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.
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BibTeX
@misc{berwanger2026disentangling,
title = {{Disentangling the sucrose metabolism of the corn smut Ustilago maydis reveals unexpected complexity}},
author = {Tom Berwanger and Ali Khoshouei and Heba Yehia and Joana Charlot Hasenklever and Tanvir Hassan and Anna Barbara Matuszyńska and Jörg Kämper and Khaled A. Selim and Florian Altegoer and Kerstin Schipper},
howpublished = {BioRxiv},
year = {2026},
month = oct,
doi = {10.64898/2026.06.11.731450},
url = {https://hal.science/hal-05780512v1},
note = {CC BY-NC},
}
RIS
TY - UNPB
TI - Disentangling the sucrose metabolism of the corn smut Ustilago maydis reveals unexpected complexity
AU - Tom Berwanger
AU - Ali Khoshouei
AU - Heba Yehia
AU - Joana Charlot Hasenklever
AU - Tanvir Hassan
AU - Anna Barbara Matuszyńska
AU - Jörg Kämper
AU - Khaled A. Selim
AU - Florian Altegoer
AU - Kerstin Schipper
PY - 2026
DA - 2026/10/06
PB - BioRxiv
DO - 10.64898/2026.06.11.731450
UR - https://hal.science/hal-05780512v1
AB - 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.
SN - 2692-8205
ER -