| Summary: | Aflatoxins are immunosuppressive and carcinogenic secondary metabolites, produced by the filamentous ascomycete <i>Aspergillus flavus</i>, that are hazardous to animal and human health. In this study, we show that multiplexed host-induced gene silencing (HIGS) of <i>Aspergillus flavus</i> genes essential for fungal sporulation and aflatoxin production (<i>nsdC</i>, <i>veA</i>, <i>aflR</i>, and <i>aflM)</i> confers enhanced resistance to <i>Aspergillus</i> infection and aflatoxin contamination in groundnut (<20 ppb). Comparative proteomic analysis of contrasting groundnut genotypes (WT and near-isogenic HIGS lines) supported a better understanding of the molecular processes underlying the induced resistance and identified several groundnut metabolites that might play a significant role in resistance to <i>Aspergillus</i> infection and aflatoxin contamination. Fungal differentiation and pathogenicity proteins, including calmodulin, transcriptional activator-HacA, kynurenine 3-monooxygenase 2, VeA, VelC, and several aflatoxin pathway biosynthetic enzymes, were downregulated in <i>Aspergillus</i> infecting the HIGS lines. Additionally, in the resistant HIGS lines, a number of host resistance proteins associated with fatty acid metabolism were strongly induced, including phosphatidylinositol phosphate kinase, lysophosphatidic acyltransferase-5, palmitoyl-monogalactosyldiacylglycerol Δ-7 desaturase, ceramide kinase-related protein, sphingolipid Δ-8 desaturase, and phospholipase-D. Combined, this knowledge can be used for groundnut pre-breeding and breeding programs to provide a safe and secure food supply.
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