Ustilago maydis is a phytopathogenic fungus causing corn smut disease. It also is known for its extreme tolerance to UV‐ and ionizing radiation. It has not been elucidated whether light‐sensing proteins, and in particular photolyases play a role in its UV‐tolerance. Based on homology analysis, U. maydis has 10 genes encoding putative light‐responsive proteins. Four amongst these belong to the cryptochrome/photolyase family (CPF) and one represents a white collar 1 ortholog (wco1). Deletion mutants in the predicted cyclobutane pyrimidine dimer CPD‐ and (6–4)‐photolyase were impaired in photoreactivation. In line with this, in vitro studies with recombinant CPF proteins demonstrated binding of the catalytic FAD cofactor, its photoreduction to fully reduced FADH − and repair activity for cyclobutane pyrimidine dimers (CPDs) or (6–4)‐photoproducts, respectively. We also investigated the role of Wco1. Strikingly, transcriptional profiling showed 61 genes differentially expressed upon blue light exposure of wild‐type, but only eight genes in the Δwco1 mutant. These results demonstrate that Wco1 is a functional blue light photoreceptor in U. maydis regulating expression of several genes including both photolyases. Finally, we show that the Δwco1 mutant is less tolerant against UV‐B due to its incapability to induce photolyase expression.

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Smut fungi comprise one of the largest groups of fungal plant pathogens causing disease in all cereal crops. They directly penetrate host tissues and establish a biotrophic interaction. To do so, smut fungi secrete a wide range of effector proteins, which suppress plant immunity and modulate cellular functions as well as development of the host, thereby determining the pathogen’s lifestyle and virulence potential. The conserved effector Erc1 (enzyme required for cell-to-cell extension) contributes to virulence of the corn smut Ustilago maydis in maize leaves but not on the tassel. Erc1 binds to host cell wall components and displays 1,3-β-glucanase activity, which is required to attenuate β-glucan-induced defense responses. Here we show that Erc1 has a cell type-specific virulence function, being necessary for fungal cell-to-cell extension in the plant bundle sheath and this function is fully conserved in the Erc1 orthologue of the barley pathogen Ustilago hordei.

The smut fungi are one of the largest groups of fungal plant pathogens, causing disease in all cereal crops. They directly penetrate their hosts and establish a biotrophic interaction. During colonization of the plant, smut fungi secrete a wide range of effector proteins, which suppress plant immunity and modulate cellular functions as well as development of the host, thereby determining the pathogens life-style and virulence potential. The conserved effector Erc1 (enzyme required for cell-to-cell movement) contributes to virulence of the corn smut Ustilago maydis in maize leaves, but not on the tassel. Erc1 binds to host cell wall components and has a 1,3-B-glucanase activity, which is required to attenuate B-glucan-induced defense responses in host leaves. Confocal microscopy revealed that Erc1 has a cell type-specific virulence function, being necessary for fungal cell-to-cell movement in the plant bundle sheath. This cell type-specific virulence function of Erc1 is fully conserved in the barley pathogen Ustilago hordei, which has a functionally conserved Erc1 orthologue. Thus, Erc1 is an enzymatically active core virulence factor with a cell type-specific virulence function in different hosts, which is important for cell-to-cell movement during host colonization of pathogenic smut fungi.