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Capping proteins regulate fungal development, DON-toxisome formation and virulence in Fusarium graminearum.

ABSTRACT: Deoxynivalenol (DON) is an important trichothecene mycotoxin produced by the cereal pathogen Fusarium graminearum. DON is synthesized in organized endoplasmic reticulum structures called toxisomes. However, the mechanism for toxisome formation and the components of toxisomes are not yet fully understood. In a previous study, we found that myosin I (FgMyo1)-actin cytoskeleton participated in toxisome formation. In the current study, we identified two new components of toxisomes, the actin capping proteins (CAPs) FgCapA and FgCapB. These two CAPs form a heterodimer in F. graminearum, and physically interact with FgMyo1 and Tri1. The deletion mutants ?FgcapA and ?FgcapB and the double deletion mutant ??FgcapA/B dramatically reduced hyphal growth, asexual and sexual reproduction and endocytosis. More importantly, the deletion mutants markedly disrupted toxisome formation and DON production, and attenuated virulence in planta. Collectively, these results suggest that the actin CAPs are associated with toxisome formation and contribute to the virulence and development of F. graminearum.

SUBMITTER: Tang G

PROVIDER: S-EPMC6988429 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Capping proteins regulate fungal development, DON-toxisome formation and virulence in Fusarium graminearum.

Tang Guangfei G Chen Ahai A Dawood Dawood H DH Liang Jingting J Chen Yun Y Ma Zhonghua Z

Molecular plant pathology 20191106 2

Deoxynivalenol (DON) is an important trichothecene mycotoxin produced by the cereal pathogen Fusarium graminearum. DON is synthesized in organized endoplasmic reticulum structures called toxisomes. However, the mechanism for toxisome formation and the components of toxisomes are not yet fully understood. In a previous study, we found that myosin I (FgMyo1)-actin cytoskeleton participated in toxisome formation. In the current study, we identified two new components of toxisomes, the actin capping ...[more]

PMID: 31693278

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Project description:The sesquiterpenoid deoxynivalenol (DON) is an important trichothecene mycotoxin produced by the cereal pathogen Fusarium graminearum. DON is synthesized in specialized subcellular structures called toxisomes. The first step in DON synthesis is catalyzed by the sesquiterpene synthase (STS), Tri5 (trichodiene synthase), resulting in the cyclization of farnesyl diphosphate (FPP) to produce the sesquiterpene trichodiene. Tri5 is one of eight putative STSs in the F. graminearum genome. To better understand the F. graminearum terpenome, the volatile and soluble fractions of fungal cultures were sampled. Stringent regulation of sesquiterpene accumulation was observed. When grown in trichothecene induction medium, the fungus produces trichothecenes as well as several volatile non-trichothecene related sesquiterpenes, whereas no volatile terpenes were detected when grown in non-inducing medium. Surprisingly, a Δtri5 deletion strain grown in inducing conditions not only ceased accumulation of trichothecenes, but also failed to produce the non-trichothecene related sesquiterpenes. To test whether Tri5 from F. graminearum may be a promiscuous STS directly producing all observed sesquiterpenes, Tri5 was cloned and expressed in E. coli and shown to produce primarily trichodiene in addition to minor, related cyclization products. Therefore, while Tri5 expression in F. graminearum is necessary for non-trichothecene sesquiterpene biosynthesis, direct catalysis by Tri5 does not explain the sesquiterpene deficient phenotype observed in the Δtri5 strain. To test whether Tri5 protein, separate from its enzymatic activity, may be required for non-trichothecene synthesis, the Tri5 locus was replaced with an enzymatically inactive, but structurally unaffected tri5N225D S229T allele. This allele restores non-trichothecene synthesis but not trichothecene synthesis. The tri5N225D S229T allele also restores toxisome structure which is lacking in the Δtri5 deletion strain. Our results indicate that the Tri5 protein, but not its enzymatic activity, is also required for the synthesis of non-trichothecene related sesquiterpenes and the formation of toxisomes. Toxisomes thus not only may be important for DON synthesis, but also for the synthesis of other sesquiterpene mycotoxins such as culmorin by F. graminearum.

Project description:The AP1 complex is a highly conserved clathrin adaptor that plays important roles in regulating cargo protein sorting and intracellular vesicle trafficking in eukaryotes. However, the functions of the AP1 complex in the plant pathogenic fungi including the devastating wheat pathogen Fusarium graminearum are still unclear. In this study, we investigated the biological functions of FgAP1σ, a subunit of the AP1 complex in F. graminearum. Disruption of FgAP1σ causes seriously impaired fungal vegetative growth, conidiogenesis, sexual development, pathogenesis, and deoxynivalenol (DON) production. The ΔFgap1σ mutants were found to be less sensitive to KCl- and sorbitol-induced osmotic stresses but more sensitive to SDS-induced stress than the wild-type PH-1. Although the growth inhibition rate of the ΔFgap1σ mutants was not significantly changed under calcofluor white (CFW) and Congo red (CR) stresses, the protoplasts released from ΔFgap1σ hyphae were decreased compared with the wild-type PH-1, suggesting that FgAP1σ is necessary for cell wall integrity and osmotic stresses in F. graminearum. Subcellular localization assays showed that FgAP1σ was predominantly localized to endosomes and the Golgi apparatus. In addition, FgAP1β-GFP, FgAP1γ-GFP, and FgAP1μ-GFP also localize to the Golgi apparatus. FgAP1β interacts with FgAP1σ, FgAP1γ, and FgAP1μ, while FgAP1σ regulates the expression of FgAP1β, FgAP1γ, and FgAP1μ in F. graminearum. Furthermore, the loss of FgAP1σ blocks the transportation of the v-SNARE protein FgSnc1 from the Golgi to the plasma membrane and delays the internalization of FM4-64 dye into the vacuole. Taken together, our results demonstrate that FgAP1σ plays vital roles in vegetative growth, conidiogenesis, sexual reproduction, DON production, pathogenicity, cell wall integrity, osmotic stress, exocytosis, and endocytosis in F. graminearum. These findings unveil the functions of the AP1 complex in filamentous fungi, most notably in F. graminearum, and lay solid foundations for effective prevention and control of Fusarium head blight (FHB).

Project description:Fusarium graminearum, the main pathogenic fungus causing Fusarium head blight (FHB), produces deoxynivalenol (DON), a key virulence factor, which is synthesized in the endoplasmic reticulum (ER). Sey1/atlastin, a dynamin-like GTPase protein, is known to be required for homotypic fusion of ER membranes, but the functions of this protein are unknown in pathogenic fungi. Here, we characterized Sey1/atlastin homologue FgSey1 in F. graminearum Like Sey1/atlastin, FgSey1 is located in the ER. The FgSEY1 deletion mutant exhibited significantly reduced vegetative growth, asexual development, DON biosynthesis, and virulence. Moreover, the ΔFgsey1 mutant was impaired in the formation of normal lipid droplets (LDs) and toxisomes, both of which participate in DON biosynthesis. The GTPase, helix bundle (HB), transmembrane segment (TM), and cytosolic tail (CT) domains of FgSey1 are essential for its function, but only the TM domain is responsible for its localization. Furthermore, the mutants FgSey1K63A and FgSey1T87A lacked GTPase activity and failed to rescue the defects of the ΔFgsey1 mutant. Collectively, our data suggest that the dynamin-like GTPase protein FgSey1 affects the generation of LDs and toxisomes and is required for DON biosynthesis and pathogenesis in F. graminearumIMPORTANCEFusarium graminearum is a major plant pathogen that causes Fusarium head blight (FHB) of wheats worldwide. In addition to reducing the plant yield, F. graminearum infection of wheats also results in the production of deoxynivalenol (DON) mycotoxins, which are harmful to humans and animals and therefore cause great economic losses through pollution of food products and animal feed. At present, effective strategies for controlling FHB are not available. Therefore, understanding the regulation mechanisms of fungal development, pathogenesis, and DON biosynthesis is important for the development of effective control strategies of this disease. In this study, we demonstrated that a dynamin-like GTPase protein Sey1/atlastin homologue, FgSey1, is required for vegetative growth, DON production, and pathogenicity in F. graminearum Our results provide novel information on critical roles of FgSey1 in fungal pathogenicity; therefore, FgSey1 could be a potential target for effective control of the disease caused by F. graminearum.

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Capping proteins regulate fungal development, DON-toxisome formation and virulence in Fusarium graminearum.

Publications

Capping proteins regulate fungal development, DON-toxisome formation and virulence in Fusarium graminearum.

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