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- Title
The Gβ-like protein Bcgbl1 regulates development and pathogenicity of the gray mold Botrytis cinerea via modulating two MAP kinase signaling pathways.
- Authors
Tang, Jiejing; Sui, Zhe; Li, Ronghui; Xu, Yuping; Xiang, Lixuan; Fu, Shiying; Wei, Jinfeng; Cai, Xuan; Wu, Mingde; Zhang, Jing; Chen, Weidong; Wei, Yangdou; Li, Guoqing; Yang, Long
- Abstract
The fungal Gβ-like protein has been reported to be involved in a variety of biological processes, such as mycelial growth, differentiation, conidiation, stress responses and infection. However, molecular mechanisms of the Gβ-like protein in regulating fungal development and pathogenicity are largely unknown. Here, we show that the Gβ-like protein gene Bcgbl1 in the gray mold fungus Botrytis cinerea plays a pivotal role in development and pathogenicity by regulating the mitogen-activated protein (MAP) kinases signaling pathways. The Bcgbl1 deletion mutants were defective in mycelial growth, sclerotial formation, conidiation, macroconidial morphogenesis, plant adhesion, and formation of infection cushions and appressorium-like structures, resulting in a complete loss of pathogenicity. Bcgbl1 interacted with BcSte50, the adapter protein of the cascade of MAP kinase (MAPK). Bcgbl1 mutants had reduced phosphorylation levels of two MAPKs, namely Bmp1 and Bmp3, thereby reducing infection. However, deletion of Bcgbl1 did not affect the intracellular cAMP level, and exogenous cAMP could not restore the defects. Moreover, Bcgbl1 mutants exhibited defects in cell wall integrity and oxidative stress tolerance. Transcriptional profiling revealed that Bcgbl1 plays a global role in regulation of gene expression upon hydrophobic surface induction. We further uncovered that three target genes encoding the hydrophobic surface binding proteins (HsbAs) contributed to the adhesion and virulence of B. cinerea. Overall, these findings suggest that Bcgbl1 had multiple functions and provided new insights for deciphering the Bcgbl1-mediated network for regulating development and pathogenicity of B. cinerea. Author summary: Botrytis cinerea is an important phytopathogenic fungus that causes severe diseases in over 1,400 plant species worldwide. It has been known that the Gβ-like protein plays an important role in fungal development and virulence. However, the regulatory network mediated by the Gβ-like protein and its downstream targets remain elusive. Here, we report that the Gβ-like protein Bcgbl1 is essential for development and pathogenicity of B. cinerea. We showed that the Bcgbl1 protein physically interacted with the MAPK adaptor protein Ste50 and activated two distinct MAPKs (Bmp1 and Bmp3) that regulate fungal adhesion to plant leaves and fungal cell wall integrity/oxidative response, respectively. Further RNA-seq analysis on the wild type and ΔBcgbl1 mutant incubated on the hydrophobic surface allowed identification of the potential downstream target genes, including three novel genes (BcHsbA1-3) for plant adhesion and virulence. Deletion of each individual BcHsbA gene resulted in decreased adhesion and invasion of B. cinerea on host leaf tissues, suggesting that three BcHsbA genes play an important role in fungal virulence. Taken together, this study advanced our understanding of the molecular mechanisms underlying the function of the Gβ-like protein in modulating development and pathogenicity.
- Subjects
MITOGEN-activated protein kinases; BOTRYTIS cinerea; FUNGAL proteins; CELLULAR signal transduction; FUNGICIDE resistance; FUNGAL virulence; GENE expression profiling; ADAPTOR proteins
- Publication
PLoS Pathogens, 2023, Vol 19, Issue 12, p1
- ISSN
1553-7366
- Publication type
Article
- DOI
10.1371/journal.ppat.1011839