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Plant pathogens are challenged by host-derived iron starvation or excess during infection, but the mechanism through which pathogens counteract iron stress is unclear. Here, we found that Fusarium graminearum encounters iron excess during the colonization of wheat heads. Deletion of heme activator protein X (FgHapX), siderophore transcription factor A (FgSreA) or both attenuated virulence. Further, we found that FgHapX activates iron storage under iron excess by promoting histone H2B deubiquitination (H2B deub1) at the promoter of the responsible gene. Meanwhile, FgSreA is shown to inhibit genes mediating iron acquisition during iron excess by facilitating the deposition of histone variant H2A.Z and histone 3 lysine 27 trimethylation (H3K27 me3) at the first nucleosome after the transcription start site. In addition, the monothiol glutaredoxin FgGrx4 is responsible for iron sensing and control of the transcriptional activity of FgHapX and FgSreA via modulation of their enrichment at target genes and recruitment of epigenetic regulators, respectively. Taken together, our findings elucidated the molecular mechanisms for adaptation to iron excess mediated by FgHapX and FgSreA during infection in F. graminearum and provide novel insights into regulation of iron homeostasis at the chromatin level in eukaryotes.
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Fusarium , Histonas , Hierro , Cromatina , Histonas/genética , Histonas/metabolismo , Hierro/metabolismo , Nucleosomas , Sideróforos/genética , Fusarium/metabolismoRESUMEN
Preventing grain from fungi and subsequent mycotoxins contamination has attracted notable attention. Present study demonstrated the limonene-formulated product Wetcit®, might be a biocontrol agent and potential alternative to synthetic fungicides to control Fusarium graminearum growth and deoxynivalenol (DON) production. The limonene formulation exhibited antifungal activity against F. graminearum with the EC50 at 1.40 µl/ml, electron microscopy and staining analysis showed limonene formulation could significantly decrease the quantity, length and septa of conidia, caused hyphal break and shrink, damaged the structures of cell membrane, cell wall, vacuoles and organelles in the hypha. Further study revealed the antifungal and antitoxic mechanism of limonene formulation against F. graminearum, limonene formulation significantly inhibited the toxisome and DON formation, was associated with the down-regulation of trichothecenes biosynthesis genes expression and many energy metabolism pathways as well as the inhibition of lipid droplets, the disturbed energy homeostasis and intracellular structures might ultimately inhibit fungal growth and DON production. In addition, limonene formulation enhanced the antifungal activity of triazole fungicides tebuconazole and mefentrifluconazole against F. graminearum, indicated limonene formulation has valuable potential as a bio-alternative fungicide and eco-friendly compound preparation for the effective management of F. graminearum and DON contamination in agriculture.
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Molecular interactions between pathogen effectors and plant immunity underpin the arms race of disease resistance and susceptibility. In a recently published Cell Reports paper, Zuo et al. reported the mechanistic characterization of Fusarium graminearum CFEM effectors that dampen ZmWAK17-mediated defenses in maize (Zea mays).
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Empalme Alternativo , Resistencia a la Enfermedad , Virulencia/genética , Empalme Alternativo/genética , Resistencia a la Enfermedad/genética , Zea mays/genética , Zea mays/metabolismo , Zea mays/microbiología , Enfermedades de las Plantas/genética , Enfermedades de las Plantas/microbiología , Proteínas Fúngicas/metabolismoRESUMEN
Pathogenic fungi are subject to DNA damage stress derived from host immune responses during infection. Small ubiquitin-like modifier (SUMO) modification and precursor (pre)-mRNA splicing are both involved in DNA damage response (DDR). However, the mechanisms of how SUMOylation and splicing coordinated in DDR remain largely unknown. Combining with biochemical analysis, RNA-Seq method, and biological analysis, we report that SUMO pathway participates in DDR and virulence in Fusarium graminearum, a causal agent of Fusarium head blight of cereal crops world-wide. Interestingly, a key transcription factor FgSR is SUMOylated upon DNA damage stress. SUMOylation regulates FgSR nuclear-cytoplasmic partitioning and its phosphorylation by FgMec1, and promotes its interaction with chromatin remodeling complex SWI/SNF for activating the expression of DDR-related genes. Moreover, the SWI/SNF complex was found to further recruit splicing-related NineTeen Complex, subsequently modulates pre-mRNA splicing during DDR. Our findings reveal a novel function of SUMOylation in DDR by regulating a transcription factor to orchestrate gene expression and pre-mRNA splicing to overcome DNA damage during the infection of F. graminearum, which advances the understanding of the delicate regulation of DDR by SUMOylation in pathogenic fungi, and extends the knowledge of cooperation of SUMOylation and pre-mRNA splicing in DDR in eukaryotes.
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Precursores del ARN , Sumoilación , Precursores del ARN/genética , Precursores del ARN/metabolismo , Proteínas Modificadoras Pequeñas Relacionadas con Ubiquitina/metabolismo , Factores de Transcripción/metabolismo , Daño del ADNRESUMEN
Very long-chain fatty acids (VLCFAs), the precursors for the synthesis of sphingolipids (SLs), play pivotal roles in the development and stress response in eukaryotes. In Saccharomyces cerevisiae, VLCFAs are synthesized in the endoplasmic reticulum (ER) through a four-step elongation cycle. However, the functions of VLCFA elongases in phytopathogenic fungi remain largely unexplored. Here, we identified a single copy of the VLCFA elongase gene FgELO2 in Fusarium graminearum that causes Fusarium head blight worldwide. FgElo2 localized to ER membrane, and deletion mutant of FgELO2 exhibited serious defects in vegetative growth and conidiation. Importantly, ΔFgElo2 led to ergosterol content reduction and disrupted the ER-localization of 14-α-demethylase FgCyp51s, indicating that the scarce of SLs reduced ergosterol, which ultimately elevated the sensitivity of ΔFgElo2 to tebuconazole. Fluorescent microscopic examination suggested that FgElo2 was degraded upon cell membrane stress. ΔFgElo2 showed decreased phosphorylation of high osmolarity glycerol (HOG) pathway and subsequently exhibited remarkable sensitivity to osmotic stress. In addition, fungal virulence was dramatically reduced in ΔFgElo2 via inhibiting deoxynivalenol production and formation of infection structures. Together, this study demonstrates that the VLCFA elongase FgElo2 modulates fungal development, tebuconazole sensitivity, stress responses and virulence, which may advance our understanding of pathogen-host interactions mediated by VLCFAs.
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Fusarium , Fusarium/metabolismo , Virulencia/genética , Elongasas de Ácidos Grasos , Proteínas Fúngicas/genética , Ergosterol/metabolismo , Saccharomyces cerevisiae/genética , Saccharomyces cerevisiae/metabolismo , Esporas Fúngicas/metabolismo , Enfermedades de las Plantas/microbiologíaRESUMEN
Introduction: Fusarium graminearum is a most destructive fungal pathogen that causes Fusarium head blight (FHB) disease in cereal crops, resulting in severe yield loss and mycotoxin contamination in food and feed. Silver nanoparticles (AgNPs) are extensively applied in multiple fields due to their strong antimicrobial activity and are considered alternatives to fungicides. However, the antifungal mechanisms and the effects of AgNPs on mycotoxin production have not been well characterized. Objectives: This study aimed to investigate the antifungal activity and mechanisms of AgNPs against both fungicide-resistant and fungicide-sensitive F. graminearum strains, determine their effects on mycotoxin deoxynivalenol (DON) production, and evaluate the potential of AgNPs for FHB management in the field. Methods: Scanning electron microscopy (SEM), transmission electron microscopy (TEM), and fluorescence microscopy were used to examine the fungal morphological changes caused by AgNPs. In addition, RNA-Seq, qRT-PCR, and western blotting were conducted to detect gene transcription and DON levels. Results: AgNPs with a diameter of 2 nm exhibited effective antifungal activity against both fungicide-sensitive and fungicide-resistant strains of F. graminearum. Further studies showed that AgNP application could impair the development, cell structure, cellular energy utilization, and metabolism pathways of this fungus. RNA-Seq analysis and sensitivity determination revealed that AgNP treatment significantly induced the expression of azole-related ATP-binding cassette (ABC) transporters without compromising the control efficacy of azoles in F. graminearum. AgNP treatment stimulated the generation of reactive oxygen species (ROS), subsequently induced transcription of DON biosynthesis genes, toxisome formation, and mycotoxin production. Conclusion: This study revealed the underlying mechanisms of AgNPs against F. graminearum, determined their effects on DON production, and evaluated the potential of AgNPs for controlling fungicide-resistant F. graminearum strains. Together, our findings suggest that combinations of AgNPs with DON-reducing fungicides could be used for the management of FHB in the future.
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Fungicidas Industriales , Fusarium , Nanopartículas del Metal , Micotoxinas , Tricotecenos , Antifúngicos/farmacología , Azoles/metabolismo , Azoles/farmacología , Fungicidas Industriales/metabolismo , Fungicidas Industriales/farmacología , Fusarium/genética , Fusarium/metabolismo , Micotoxinas/metabolismo , Micotoxinas/farmacología , Plata/metabolismo , Plata/farmacología , Tricotecenos/metabolismo , Tricotecenos/farmacologíaRESUMEN
Fusarium graminearum produces the mycotoxin deoxynivalenol (DON) which promotes its expansion during infection on its plant host wheat. Conditional expression of DON production during infection is poorly characterized. Wheat produces the defense compound putrescine, which induces hypertranscription of DON biosynthetic genes (FgTRIs) and subsequently leads to DON accumulation during infection. Further, the regulatory mechanisms of FgTRIs hypertranscription upon putrescine treatment were investigated. The transcription factor FgAreA regulates putrescine-mediated transcription of FgTRIs by facilitating the enrichment of histone H2B monoubiquitination (H2B ub1) and histone 3 lysine 4 di- and trimethylations (H3K4 me2/3) on FgTRIs. Importantly, a DNA-binding domain (bZIP) specifically within the Fusarium H2B ub1 E3 ligase Bre1 othologs is identified, and the binding of this bZIP domain to FgTRIs depends on FgAreA-mediated chromatin rearrangement. Interestingly, H2B ub1 regulates H3K4 me2/3 via the methyltransferase complex COMPASS component FgBre2, which is different from Saccharomyces cerevisiae. Taken together, our findings reveal the molecular mechanisms by which host-generated putrescine induces DON production during F. graminearum infection. Our results also provide a novel insight into the role of putrescine during phytopathogen-host interactions and broaden our knowledge of H2B ub1 biogenesis and crosstalk between H2B ub1 and H3K4 me2/3 in eukaryotes.
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Fusarium , Micotoxinas , Proteínas de Saccharomyces cerevisiae , Cromatina , Fusarium/genética , Histonas/genética , Enfermedades de las Plantas , Saccharomyces cerevisiae/metabolismo , Proteínas de Saccharomyces cerevisiae/metabolismoRESUMEN
Nitric oxide (NO) is a diffusible signaling molecule that modulates animal and plant immune responses. In addition, reactive nitrogen species derived from NO can display antimicrobial activities by reacting with microbial cellular components, leading to nitrosative stress (NS) in pathogens. Here, we identify FgAreB as a regulator of the NS response in Fusarium graminearum, a fungal pathogen of cereal crops. FgAreB serves as a pioneer transcription factor for recruitment of the chromatin-remodeling complex SWI/SNF at the promoters of genes involved in the NS response, thus promoting their transcription. FgAreB plays important roles in fungal infection and growth. Furthermore, we show that a transcription repressor (FgIxr1) competes with the SWI/SNF complex for FgAreB binding, and negatively regulates the NS response. NS, in turn, promotes the degradation of FgIxr1, thus enhancing the recruitment of the SWI/SNF complex by FgAreB.
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Ensamble y Desensamble de Cromatina/genética , Proteínas Cromosómicas no Histona/metabolismo , Fusarium/metabolismo , Factores de Transcripción GATA/metabolismo , Regulación Fúngica de la Expresión Génica/genética , Enfermedades de las Plantas/microbiología , Proteína SMARCB1/metabolismo , Factores de Transcripción/metabolismo , Inmunoprecipitación de Cromatina , Proteínas Cromosómicas no Histona/genética , Fusarium/genética , Fusarium/patogenicidad , Factores de Transcripción GATA/genética , Proteínas del Grupo de Alta Movilidad/genética , Proteínas del Grupo de Alta Movilidad/metabolismo , Óxido Nítrico/metabolismo , Estrés Nitrosativo , Proteína SMARCB1/genética , Factores de Transcripción/genética , Triticum/microbiología , Zea mays/microbiologíaRESUMEN
Strawberry anthracnose, caused by Colletotrichum species, is a major fungal disease threatening the strawberry industry in Sichuan Province of southwestern China. However, research on identification of Colletotrichum species associated with strawberry anthracnose in Sichuan remains scarce. In this study, 73 representative Colletotrichum strains were isolated from diseased leaves, stolons, petioles, and crowns of 11 major strawberry-planting localities in Sichuan Province. Based on morphological characteristics and multiloci phylogenetic analysis, the Colletotrichum strains were identified as three distinct species: Colletotrichum fructicola (53 strains, 72.60%), Colletotrichum siamense (17 strains, 23.29%), and Colletotrichum gloeosporioides sensu stricto (3 strains, 4.11%). Among them, C. fructicola was the most ubiquitous and dominant species, whereas C. gloeosporioides sensu stricto was restricted to Chongzhou. Importantly, our pathogenicity tests showed that C. fructicola and C. siamense can infect both leaves and stolons, whereas C. gloeosporioides sensu stricto was only pathogenic to leaves. Interestingly, although the sexual stage of C. siamense was not observed in this study, it still exhibited the strongest virulence to strawberry compared with C. gloeosporioides sensu stricto and C. fructicola. This is the first study to characterize Colletotrichum species causing strawberry anthracnose and evaluate their pathogenicity in Sichuan Province of southwestern China, which will provide a better strategy for accurate diagnosis and management of anthracnose disease in strawberry.
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Colletotrichum , Fragaria , Enfermedades de las Plantas/microbiología , Colletotrichum/genética , Colletotrichum/patogenicidad , Fragaria/microbiología , Filogenia , VirulenciaRESUMEN
The SWI/SNF chromatin remodeling complex utilizes the energy of ATP hydrolysis to facilitate chromatin access and plays essential roles in DNA-based events. Studies in animals, plants and fungi have uncovered sophisticated regulatory mechanisms of this complex that govern development and various stress responses. In this review, we summarize the composition of SWI/SNF complex in eukaryotes and discuss multiple functions of the SWI/SNF complex in regulating gene transcription, mRNA splicing, and DNA damage response. Our review further highlights the importance of SWI/SNF complex in regulating plant immunity responses and fungal pathogenesis. Finally, the potentials in exploiting chromatin remodeling for management of crop disease are presented.
RESUMEN
Sterol biosynthesis is controlled by transcription factor SREBP in many eukaryotes. Here, we show that SREBP orthologs are not involved in the regulation of sterol biosynthesis in Fusarium graminearum, a fungal pathogen of cereal crops worldwide. Instead, sterol production is controlled in this organism by a different transcription factor, FgSR, that forms a homodimer and binds to a 16-bp cis-element of its target gene promoters containing two conserved CGAA repeat sequences. FgSR is phosphorylated by the MAP kinase FgHog1, and the phosphorylated FgSR interacts with the chromatin remodeling complex SWI/SNF at the target genes, leading to enhanced transcription. Interestingly, FgSR orthologs exist only in Sordariomycetes and Leotiomycetes fungi. Additionally, FgSR controls virulence mainly via modulating deoxynivalenol biosynthesis and responses to phytoalexin.