Genome-Wide Characterization of PX Domain-Containing Proteins Involved in Membrane Trafficking-Dependent Growth and Pathogenicity of Fusarium graminearum

• Published in: mBio 2021-12, Vol.12 (6), p.e0232421-e0232421
• Main Authors: Lou, Yi, Zhang, Jing, Wang, Guanghui, Fang, Wenqin, Wang, Shumin, Abubakar, Yakubu Saddeeq, Zhou, Jie, Wang, Zonghua, Zheng, Wenhui
• Format: Article
• Language: English
• Subjects: Endoplasmic Reticulum - microbiology; FgBem1; Fungal Proteins - chemistry; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fusarium - genetics; Fusarium - growth & development; Fusarium - metabolism; Fusarium - pathogenicity; Fusarium graminearum; Gene Expression Regulation, Fungal; Genome, Fungal; Intracellular Membranes - microbiology; Microbial Pathogenesis; pathogenicity; Plant Diseases - microbiology; Protein Domains; Protein Transport; PX domain; Research Article; septum development; Trichothecenes - metabolism; Vacuoles - microbiology; Virulence
• ISSN: 2150-7511; 2150-7511
• DOI: 10.1128/mBio.02324-21

The Phox homology (PX) domain is a membrane recruitment module that binds to phosphoinositides (PI) mediating the selective sorting and transport of transmembrane proteins, lipids, and other critical cargo molecules via membrane trafficking processes. However, the mechanism of vesicular trafficking mediated by PX domain-containing proteins in phytopathogenic fungi and how this relates to the fungal development and pathogenicity remain unclear. Here, we systematically identified and characterized the functions of PX domain-containing proteins in the plant fungal pathogen Fusarium graminearum. Our data identified 14 PX domain-containing proteins in F. graminearum, all of which were required for plant infection and deoxynivalenol (DON) production, with the exception of FgMvp1 and FgYkr078. Furthermore, all the PX domain-containing proteins showed distinct localization patterns that were limited to the endosomes, vacuolar membrane, endoplasmic reticulum, cytoplasm, and hyphal septa/tips. Remarkably, among these proteins, FgBem1 targeted to surface crescent and septal pores and was retained at the septum pores even after actin constriction during septum development. Further analyses demonstrated that the surface crescent targeting of FgBem1 solely depended on its SH3 domains, while its septum and apex anchoring localization relied on its PX domain, which was also indispensable for reactive oxygen species (ROS) production, sexual development, and pathogenicity in F. graminearum. In summary, our study is the first detailed and comprehensive functional analysis of PX domain-containing proteins in filamentous fungi, and it provides new insight into the mechanism of FgBem1 involved in septum and apex anchorage mediated by its PX domain, which is necessary for sexual development and pathogenicity of F. graminearum. Fusarium head blight (FHB), caused predominantly by Fusarium graminearum, is an economically devastating disease of a wide range of cereal crops. Our previous study identified F. graminearum Vps17, Vps5, Snx41, and Snx4 as PX domain-containing proteins that were involved in membrane trafficking mediating the fungal development and pathogenicity, but the identity and biological roles of the remaining members of this protein family remain unknown in this model phytopathogen. In this study, we first unveiled all the PX domain-containing proteins in F. graminearum and then established their subcellular localizations and biological functions in relation to the