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White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis.

ABSTRACT: 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.

SUBMITTER: Brych A

PROVIDER: S-EPMC4831468 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis.

Brych Annika A Mascarenhas Judita J Jaeger Elaine E Charkiewicz Elzbieta E Pokorny Richard R Bölker Michael M Doehlemann Gunther G Batschauer Alfred A

MicrobiologyOpen 20151220 2

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 mutan ...[more]

PMID: 26687452

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Project description:Ustilago maydis is a phytopathogenic fungus responsible for corn smut disease. Although it is a very well-established model organism for the study of plant-microbe interactions, its potential to produce specialized metabolites, which might contribute to this interaction, has not been studied in detail. By analyzing the U. maydis genome, we identified a biosynthetic gene cluster whose activation led to the production of a black melanin pigment. Single deletion mutants of the cluster genes revealed that five encoded enzymes are required for the accumulation of the black pigment, including three polyketide synthases (pks3, pks4, and pks5), a cytochrome P450 monooxygenase (cyp4), and a protein with similarity to versicolorin B synthase (vbs1). Metabolic profiles of deletion mutants in this gene cluster suggested that Pks3 and Pks4 act in concert as heterodimers to generate orsellinic acid (OA), which is reduced to the corresponding aldehyde by Pks5. The OA-aldehyde can then react with triacetic acid lactone (TAL), also derived from Pks3/Pks4 heterodimers to form larger molecules, including novel coumarin derivatives. Our findings suggest that U. maydis synthesizes a novel type of melanin based on coumarin and pyran-2-one intermediates, while most fungal melanins are derived from 1,8-dihydroxynaphthalene (DHN) or l-3,4-dihydroxyphenylalanine (l-DOPA). Along with these observations, this work also provides insight into the mechanisms of polyketide synthases in this filamentous fungus.IMPORTANCE The fungus Ustilago maydis represents one of the major threats to maize plants since it is responsible for corn smut disease, which generates considerable economical losses around the world. Therefore, contributing to a better understanding of the biochemistry of defense mechanisms used by U. maydis to protect itself against harsh environments, such as the synthesis of melanin, could provide improved biological tools for tackling the problem and protect the crops. In addition, the fact that this fungus synthesizes melanin in an unconventional way, requiring more than one polyketide synthase for producing melanin precursors, gives a different perspective on the complexity of these multidomain enzymes and their evolution in the fungal kingdom.

Dataset Information

White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis.

Publications

White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis.

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