Lipid droplet biogenesis regulated by the FgNem1/Spo7‐FgPah1 phosphatase cascade plays critical roles in fungal development and virulence in <i>Fusarium graminearum</i>

Liu, Na; Yun, Yingzi; Yin, Yanni; Hahn, Matthias; Ma, Zhonghua; Chen, Yun

doi:10.1111/nph.15748

Cited by 41 publications

(56 citation statements)

References 59 publications

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“…The reduction of glycerol production in Δ FgSah1 also explained its increased sensitivity to fludioxonil and iprodione, which have been reported to be related to osmotic pressure [ 50 ]. The lack of glycerol in deletion mutants leads to a sharp decrease in the synthesis of LDs, which has been reported to be crucial to full virulence and proper development [ 57 ]. We inferred that FgSah1 may be partly responsible for the impaired infection abilities on the host due to the deficient lipid metabolism in mutant strains.…”

Section: Discussionmentioning

confidence: 99%

S-adenosyl-L-homocysteine hydrolase FgSah1 is required for fungal development and virulence in Fusarium graminearum

et al. 2021

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The S-adenosyl-L-homocysteine hydrolase (Sah1) plays a crucial role in methylation and lipid metabolism in yeast and mammals, yet its function remains elusive in filamentous fungi. In this study, we characterized Sah1 in the phytopathogenic fungus F. graminearum by generating knockout and knockout-complemented strains of FgSAH1 . We found that the FgSah1-GFP fusion protein was localized to the cytoplasm, and that deletion of FgSAH1 resulted in defects in vegetative growth, asexual and sexual reproduction, stress responses, virulence, lipid metabolism, and tolerance against fungicides. Moreover, the accumulations of S-adenosyl-L-homocysteine (AdoHcy) and S-adenosyl-L-methionine (AdoMet) (the methyl group donor in most methyl transfer reactions) in Δ FgSah1 were seven- and ninefold higher than those in the wild-type strain, respectively. All of these defective phenotypes in Δ FgSah1 mutants were rescued by target gene complementation. Taken together, these results demonstrate that FgSah1 plays essential roles in methylation metabolism, fungal development, full virulence, multiple stress responses, lipid metabolism, and fungicide sensitivity in F. graminearum . To our knowledge, this is the first report on the systematic functional characterization of Sah1 in F. graminearum .

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Section: Discussionmentioning

confidence: 99%

S-adenosyl-L-homocysteine hydrolase FgSah1 is required for fungal development and virulence in Fusarium graminearum

et al. 2021

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“…The ER plays a role in the biosynthesis of DON, which requires the formation of toxisomes on the ER (11), a large organelle with various key functions. Recent studies have shown that the formation of toxisomes is related to the generation of LDs during DON biosynthesis in vitro and in planta (37). LDs are also produced in the ER, and Atl1, as an ER-associated protein, has been shown to regulate the size of LDs in mammalian cells (20).…”

Section: Discussionmentioning

confidence: 99%

“…FgSey1 is involved in formation of lipid droplets and toxisomes. During plant infection, a large number of LDs, which are associated with toxisome formation, are synthesized in F. graminearum (37). In eukaryotes, LDs are synthesized on endoplasmic reticulum, while the mammalian dynamin-like GTPase protein atlastin, ATL1 (the ortholog of FgSey1), is involved in the regulation of normal LD formation (20).…”

Section: Saccharomyces Cerevisiae Sey1mentioning

confidence: 99%

“…The generation and expansion of LDs in ER membrane is well documented (20,35). In F. graminearum, the formation of DON toxisomes is related to the generation of a large number of LDs during plant infection (36,37), and the FgNem1/Spo7-FgPah1 cascade is involved in fungal development and pathogenicity through regulating the biogenesis of LDs (37). The accumulation of LDs plays a key role in fungal pathogenicity.…”

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confidence: 99%

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The Dynamin-Like GTPase FgSey1 Plays a Critical Role in Fungal Development and Virulence in Fusarium graminearum

Chong

Wang

et al. 2020

Appl Environ Microbiol

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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. graminearum. IMPORTANCE Fusarium 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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“…LDs contain dozens of different proteins on their surfaces, form tight associations with other organelles and cellular structures, and play essential roles in diverse cellular processes such as energy homeostasis, oxidative stress, detoxification, membrane stability, and gene regulation [ 28 , 29 , 30 , 31 , 32 ]. A number of bacterial and fungal pathogens use their own lipid droplets, or exploit host lipid droplets, as a means of initiating and maintaining infection [ 33 , 34 , 35 ]. The rice blast fungus, Magnaporthe grisea , for instance, mobilizes lipid droplets during infection structure (appressoria) formation, where they are degraded for use as energy stores and for maintaining the extremely high turgor pressure necessary to infect its host by mechanical penetration of tissues [ 36 , 37 ].…”

Section: Introductionmentioning

confidence: 99%

Unique Attributes of the Laurel Wilt Fungal Pathogen, Raffaelea lauricola, as Revealed by Metabolic Profiling

et al. 2021

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Raffaelea lauricola is the causative agent of laurel wilt, a devastating disease of lauraceous trees. R. lauricola is also an obligate nutritional symbiont of several ambrosia beetle species who act as vectors for the pathogen. Here, we sought to establish the baseline “phenome” of R. lauricola with knowledge concerning its metabolic capability, expanding our understanding of how these processes are impacted by environmental and host nutrients. Phenotypic screening using a microarray of over one thousand compounds was used to generate a detailed profile of R. lauricola substrate utilization and chemical sensitivity. These data revealed (i) relatively restricted carbon utilization, (ii) broad sulfur and phosphate utilization, and (iii) pH and osmotic sensitivities that could be rescued by specific compounds. Additional growth profiling on fatty acids revealed toxicity on C10 substrates and lower, with robust growth on C12–C18 fatty acids. Conditions for lipid droplet (LD) visualization and LD dynamics were examined using a series of lipid dyes. These data provide unique insights regarding R. lauricola metabolism and physiology, and identify distinct patterns of substrate usage and sensitivity which likely reflect important aspects of the host-microbe interface and can be exploited for the development of strategies for mitigating the spread of laurel wilt.

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Lipid droplet biogenesis regulated by the FgNem1/Spo7‐FgPah1 phosphatase cascade plays critical roles in fungal development and virulence in Fusarium graminearum

Cited by 41 publications

References 59 publications

S-adenosyl-L-homocysteine hydrolase FgSah1 is required for fungal development and virulence in Fusarium graminearum

S-adenosyl-L-homocysteine hydrolase FgSah1 is required for fungal development and virulence in Fusarium graminearum

The Dynamin-Like GTPase FgSey1 Plays a Critical Role in Fungal Development and Virulence in Fusarium graminearum

Unique Attributes of the Laurel Wilt Fungal Pathogen, Raffaelea lauricola, as Revealed by Metabolic Profiling

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