Small GTPase Rab7-mediated FgAtg9 trafficking is essential for autophagy-dependent development and pathogenicity in Fusarium graminearum

Zheng, Huawei; Miao, Pengfei; Lin, Xiaolian; Li, Lingping; Wu, Congxian; Chen, Xiaomin; Abubakar, Yakubu Saddeeq; Norvienyeku, Justice; Li, Guangpu; Zhou, Jie; Wang, Zonghua; Zheng, Wenhui

doi:10.1371/journal.pgen.1007546

Cited by 46 publications

(28 citation statements)

References 66 publications

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“…In addition, the Δ Folvps9 mutant has defects in the trafficking and degradation of autophagosomes. Several Rab proteins were well-known mediators of vesicle trafficking and involved in regulation of autophagy (Liu et al, 2015; Zheng et al, 2018b). For example, Rab5 plays roles in vesicle trafficking, cargo recycling and maturation of early endosomes and is involved in membrane fusion events.…”

Section: Discussionmentioning

confidence: 99%

FolVps9, a Guanine Nucleotide Exchange Factor for FolVps21, Is Essential for Fungal Development and Pathogenicity in Fusarium oxysporum f. sp. lycopersici

Mao

Zhang

et al. 2019

Front. Microbiol.

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The soil-borne, asexual fungus Fusarium oxysporum f.sp. lycopersici (Fol) is the causal agent of tomato wilt disease. Autophagy plays a crucial role in the development and virulence of Fol. The Fol endosomal system is highly dynamic and has been shown to be associated with conidiogenesis and pathogenicity. Rab GTPases and the regulators are highly conserved in regulating autophagy and endocytosis in most eukaryotes. Identification and characterization of additional Rab regulators in fungal pathogens should facilitate the understanding of the autophagy and endocytosis in different filamentous fungi. Here, we have identified and characterized the yeast VPS9 homolog FolVPS9 in Fol. Targeted gene deletion showed that FolVPS9 is important for growth, conidiation and virulence in Fol. Cytological examination revealed that FolVps9 co-localized with FolVps21 (a marker of early endosome) and played a critical role in endocytosis and autophagosome degradation. Pull-down assays showed that FolVps9 interacted with FolVps21, which was also important for development and plant infection in Fol. Yeast two-hybrid, bimolecular fluorescence complementation and co-immunoprecipitation assays revealed that FolVps9 specifically interacts with the GDP-bound form of FolVps21. Furthermore, a constitutively active form of FolVps21 (Q72L) was able to rescue defects of ΔFolvps9 and ΔFolvps21 mutants. In summary, our study provides solid evidence that FolVps9 acts as a FolVps21 guanine nucleotide exchange factor (GEFs) to modulate endocytosis and autophagy, thereby controlling vegetative growth, asexual development and pathogenicity in Fol.

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Section: Discussionmentioning

confidence: 99%

FolVps9, a Guanine Nucleotide Exchange Factor for FolVps21, Is Essential for Fungal Development and Pathogenicity in Fusarium oxysporum f. sp. lycopersici

Mao

Zhang

et al. 2019

Front. Microbiol.

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“…A recent study shows that FgMon1, a FgRab7 GEF, regulates vacuolar fusion, autophagy and plant infection (Li et al, ). Rab7‐mediated FgAtg9 trafficking is essential for autophagy‐dependent development and pathogenicity in F. graminearum (Zheng et al, ). Identification and characterization of additional Rab regulators in fungal pathogens should provide more information on the organization of membrane traffic, pathogenesis and the regulation of Rabs unique to these filamentous fungi.…”

Section: Introductionmentioning

confidence: 99%

FgSec2A, a guanine nucleotide exchange factor of FgRab8, is important for polarized growth, pathogenicity and deoxynivalenol production in Fusarium graminearum

Zheng

Miao

et al. 2018

Environmental Microbiology

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Sec4/Rab8 is one of the well-studied members of the Rab GTPase family, previous studies have shown that Sec4/Rab8 crucially promotes the pathogenesis of phytopathogens, but the upstream regulators of Rab8 are still unknown. Here, we have identified two Sec2 homologues FgSec2A and FgSec2B in devastating fungal pathogen Fusarium graminearum and investigated their functions and interactions with FgRab8 by live-cell imaging, genetic and functional analyses. Yeast two-hybrid assay shows that FgSec2A specifically interacts with FgRab8DN(N123I) and itself. Importantly, FgSec2A is required for growth, conidiation, DON production and virulence of F. graminearum. Live-cell imaging shows that FgSec2A and FgSec2B are both localized to the tip region of hyphae and conidia. Both N-terminal region and Sec2 domain of FgSec2A are essential for its function, but not for localization, whereas the C-terminal region is important for its polarized localization. Furthermore, constitutively active FgRab8CA(Q69L) partially rescues the defects of ΔFgsec2A. Consistently, FgSec2A is required for the polarized localization of FgRab8. Finally, FgSec2A and FgSec2B show partial functions, but FgSec2A does not interact and co-localize with FgSec2B. Taken together, these results indicate that FgSec2A acts as a FgRab8 guanine nucleotide exchange factor and is necessary for polarized growth, DON production and pathogenicity in F. graminearum.

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“…In recent years, autophagy has been found to be associated with endocytosis, and same proteins function in both processes. Vesicle-trafficking-related proteins Rab5/Vps21, FgRab7, and its GEF FgMon1 are involved in both autophagic pathway and endocytosis in S. cerevisiae and F. graminearum , respectively ( Singer-Kruger et al, 1994 ; Chen et al, 2014 ; Li et al, 2015 ; Zheng et al, 2015 , 2018b ). In addition, deletion of VPS9 in P. oryzae and Fol seriously disrupted fungal growth and pathogenicity by blocking autophagic and endocytic processes ( Zhu et al, 2018 ; Li et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

FgVps9, a Rab5 GEF, Is Critical for DON Biosynthesis and Pathogenicity in Fusarium graminearum

Yang

Zhang

et al. 2020

Front. Microbiol.

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Rab GTPases play an important role in vesicle-mediated membrane trafficking in eukaryotes. Previous studies have demonstrated that deletion of RAB5/VPS21 reduces endocytosis and virulence of fungal phytopathogens in their host plants. However, Rab5 GTPase cycle regulators have not been characterized in Fusarium graminearum, the causal agent of Fusarium head blight (FHB) or head scab disease in cereal crops. In this study, we have identified and characterized a Rab5 guanine nucleotide exchange factor (GEF), the Vps9 homolog FgVps9, in F. graminearum. Yeast two hybrid (Y2H) assays have shown that FgVps9 specifically interacts with the guanosine diphosphate (GDP)bound (inactive) forms of FgRab51 and FgRab52, the Rab5 isoforms in F. graminearum. Deletion of FgVPS9 shows impaired fungal growth and conidiation. Pathogenicity assays indicate that deletion of FgVPS9 can significantly decrease the virulence of F. graminearum in wheat. Cytological analyses have indicated that FgVps9 colocalizes with FgRab51 and FgRab52 on early endosomes and regulates endocytosis and autophagy processes. Gene expression and cytological examination have shown that FgVps9 and FgRab51 or FgRab52 function in concert to control deoxynivalenol (DON) biosynthesis by regulating the expression of trichothecene biosynthesis-related genes and toxisome biogenesis. Taken together, FgVps9 functions as a GEF for FgRab51 and FgRab52 to regulate endocytosis, which, as a basic cellular function, has significant impact on the vegetative growth, asexual development, autophagy, DON production, and plant infection in F. graminearum.

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Small GTPase Rab7-mediated FgAtg9 trafficking is essential for autophagy-dependent development and pathogenicity in Fusarium graminearum

Cited by 46 publications

References 66 publications

FolVps9, a Guanine Nucleotide Exchange Factor for FolVps21, Is Essential for Fungal Development and Pathogenicity in Fusarium oxysporum f. sp. lycopersici

FolVps9, a Guanine Nucleotide Exchange Factor for FolVps21, Is Essential for Fungal Development and Pathogenicity in Fusarium oxysporum f. sp. lycopersici

FgSec2A, a guanine nucleotide exchange factor of FgRab8, is important for polarized growth, pathogenicity and deoxynivalenol production in Fusarium graminearum

FgVps9, a Rab5 GEF, Is Critical for DON Biosynthesis and Pathogenicity in Fusarium graminearum

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