Abstract

As a natural severe contaminant of stored grains and other crops worldwide, Aspergillus flavus can produce aflatoxins (AFs), the most powerful naturally producing toxic and hepatocarcinogenic compounds. AFs production is regulated by diverse factors including AFs cluster genes, transcription factors, regulators, and environmental factors. Among them, crop substrate is one of the most important factors. Here, we found that AFB1 production was significantly higher in maize and rice broth than in peanut broth. To clarify the mechanisms involved, complementary transcriptomic and proteomic analyses were performed to identify changes in A. flavus incubated in the three crop substrates. The results indicated that fewer genes and proteins were differentially expressed between maize and rice substrates, whereas more differentially expressed genes were observed between maize/rice broth and peanut broth. In particular, the genes involved in the initial step of AFs biosynthesis (aflA, aflB, and aflC) and the ACCase-encoding gene accA were significantly upregulated on the maize and rice substrates. Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analyses indicated that carbon-metabolism-related genes were obviously enriched in the maize broth, and the genes involved in acetyl-CoA accumulation and consumption were up- and downregulated, respectively. Several genes involved in the regulation of AFs biosynthesis, including veA, ppoB, snf1, and the G-protein-coupled receptor (GPCR) genes, were differentially expressed on the three substrates, suggesting that these genes may be also involved in sugar signal sensing, transfer, and regulation. Interestingly, by the correlation analyses of transcriptome and proteome, trehalose metabolism genes, aldehyde dehydrogenase gene, and tryptophan synthase gene were found to be relevant with the regulation of AFs production on different crop substrates. Taken together, the differential expressions of the AFs cluster genes, several regulatory genes, and carbon metabolism genes were involved in the comprehensive modulation of AFs production on different crop substrates.

Highlights

  • Aspergillus flavus is widely distributed in tropical and subtropical regions and infects various crops, including wheat, maize, and peanuts

  • No significant difference in the dry mycelial weights was detected among the three crop media, whereas the mycelial weights in yeast extract sucrose (YES) medium were clearly higher compared with the crop substrates (Figure 1A)

  • 50.03, 49.75, 57.89, and 55.99 million raw reads were generated from A. flavus in rice, maize, peanut, and YES media, respectively and 47.27, 47.29, 55.46, and 53.71 million clean reads were obtained after quality filtering, respectively (Supplementary Table S1)

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Summary

Introduction

Aspergillus flavus is widely distributed in tropical and subtropical regions and infects various crops, including wheat, maize, and peanuts It can produce different kinds of mycotoxins, especially aflatoxins (AFs), which cause huge losses in crop quality, safety, and commodity price (Amaike and Keller, 2011). The precursors of AFs, acetyl-CoA, and malonyl-CoA derived from carbon and lipid metabolism, are cyclized by the polyketide synthase AflC, and a series of enzymatic reactions are performed to generate AFs (Georgianna and Payne, 2009). Among these genes, aflR and aflS are the two key pathway-specific regulatory genes for AFs biosynthesis (Yin and Keller, 2011). The ratio of aflS and aflR is an indicator of the AFs biosynthesis activation (Schmidt-Heydt et al, 2010)

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