Plant Surface Cues Prime Ustilago maydis for Biotrophic Development

Infection-related development of phytopathogenic fungi is initiated by sensing and responding to plant surface cues. This response can result in the formation of specialized infection structures, so-called appressoria. To unravel the program inducing filaments and appressoria in the biotrophic smut...

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Main Authors: Lanver, Daniel, Berndt, Patrick, Tollot, Marie, Naik, Vikram, Vranes, Miroslav, Warmann, Tobias, Münch, Karin, Rössel, Nicole, Kahmann, Regine
Format: Online
Language:English
Published: Public Library of Science 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4102580/
id pubmed-4102580
recordtype oai_dc
spelling pubmed-41025802014-07-21 Plant Surface Cues Prime Ustilago maydis for Biotrophic Development Lanver, Daniel Berndt, Patrick Tollot, Marie Naik, Vikram Vranes, Miroslav Warmann, Tobias Münch, Karin Rössel, Nicole Kahmann, Regine Research Article Infection-related development of phytopathogenic fungi is initiated by sensing and responding to plant surface cues. This response can result in the formation of specialized infection structures, so-called appressoria. To unravel the program inducing filaments and appressoria in the biotrophic smut fungus Ustilago maydis, we exposed cells to a hydrophobic surface and the cutin monomer 16-hydroxy hexadecanoic acid. Genome-wide transcriptional profiling at the pre-penetration stage documented dramatic transcriptional changes in almost 20% of the genes. Comparisons with the U. maydis sho1 msb2 double mutant, lacking two putative sensors for plant surface cues, revealed that these plasma membrane receptors regulate a small subset of the surface cue-induced genes comprising mainly secreted proteins including potential plant cell wall degrading enzymes. Targeted gene deletion analysis ascribed a role to up-regulated GH51 and GH62 arabinofuranosidases during plant penetration. Among the sho1/msb2-dependently expressed genes were several secreted effectors that are essential for virulence. Our data also demonstrate specific effects on two transcription factors that redirect the transcriptional regulatory network towards appressorium formation and plant penetration. This shows that plant surface cues prime U. maydis for biotrophic development. Public Library of Science 2014-07-17 /pmc/articles/PMC4102580/ /pubmed/25033195 http://dx.doi.org/10.1371/journal.ppat.1004272 Text en © 2014 Lanver et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Lanver, Daniel
Berndt, Patrick
Tollot, Marie
Naik, Vikram
Vranes, Miroslav
Warmann, Tobias
Münch, Karin
Rössel, Nicole
Kahmann, Regine
spellingShingle Lanver, Daniel
Berndt, Patrick
Tollot, Marie
Naik, Vikram
Vranes, Miroslav
Warmann, Tobias
Münch, Karin
Rössel, Nicole
Kahmann, Regine
Plant Surface Cues Prime Ustilago maydis for Biotrophic Development
author_facet Lanver, Daniel
Berndt, Patrick
Tollot, Marie
Naik, Vikram
Vranes, Miroslav
Warmann, Tobias
Münch, Karin
Rössel, Nicole
Kahmann, Regine
author_sort Lanver, Daniel
title Plant Surface Cues Prime Ustilago maydis for Biotrophic Development
title_short Plant Surface Cues Prime Ustilago maydis for Biotrophic Development
title_full Plant Surface Cues Prime Ustilago maydis for Biotrophic Development
title_fullStr Plant Surface Cues Prime Ustilago maydis for Biotrophic Development
title_full_unstemmed Plant Surface Cues Prime Ustilago maydis for Biotrophic Development
title_sort plant surface cues prime ustilago maydis for biotrophic development
description Infection-related development of phytopathogenic fungi is initiated by sensing and responding to plant surface cues. This response can result in the formation of specialized infection structures, so-called appressoria. To unravel the program inducing filaments and appressoria in the biotrophic smut fungus Ustilago maydis, we exposed cells to a hydrophobic surface and the cutin monomer 16-hydroxy hexadecanoic acid. Genome-wide transcriptional profiling at the pre-penetration stage documented dramatic transcriptional changes in almost 20% of the genes. Comparisons with the U. maydis sho1 msb2 double mutant, lacking two putative sensors for plant surface cues, revealed that these plasma membrane receptors regulate a small subset of the surface cue-induced genes comprising mainly secreted proteins including potential plant cell wall degrading enzymes. Targeted gene deletion analysis ascribed a role to up-regulated GH51 and GH62 arabinofuranosidases during plant penetration. Among the sho1/msb2-dependently expressed genes were several secreted effectors that are essential for virulence. Our data also demonstrate specific effects on two transcription factors that redirect the transcriptional regulatory network towards appressorium formation and plant penetration. This shows that plant surface cues prime U. maydis for biotrophic development.
publisher Public Library of Science
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4102580/
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