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Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat

BACKGROUND: Fungal plant pathogens pose major threats to crop yield and sustainable food production if they are highly adapted to their host and the local environment. Variation in gene expression contributes to phenotypic diversity within fungal species and affects adaptation. However, very few cas...

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Autores principales: Krishnan, Parvathy, Meile, Lukas, Plissonneau, Clémence, Ma, Xin, Hartmann, Fanny E., Croll, Daniel, McDonald, Bruce A., Sánchez-Vallet, Andrea
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6047131/
https://www.ncbi.nlm.nih.gov/pubmed/30012138
http://dx.doi.org/10.1186/s12915-018-0543-2
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author Krishnan, Parvathy
Meile, Lukas
Plissonneau, Clémence
Ma, Xin
Hartmann, Fanny E.
Croll, Daniel
McDonald, Bruce A.
Sánchez-Vallet, Andrea
author_facet Krishnan, Parvathy
Meile, Lukas
Plissonneau, Clémence
Ma, Xin
Hartmann, Fanny E.
Croll, Daniel
McDonald, Bruce A.
Sánchez-Vallet, Andrea
author_sort Krishnan, Parvathy
collection PubMed
description BACKGROUND: Fungal plant pathogens pose major threats to crop yield and sustainable food production if they are highly adapted to their host and the local environment. Variation in gene expression contributes to phenotypic diversity within fungal species and affects adaptation. However, very few cases of adaptive regulatory changes have been reported in fungi and the underlying mechanisms remain largely unexplored. Fungal pathogen genomes are highly plastic and harbor numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. In this work, we elucidated how transposable elements contribute to variation in melanin accumulation, a quantitative trait in fungi that affects survival under stressful conditions. RESULTS: We demonstrated that differential transcriptional regulation of the gene encoding the transcription factor Zmr1, which controls expression of the genes in the melanin biosynthetic gene cluster, is responsible for variation in melanin accumulation in the fungal plant pathogen Zymoseptoria tritici. We show that differences in melanin levels between two strains of Z. tritici are due to two levels of transcriptional regulation: (1) variation in the promoter sequence of Zmr1 and (2) an insertion of transposable elements upstream of the Zmr1 promoter. Remarkably, independent insertions of transposable elements upstream of Zmr1 occurred in 9% of Z. tritici strains from around the world and negatively regulated Zmr1 expression, contributing to variation in melanin accumulation. CONCLUSIONS: Our studies identified two levels of transcriptional control that regulate the synthesis of melanin. We propose that these regulatory mechanisms evolved to balance the fitness costs associated with melanin production against its positive contribution to survival in stressful environments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0543-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-60471312018-07-19 Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat Krishnan, Parvathy Meile, Lukas Plissonneau, Clémence Ma, Xin Hartmann, Fanny E. Croll, Daniel McDonald, Bruce A. Sánchez-Vallet, Andrea BMC Biol Research Article BACKGROUND: Fungal plant pathogens pose major threats to crop yield and sustainable food production if they are highly adapted to their host and the local environment. Variation in gene expression contributes to phenotypic diversity within fungal species and affects adaptation. However, very few cases of adaptive regulatory changes have been reported in fungi and the underlying mechanisms remain largely unexplored. Fungal pathogen genomes are highly plastic and harbor numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. In this work, we elucidated how transposable elements contribute to variation in melanin accumulation, a quantitative trait in fungi that affects survival under stressful conditions. RESULTS: We demonstrated that differential transcriptional regulation of the gene encoding the transcription factor Zmr1, which controls expression of the genes in the melanin biosynthetic gene cluster, is responsible for variation in melanin accumulation in the fungal plant pathogen Zymoseptoria tritici. We show that differences in melanin levels between two strains of Z. tritici are due to two levels of transcriptional regulation: (1) variation in the promoter sequence of Zmr1 and (2) an insertion of transposable elements upstream of the Zmr1 promoter. Remarkably, independent insertions of transposable elements upstream of Zmr1 occurred in 9% of Z. tritici strains from around the world and negatively regulated Zmr1 expression, contributing to variation in melanin accumulation. CONCLUSIONS: Our studies identified two levels of transcriptional control that regulate the synthesis of melanin. We propose that these regulatory mechanisms evolved to balance the fitness costs associated with melanin production against its positive contribution to survival in stressful environments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0543-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-07-16 /pmc/articles/PMC6047131/ /pubmed/30012138 http://dx.doi.org/10.1186/s12915-018-0543-2 Text en © Sánchez-Vallet et al. 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Krishnan, Parvathy
Meile, Lukas
Plissonneau, Clémence
Ma, Xin
Hartmann, Fanny E.
Croll, Daniel
McDonald, Bruce A.
Sánchez-Vallet, Andrea
Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
title Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
title_full Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
title_fullStr Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
title_full_unstemmed Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
title_short Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
title_sort transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6047131/
https://www.ncbi.nlm.nih.gov/pubmed/30012138
http://dx.doi.org/10.1186/s12915-018-0543-2
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