Abstract

A novel, high-affinity sucrose transporter identified in the plasma membrane of the plant pathogen Ustilago maydis is essential for fungal virulence and successful infection of maize. Plant pathogenic fungi cause massive yield losses and affect both quality and safety of food and feed produced from infected plants. The main objective of plant pathogenic fungi is to get access to the organic carbon sources of their carbon-autotrophic hosts. However, the chemical nature of the carbon source(s) and the mode of uptake are largely unknown. Here, we present a novel, plasma membrane-localized sucrose transporter (Srt1) from the corn smut fungus Ustilago maydis and its characterization as a fungal virulence factor. Srt1 has an unusually high substrate affinity, is absolutely sucrose specific, and allows the direct utilization of sucrose at the plant/fungal interface without extracellular hydrolysis and, thus, without the production of extracellular monosaccharides known to elicit plant immune responses. srt1 is expressed exclusively during infection, and its deletion strongly reduces fungal virulence. This emphasizes the central role of this protein both for efficient carbon supply and for avoidance of apoplastic signals potentially recognized by the host. Author Summary The plant parasitic fungus Ustilago maydis is a biotrophic pathogen that depends on live plant tissue for development. It is highly adapted to maize (Zea mays), where it causes the corn smut disease. Fungal cells growing within the plant apoplast are surrounded by the host plasma membrane at all growth stages, thereby establishing tight interaction zones with the host cells that assure optimal access to host-derived nutrients, including organic carbon sources. Here, we focus on the previously unknown feeding mechanisms of this plant pathogen within its host plant. We identified a fungal plasma membrane transporter, Srt1, that is expressed exclusively after plant infection and that turns out to be essential for virulence development of Ustilago in infected plants. Srt1 is the first characterized fungal transporter that allows direct utilization of sucrose without extracellular hydrolysis into monosaccharides, the carbon form more commonly taken up by pathogenic fungi. It is highly specific for sucrose, and its affinity largely exceeds that of equivalent plant transporters. This not only provides advantages for the carbon acquisition by the pathogen, but quite likely also offers a mechanism to prevent induction of plant defense responses known to occur upon apoplastic sucrose hydrolysis.