Spermidine Is Critical for Growth, Development, Environmental Adaptation, and Virulence in Fusarium graminearum.
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ABSTRACT:
SUBMITTER: Tang G
PROVIDER: S-EPMC8640359 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Golgins are coiled-coil proteins that play prominent roles in maintaining the structure and function of the Golgi complex. However, the role of golgin proteins in phytopathogenic fungi remains poorly understood. In this study, we functionally characterized the Fusarium graminearum golgin protein RUD3, a homolog of ScRUD3/GMAP-210 in Saccharomyces cerevisiae and mammalian cells. Cellular localization observation revealed that RUD3 is located in the cis-Golgi. Deletion of RUD3 caused defects in vegetative growth, ascospore discharge, deoxynivalenol (DON) production, and virulence. Moreover, the Δrud3 mutant showed reduced expression of tri genes and impairment of the formation of toxisomes, both of which play essential roles in DON biosynthesis. We further used green fluorescent protein (GFP)-tagged SNARE protein SEC22 (SEC22-GFP) as a tool to study the transport between the endoplasmic reticulum (ER) and Golgi and observed that SEC22-GFP was retained in the cis-Golgi in the Δrud3 mutant. RUD3 contains the coiled coil (CC), GRAB-associated 2 (GA2), GRIP-related Arf binding (GRAB), and GRAB-associated 1 (GA1) domains, which except for GA1, are indispensable for normal localization and function of RUD3, whereas only CC is essential for normal RUD3-RUD3 interaction. Together, these results demonstrate how the golgin protein RUD3 mediates retrograde trafficking in the ER-to-Golgi pathway and is necessary for growth, ascospore discharge, DON biosynthesis, and pathogenicity in F. graminearumIMPORTANCEFusarium head blight (FHB) caused by the fungal pathogen Fusarium graminearum is an economically important disease of wheat and other small grain cereal crops worldwide, and limited effective control strategies are available. A better understanding of the regulation mechanisms of F. graminearum development, deoxynivalenol (DON) biosynthesis, and pathogenicity is therefore important for the development of effective control management of this disease. Golgins are attached via their extreme carboxy terminus to the Golgi membrane and are involved in vesicle trafficking and organelle maintenance in eukaryotic cells. In this study, we systematically characterized a highly conserved Golgin protein, RUD3, and found that it is required for vegetative growth, ascospore discharge, DON production, and pathogenicity in F. graminearum Our findings provide a comprehensive characterization of the golgin family protein RUD3 in plant-pathogenic fungus, which could help to identify a new potential target for effective control of this devastating disease.
| S-EPMC8104996 | biostudies-literature
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.
| S-EPMC7237792 | biostudies-literature
Project description:Fusarium head blight (FHB) is a devastating disease for cereals. FHB is managed by fungicides at anthesis, but their efficacy is variable. Conventional fungicides accumulate in the soil and are dangerous for animal and human health. This study assayed the antifungal ability of chitosan hydrochloride against Fusarium graminearum. Chitosan reduced F. graminearum growth and downregulated the transcript of the major genes involved in the cell growth, respiration, virulence, and trichothecenes biosynthesis. Chitosan promoted the germination rate, the root and coleoptile development, and the nitrogen balance index in two durum wheat genotypes, Marco Aurelio (FHB-susceptible) and DBC480 (FHB-resistant). Chitosan reduced FHB severity when applied on spikes or on the flag leaves. FHB severity in DBC480 was of 6% at 21 dpi after chitosan treatments compared to F. graminearum inoculated control (20%). The elicitor-like property of chitosan was confirmed by the up-regulation of TaPAL, TaPR1 and TaPR2 (around 3-fold). Chitosan decreased the fungal spread and mycotoxins accumulation. This study demonstrated that the non-toxic chitosan is a powerful molecule with the potential to replace the conventional fungicides. The combination of a moderately resistant genotype (DBC480) with a sustainable compound (chitosan) will open new frontiers for the reduction of conventional compounds in agriculture.
| S-EPMC7587526 | biostudies-literature
Project description: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.
| S-EPMC6988429 | biostudies-literature
Project description:Peroxisomes are involved in a wide range of important cellular functions. Here, the role of the peroxisomal membrane protein PEX3 in the plant-pathogen and mycotoxin producer Fusarium graminearum was studied using knock-out and complemented strains. To fluorescently label peroxisomes' punctate structures, GFP and RFP fusions with the PTS1 and PTS2 localization signal were transformed into the wild type PH-1 and ΔFgPex3 knock-out strains. The GFP and RFP transformants in the ΔFgPex3 background showed a diffuse fluorescence pattern across the cytoplasm suggesting the absence of mature peroxisomes. The ΔFgPex3 strain showed a minor, non-significant reduction in growth on various sugar carbon sources. In contrast, deletion of FgPex3 affected fatty acid β-oxidation in F. graminearum and significantly reduced the utilization of fatty acids. Furthermore, the ΔFgPex3 mutant was sensitive to osmotic stressors as well as to cell wall-damaging agents. Reactive oxygen species (ROS) levels in the mutant had increased significantly, which may be linked to the reduced longevity of cultured strains. The mutant also showed reduced production of conidiospores, while sexual reproduction was completely impaired. The pathogenicity of ΔFgPex3, especially during the process of systemic infection, was strongly reduced on both tomato and on wheat, while to production of deoxynivalenol (DON), an important factor for virulence, appeared to be unaffected.
| S-EPMC6764106 | biostudies-literature
Project description:Mitochondrial porin, the voltage-dependent anion-selective channel (VDAC), is the most abundant protein in the outer membrane, and is critical for the exchange of metabolites and phospholipids in yeast and mammals. However, the functions of porin in phytopathogenic fungi are not known. In this study, we characterized a yeast porin orthologue, Fgporin, in Fusarium graminearum. The deletion of Fgporin resulted in defects in hyphal growth, conidiation, and perithecia development. The Fgporin deletion mutant showed reduced virulence, deoxynivalenol production, and lipid droplet accumulation. In addition, the Fgporin deletion mutant exhibited morphological changes and the dysfunction of mitochondria, and also displayed impaired autophagy in the non-nitrogen medium compared to the wild type. Yeast two-hybrid and bimolecular fluorescence complementation assays indicated that Fgporin interacted with FgUps1/2, but not with FgMdm35. Taken together, these results suggest that Fgporin is involved in hyphal growth, asexual and sexual reproduction, virulence, and autophagy in F. graminearum.
| S-EPMC9506537 | biostudies-literature
Project description:Pyruvate dehydrogenase kinase (PDK) is an important mitochondrial enzyme that blocks the production of acetyl-CoA by selectively inhibiting the activity of pyruvate dehydrogenase (PDH) through phosphorylation. PDK is an effectively therapeutic target in cancer cells, but the physiological roles of PDK in phytopathogens are largely unknown. To address these gaps, a PDK gene (FgPDK1) was isolated from Fusarium graminearum that is an economically important pathogen infecting cereals. The deletion of FgPDK1 in F. graminearum resulted in the increase in PDH activity, coinciding with several phenotypic defects, such as growth retardation, failure in perithecia and conidia production, and increase in pigment formation. The ΔFgPDK1 mutants showed enhanced sensitivity to osmotic stress and cell membrane-damaging agent. Physiological detection indicated that reactive oxygen species (ROS) accumulation and plasma membrane damage (indicated by PI staining, lipid peroxidation, and electrolyte leakage) occurred in ΔFgPDK1 mutants. The deletion of FgPDK1 also prohibited the production of deoxynivalenol (DON) and pathogenicity of F. graminearum, which may resulted from the decrease in the expression of Tri6. Taken together, this study firstly identified the vital roles of FgPDK1 in the development of phytopathogen F. graminearum, which may provide a potentially novel clue for target-directed development of agricultural fungicides.
| S-EPMC4920349 | biostudies-literature
Project description:Fusarium graminearum, the causal agent of Fusarium head blight in cereal crops, produces mycotoxins such as trichothecenes and zearalenone in infected plants. Here, we focused on the function of FgLaeA in F. graminearum, a homolog of Aspergillus nidulans LaeA encoding the global regulator for both secondary metabolism and sexual development. Prior to gene analysis, we constructed a novel luciferase reporter system consisting of a transgenic F. graminearum strain expressing a firefly luciferase gene under control of the promoter for either TRI6 or ZEB2 controlling the biosynthesis of these mycotoxins. Targeted deletion of FgLaeA led to a dramatic reduction of luminescence in reporter strains, indicating that FgLaeA controls the expression of these transcription factors in F. graminearum; reduced toxin accumulation was further confirmed by GC-MS analysis. Overexpression of FgLaeA caused the increased production of trichothecenes and additional metabolites. RNA seq-analysis revealed that gene member(s) belonging to ~70% of total tentative gene clusters, which were previously proposed, were differentially expressed in the ΔFgLaeA strain. In addition, ΔFgLaeA strains exhibited an earlier induction of sexual fruiting body (perithecia) formation and drastically reduced disease symptoms in wheat, indicating that FgLaeA seems to negatively control perithecial induction, but positively control virulence toward the host plant. FgLaeA was constitutively expressed under both mycotoxin production and sexual development conditions. Overexpression of a GFP-FgLaeA fusion construct in the ΔFgLaeA strain restored all phenotypic changes to wild-type levels and led to constitutive expression of GFP in both nuclei and cytoplasm at different developmental stages. A split luciferase assay demonstrated that FgLaeA was able to interact with FgVeA, a homolog of A. nidulans veA. Taken together, these results demonstrate that FgLaeA, a member of putative FgVeA complex, controls secondary metabolism, sexual development, and virulence in F. graminearum, although the specific regulation pattern differs from that of LaeA in A. nidulans.
| S-EPMC3713025 | biostudies-literature
Project description:Fusarium graminearum, the causal agent of Fusarium head blight, is a common pathogen on small grain cereals worldwide and produces various trichothecenes [deoxynivalenol (DON) is predominant] during infection. A previous study has revealed that DON production is positively correlated with the occurrence of carbendazim (MBC) resistance. Here, we identified and characterized two putative genes encoding hexokinase in F. graminearum (FgHXK1 and FgHXK2), which is a rate-limiting enzyme in DON biosynthesis. The expression level of hexokinase genes and the production of pyruvate, which is the precursor of DON, were up-regulated in the MBC-resistant strain, indicating that hexokinase genes might be involved in increased DON production. Phylogenetic and comparative analyses indicated that FgHXK1 was the predominant hexokinase gene. Gene disruption showed that ΔFgHXK1 severely affected DON production, indicating that FgHXK1 played a role in the regulation of DON biosynthesis. Morphological characterization showed that ΔFgHXK1 led to inhibited vegetative growth and conidiation. Sensitivity tests to MBC and various stresses indicated that both ΔFgHXK1 and ΔFgHXK2 mutants showed no significant difference from parental strains. Pathogencity assays showed that ΔFgHXK1 mutants lost virulence on wheat head and corn stigma; however, they showed no change in sexual reproduction. The FgHXK1-overexpressing transformants were obtained subsequently. Their pyruvate and DON production was confirmed to be increased, indicating that FgHXK1 positively regulated DON biosynthesis. Although additional defects appeared in overexpression mutants, MBC sensitivity showed no change. All of the results indicated that the transcriptional level of FgHXK1 regulated DON biosynthesis, but showed no direct relationship with MBC resistance.
| S-EPMC6638496 | biostudies-literature
Project description:Fusarium graminearum is one of the main causal agents of the Fusarium Head Blight, a worldwide disease affecting cereal cultures, whose presence can lead to contaminated grains with chemically stable and harmful mycotoxins. Resistant cultivars and fungicides are frequently used to control this pathogen, and several observations suggest an adaptation of F. graminearum that raises concerns regarding the future of current plant disease management strategies. To understand the genetic basis as well as the extent of its adaptive potential, we investigated the landscape of genomic diversity among six French isolates of F. graminearum, at single-nucleotide resolution using whole-genome re-sequencing.A total of 242,756 high-confidence genetic variants were detected when compared to the reference genome, among which 96% are single nucleotides polymorphisms. One third of these variants were observed in all isolates. Seventy-seven percent of the total polymorphism is located in 32% of the total length of the genome, comprising telomeric/subtelomeric regions as well as discrete interstitial sections, delineating clear variant enriched genomic regions- 7.5 times in average. About 80% of all the F. graminearum protein-coding genes were found polymorphic. Biological functions are not equally affected: genes potentially involved in host adaptation are preferentially located within polymorphic islands and show greater diversification rate than genes fulfilling basal functions. We further identified 29 putative effector genes enriched with non-synonymous effect mutation.Our results highlight a remarkable level of polymorphism in the genome of F. graminearum distributed in a specific pattern. Indeed, the landscape of genomic diversity follows a bi-partite organization of the genome according to polymorphism and biological functions. We measured, for the first time, the level of sequence diversity for the entire gene repertoire of F. graminearum and revealed that the majority are polymorphic. Those assumed to play a role in host-pathogen interaction are discussed, in the light of the subsequent consequences for host adaptation. The annotated genetic variants discovered for this major pathogen are valuable resources for further genetic and genomic studies.
| S-EPMC5324198 | biostudies-literature