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The Transcription factor FgSfp1 orchestrates mycotoxin deoxynivalenol biosynthesis in Fusarium graminearum

ABSTRACT: Fusarium graminearum (F. graminearum) and its derivative mycotoxin deoxynivalenol (DON) are highly concerned with food security, safety and sustainability worldwide. The molecular mechanism regulates DON biosynthesis in F. graminearum remains enigmatic, despite several transcription factors (TFs) have been revealed containing regulatory functions. Here, we first characterized a zinc finger-contained TF, FgSfp1. Interestingly, contrast to the previous knowledge, all TRI-cluster genes were abnormally upregulated in ∆FgSfp1 while Tri proteins abundance rationally decreased, resulting in a 95.4% reduction of DON yield simultaneously. Further evidence determined FgSfp1 acted as a nutrient-sensing factor coordinates genetic expression efficiency through interference of ribosomal biogenesis process. Specifically, FgSfp1-depletion leads to ribosome biogenesis assembly factor (RiBi) expression attenuation along with DON precursor acetyl-CoA synthase reduction since FgSfp1 actively interacts with RNA 2’-O-methylation enzyme FgNop1 revealed by Bi-FC and subsequently influences mRNA translation capacity. In conclusion, we elucidated that the FgSfp1 orchestrates DON biosynthesis via participating RNA posttranscriptional modification for ribosomal RNA maturation, offering new insights into the DON biosynthesis regulation. Ultimately, this novel TF might be a key regulator for DON contamination control in the whole food chain.

ORGANISM(S): Fusarium graminearum PH-1

PROVIDER: GSE262607 | GEO | 2024/11/06

REPOSITORIES: GEO

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Project description:Deoxynivalenol (DON) is a type B trichothecene mycotoxin that is commonly found in cereals and grains worldwide. The presence of this fungal secondary-metabolite raises public-health concerns at both the agriculture and food industry level. The toxicity of DON is mainly characterized by its ability to inhibit ribosomal protein biosynthesis. Recently, we have shown that DON has a negative impact on gut integrity, a feature also noticed for Campylobacter (C.) jejuni. We further demonstrated that DON increased the load of C. jejuni in the gut and inner organs. In contrast, feeding the less toxic DON metabolite deepoxy-deoxynivalenol (DOM-1) to broilers reduced the Campylobacter load in vivo. Consequently, it can be hypothesized that DON and DOM-1 have a direct or indirect effect on the growth profile of C. jejuni. The aim of the present study was to further resolve the nature of this interaction in vitro by co-incubation and RNA-sequencing. The co-incubation of C. jejuni with DON resulted in significantly higher bacterial growth rates from 30 h of incubation onwards. On the contrary, the co-incubation of C. jejuni with DOM-1 reduced the CFU counts, indicating that this DON metabolite might contribute to reduce the burden of C. jejuni in birds, altogether confirming in vivo data. Furthermore, the transcriptomic profile of C. jejuni following incubation with either DON or DOM-1 differed. Co-incubation of C. jejuni with DON significantly increased the expression of multiple genes which are critical for Campylobacter growth, particularly members of the Flagella gene family, frr (ribosome-recycling factor), PBP2 futA-like (Fe3+ periplasmic binding family) and PotA (ATP-binding subunit). These organelles are required for pathogenicity-related phenotypes including motility, biofilm formation, host cell interactions, and host colonization, which may explain the high Campylobacter load in the intestine of DON-fed broiler chickens. On the contrary, DOM-1 downregulated the Flagella gene family and upregulated ribosomal proteins. The results highlight the adaptive mechanisms involved in the transcriptional response of C. jejuni to DON and its metabolite DOM-1, based on the following effects: (a) ribosomal proteins; (b) flagellar proteins; (c) engagement of different metabolic pathways. The results provide insight into the response of an important intestinal microbial pathogen against DON and lead to a better understanding of the luminal or environmental acclimation mechanisms in chickens.

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The Transcription factor FgSfp1 orchestrates mycotoxin deoxynivalenol biosynthesis in Fusarium graminearum

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