The TOR Signaling Pathway Governs Fungal Development, Virulence and Ustiloxin Biosynthesis in Ustilaginoidea virens

Ustilaginoidea virens is an economically important plant pathogen that causes rice false smut, which causes yield reduction and produces mycotoxins in infected grains that pose a serious threat to human and animal health. The target of rapamycin (TOR) signaling pathway acts as a master regular in regulating cell growth and secondary metabolism in fungi. However, little is known about the function of the TOR pathway in regulating fungal development, pathogenicity and mycotoxin biosynthesis in U. virens. Here, we demonstrate that the TOR signaling pathway positively regulates the cell growth, conidiation and pathogenicity in U. virens through the biochemical inhibition of TOR kinases. The inhibition of TOR in U. virens (UvTOR) by rapamycin significantly induces the expression of genes related to mycotoxin biosynthesis, especially that of ustiloxins. Transcriptome analysis under TOR inhibition revealed that the TOR signaling pathway is a regulatory hub that governs U. virens growth and metabolism. A total of 275 differentially expressed genes (DEGs), consisting of 109 up-regulated DEGs and 166 down-regulated DEGs, were identified after rapamycin treatment. The up-regulated DEGs were enriched in amino acid- and acetyl-CoA-related metabolism pathways and the down-regulated DEGs were enriched in carbohydrate- and fatty acid-related metabolism pathways. Collectively, our results provide the first in-depth insight into the TOR signaling pathway in regulating vegetable growth, virulence and mycotoxin biosynthesis in U. virens.