The Gß-like protein Bcgbl1 regulates development and pathogenicity of the gray mold Botrytis cinerea via modulating two MAP kinase signaling pathways

Authors: TANG, JIEJING - Huazhong Agricultural University; SUI, ZHE - Huazhong Agricultural University; LI, RONGHUI - Huazhong Agricultural University; XU, YUPING - Huazhong Agricultural University; WU, MINGDE - Huazhong Agricultural University; ZHANG, JING - Huazhong Agricultural University; Chen, Weidong; WEI, YANGDOU - University Of Saskatchewan; LI, GUOQING - Huazhong Agricultural University; YANG, LONG - Huazhong Agricultural University

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/17/2023
Publication Date: 12/4/2023
Citation: Tang, J., Sui, Z., Li, R., Xu, Y., Wu, M., Zhang, J., Chen, W., Wei, Y., Li, G., Yang, L. 2023. The Gß-like protein Bcgbl1 regulates development and pathogenicity of the gray mold Botrytis cinerea via modulating two MAP kinase signaling pathways. PLoS Pathogens. 19(12): e1011839. https://doi.org/10.1371/journal.ppat.1011839.
DOI: https://doi.org/10.1371/journal.ppat.1011839

Interpretive Summary: The fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea are necrotrophic and have broad host range, causing significant economical loses on many important crops. Despite intensive investigations on the biology and pathogenesis of these pathogens, the regulatory mechanisms of a special protein, the Gß-like protein, in the biology and pathogenicity are still not understood. The Gß-like protein is known to be involved in various biological processes, such as mycelial growth, differentiation, conidiation, stress responses, and infection. Using specific gene-deletion techniques, this study demonstrates that the Gß-like protein gene Bcgbl1 in Botrytis cinerea plays a pivotal role in development and pathogenesis by regulating the MAPK signaling pathways. Mutants without the Bcgbl1 gene were abnormal in many biological traits such as mycelial growth, sclerotial formation, conidiation, conidial morphogenesis, adhesion, infection cushion, and appressorium-like structure formation, resulting in loss of virulence. Furthermore, the protein Bcgbl1 was associated with another protein BcSte50, the adapter protein of MAPK cascade. The Gß-like protein gene also affected expression of several virulence genes. Overall, these findings systematically clarify Bcgbl1 functions and provide novel insight into regulatory pathway of how the Bcgbl1-protein functions in fungi in general and in fungal pathogenesis in particular.

Technical Abstract: In fungi, the Gß-like protein is involved in various biological processes, such as mycelial growth, differentiation, conidiation, stress responses, and infection. However, regulatory mechanisms of the Gß-like protein in regulating fungal development and pathogenesis are largely unknown. Here, we show that the Gß-like protein gene Bcgbl1 in the gray mold fungus Botrytis cinerea plays a pivotal role in development and pathogenesis by regulating the MAPK signaling pathways. The Bcgbl1 deletion mutants were defective in mycelial growth, sclerotial formation, conidiation, conidial morphogenesis, adhesion, infection cushion, and appressorium-like structure formation, resulting in loss of virulence. Deletion of Bcgbl1 did not affect intracellular cAMP level, and exogenous cAMP could not restore the defects, indicating that Bcgbl1 is dispensable for cAMP signaling in B. cinerea. Furthermore, Bcgbl1 interacted with BcSte50, the adapter protein of MAPK cascade, and Bcgbl1 mutants had reduced phosphorylation levels of Bmp1 and Bmp3. These results suggested that Bcgbl1 is involved in the Bmp1 and Bmp3 pathways. In addition, Bcgbl1 mutants also exhibited defects in cell wall and oxidative stress tolerance. Transcriptional profiling revealed that several virulence genes were significantly down-regulated in the Bcgbl1 mutant. Moreover, three hydrophobic surface binding proteins (HsbAs) acting downstream of the Bcgbl1-Bmp1-BcSte12 signaling pathway, were found to contribute to the adhesion and virulence of B. cinerea. Overall, these findings systematically clarify Bcgbl1 functions and provide novel insight into Bcgbl1-mediated Bmp1-BcSte12-BcHsbAs regulatory pathway in regulating fungal pathogenesis.