.

Molecular basis and regulatory mechanisms underlying fungal insecticides' resistance to solar ultraviolet irradiation

“…The remaining genes contribute 12–32% based on reduced LD 50 in the absence of each 117–124 . However, UVB LD 50 increased markedly by 18–23% in the absence of each of three other genes encoding the phosphatase Cdc25 120 and the histidine kinases HK6 (group VI) and HK10 (group X) in B. bassiana , 96 suggesting negative roles in fungal UV resistance akin to those mentioned in the TRX‐TRR and GRX‐GLR systems.…”

“…Among heat‐shock protein (HSP) genes elucidated in B. bassiana , single‐gene deletions of two HSP40 (Ma5 and Mdj1), four HSP70 family members (Lsh1 and Hsp70c/d/e), and one HSF (heat‐shock transcription factor) domain‐containing protein (Skn7) led to 15–33% reductions in conidial UVB resistance 88–91 . The UVB LD 50 estimates were lowered by 16–42% in the disruption mutants of ten genes that function in, upstream or downstream of the MAPK Hog1 pathway required for cellular responses to high osmolarity and other stress cues in B. bassiana 92–97 . Among those, interestingly, Group III histidine kinase (HK3) acting as a signal sensor of fungicidal (fludioxonil) signal contributed much more to the UVB resistance of B. bassiana (41%) 96 than of M. robertsii (only 6%) 98 .…”

“…The UVB LD 50 estimates were lowered by 16–42% in the disruption mutants of ten genes that function in, upstream or downstream of the MAPK Hog1 pathway required for cellular responses to high osmolarity and other stress cues in B. bassiana 92–97 . Among those, interestingly, Group III histidine kinase (HK3) acting as a signal sensor of fungicidal (fludioxonil) signal contributed much more to the UVB resistance of B. bassiana (41%) 96 than of M. robertsii (only 6%) 98 . In another study, the key transcription factor Msn2 downstream of the Hog1 pathway was found to regulate ~3% more genes under oxidative stress, but ~12% fewer genes under heat shock, at the genomic level of B. bassiana than of M. robertsii 93 .…”

The DUF1996 and WSC domain‐containing protein Wsc1I acts as a novel sensor of multiple stress cues in Beauveria bassiana

“…This speculation is validated by our Western blot experiments. Although expression levels were similar in all tested strains, phosphorylation level of (group VIII HK) to sense fungicidal (fludioxonil) and hyperosmotic cues, respectively (Liu, Tong, Qiu, Ying, & Feng, 2017). Previously, WSC proteins with an N-terminal WSC domain and a TMD were shown to FIGURE 4 Influences of Wsc1I deletion on cuticular infectivity, virulence, and related cellular events of Beauveria bassiana.…”

“…The attenuated Hog1 phosphorylation unveils for the first time an essential role of Wsc1I in activation of the HOG pathway by sensing the stress cues of high osmolarity, oxidation, and cell wall perturbation likely due to its cell periphery localization determined by the WSC domain. To date, only two sensors have been found to act upstream of the Hog1 cascade in B. bassiana , namely, HK3 and HK8 (group VIII HK) to sense fungicidal (fludioxonil) and hyperosmotic cues, respectively (Liu, Tong, Qiu, Ying, & Feng, ). Previously, WSC proteins with an N‐terminal WSC domain and a TMD were shown to function in sensing stress cues upstream of the CWI pathway in S. cerevisiae (Maddi, Dettman, Fu, Seiler, & Free, ) or serve as methanol sensors in Pichia pastoris (Ohsawa, Yurimoto, & Sakai, ; Wilk, Wittland, Thywissen, Schmitz, & Heinisch, ).…”