Disentangling the sucrose metabolism of the corn smut Ustilago maydis reveals unexpected complexity

Abstract

The race for carbohydrates shapes organismic interactions. In plant pathogenic fungi, sucrose is a key nutrient as it constitutes the major transport sugar in plants. Here, we investigate sucrose acquisition in the corn smut fungus Ustilago maydis, a biotrophic pathogen that transitions from yeast-like to hyphal growth for infection. We establish that the fungus encodes a secreted acidic invertase, Suc2, with a dimeric canonical glycoside hydrolase 32 architecture. Comparative biochemical analyses across fungal homologs indicate that this dimeric architecture represents the predominant state, whereas higher-order oligomers, as initially described for Saccharomyces cerevisiae Suc2, are restricted to a subset of lineages. Unexpectedly, elimination of Suc2 did not impair yeast-like growth on sucrose. Similarly, deletion of genes for sucrose transporter Srt1 and cytosolic hydrolase Suc1, typically associated with intracellular sucrose metabolism, did not abolish growth. Instead, sucrose utilization during yeast-like growth depended on a repurposed non-canonical module comprising maltose transporter Agt1 and intracellular (iso)maltases. In contrast, pathogenic development strongly relied on the canonical intracellular sucrose utilization pathway mediated by Srt1 and Agt1. Infection was strongly diminished in strains unable to metabolise sucrose, confirming its central nutritional role for the fungus. Together, our work defines the complete sucrose utilization repertoire of U. maydis and uncovers a lifestyle-dependent metabolic switch between alternative sucrose acquisition strategies. Flexible carbon acquisition might represent a widespread adaptive strategy in basidiomycete pathogenic fungi.