Dataset Information

The Transcriptional Regulator Hbx1 Affects the Expression of Thousands of Genes in the Aflatoxin-Producing Fungus Aspergillus flavus.

ABSTRACT: In filamentous fungi, homeobox proteins are conserved transcriptional regulators described to control conidiogenesis and fruiting body formation. Eight homeobox (hbx) genes are found in the genome of the aflatoxin-producing ascomycete, Aspergillus flavus While loss-of-function of seven of the eight genes had little to no effect on fungal growth and development, disruption of hbx1, resulted in aconidial colonies and lack of sclerotial production. Furthermore, the hbx1 mutant was unable to produce aflatoxins B1 and B2, cyclopiazonic acid and aflatrem. In the present study, hbx1 transcriptome analysis revealed that hbx1 has a broad effect on A. flavus gene expression, and the effect of hbx1 increases overtime, impacting more than five thousand protein-coding genes. Among the affected genes, those in the category of secondary metabolism (SM), followed by that of cellular transport, were the most affected. Specifically, regarding the effect of hbx1 on SM, we found that genes in 44 SM gene clusters where upregulated while 49 were downregulated in the absence of hbx1, including genes in the SM clusters responsible for the synthesis of asparasone, piperazine and aflavarin, all known to be associated with sclerotia. In addition, our study revealed that hbx1 affects the expression of other transcription factor genes involved in development, including the conidiation central regulatory pathway and flb genes.

SUBMITTER: Cary JW

PROVIDER: S-EPMC6325891 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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The Transcriptional Regulator Hbx1 Affects the Expression of Thousands of Genes in the Aflatoxin-Producing Fungus Aspergillus flavus.

Cary Jeffrey W JW Entwistle Sarah S Satterlee Timothy T Mack Brian M BM Gilbert Matthew K MK Chang Perng K PK Scharfenstein Leslie L Yin Yanbin Y Calvo Ana M AM

G3 (Bethesda, Md.) 20190109 1

In filamentous fungi, homeobox proteins are conserved transcriptional regulators described to control conidiogenesis and fruiting body formation. Eight homeobox (hbx) genes are found in the genome of the aflatoxin-producing ascomycete, Aspergillus flavus While loss-of-function of seven of the eight genes had little to no effect on fungal growth and development, disruption of hbx1, resulted in aconidial colonies and lack of sclerotial production. Furthermore, the hbx1 ...[more]

PMID: 30425054

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Project description:The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of Aspergillus flavus impact the evolution of genes associated with the synthesis of aflatoxin, a notoriously potent carcinogen. We sequenced the genomes of, and quantified aflatoxin production in, 94 isolates of A. flavus sampled from seven states in eastern and central latitudinal transects of the United States. The overall population is subdivided into three genetically differentiated populations (A, B, and C) that differ greatly in their extent of recombination, diversity, and aflatoxin-producing ability. Estimates of the number of recombination events and linkage disequilibrium decay suggest relatively frequent sex only in population A. Population B is sympatric with population A but produces significantly less aflatoxin and is the only population where the inability of nonaflatoxigenic isolates to produce aflatoxin was explained by multiple gene deletions. Population expansion evident in population B suggests a recent introduction or range expansion. Population C is largely nonaflatoxigenic and restricted mainly to northern sampling locations through restricted migration and/or selection. Despite differences in the number and type of mutations in the aflatoxin gene cluster, codon optimization and site frequency differences in synonymous and nonsynonymous mutations suggest that low levels of recombination in some A. flavus populations are sufficient to purge deleterious mutations.IMPORTANCE Differences in the relative frequencies of sexual and asexual reproduction have profound implications for the accumulation of deleterious mutations (Muller's ratchet), but little is known about how these differences impact the evolution of ecologically important phenotypes. Aspergillus flavus is the main producer of aflatoxin, a notoriously potent carcinogen that often contaminates food. We investigated if differences in the levels of production of aflatoxin by A. flavus could be explained by the accumulation of deleterious mutations due to a lack of recombination. Despite differences in the extent of recombination, variation in aflatoxin production is better explained by the demography and history of specific populations and may suggest important differences in the ecological roles of aflatoxin among populations. Furthermore, the association of aflatoxin production and populations provides a means of predicting the risk of aflatoxin contamination by determining the frequencies of isolates from low- and high-production populations.

Project description:Purpose: Aflatoxin B1 is the most toxic and carcinogenic compound in nature produced by Aspergillus fungi. In our study, we applied RNA-seq to compare the transcriptomic profiles of Aspergillus flavus strains in the presence and absence of medicinal plant Zanthoxylum bungeanum. Methods: mRNA profiles of Aspergillus flavus supplemented with 250 µg/ml of methanolic extract fraction (treated samples) or DMSO (control samples) were generated in triplicate, by an Illumina platform using paired-end 150 bp sequencing strategy. Clean paired-end reads were mapped to the reference genome of A. flavus NRRL3357. Gene expression quantification was calculated by FPKM (Fragments Per Kilobase of transcript sequence per Millions base pairs sequenced). The differentially expressed genes (DGEs) between the control and test samples were analyzed using the DESeq2 R package. Results: RNA-seq produced 24.5–32.1 million clean paired-end reads (150 bp read length) per sample and most of them (83–91%) were uniquely mapped to the reference genome of A. flavus NRRL3357. Eighty-two percent of genes displayed FPKM value ≥1 and were thus classified as expressed genes. Ninety-six percent of the expressed genes were expressed both in the control and test groups whereas 2.3% and 1.8% of the genes were expressed only in the control or test group, respectively. With the combination of FPKM fold change ≥2 and adjusted p-value <0.05, we found in total 950 DEG’s. Among them, 515 genes were downregulated and 435 genes were upregulated. We used FungiFun software to analyze the functions of the DEGs based on FunCat pathways and categories. About half of the DEG’s had a relevant annotation in the FunCat database, and 60–70% of the annotated DEG’s were found to be enriched in specific functional pathways. Conclusions: we showed that simple organic extracts from Z. bungeanum inhibit both the growth and aflatoxin production by Aspergillus flavus. The repression of AF pathway is mediated by global regulators instead of pathway specific regulators AflR or AflS. Consistently, the expression of Velvet complex, a prominent regulator of fungal secondary metabolism and development, was substantially reduced. Natural compound extracts from Z. bungeanum have potential to facilitate the development of safe and economical control strategies that shutdown aflatoxin production in aflatoxigenic Aspergillus species.

Dataset Information

The Transcriptional Regulator Hbx1 Affects the Expression of Thousands of Genes in the Aflatoxin-Producing Fungus Aspergillus flavus.

Publications

The Transcriptional Regulator Hbx1 Affects the Expression of Thousands of Genes in the Aflatoxin-Producing Fungus <i>Aspergillus flavus</i>.

Similar Datasets

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