Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway

In Aspergillus nidulans a regulon including 11 hxn genes (hxnS, T, R, P, Y, Z, X, W, V, M and N) is inducible by a nicotinate metabolic derivative, repressible by ammonium and under stringent control of the nitrogen-state-sensitive GATA factor AreA and the specific transcription factor HxnR. This is...

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Main Authors: Eszter Bokor, Michel Flipphi, Sándor Kocsubé, Judit Ámon, Csaba Vágvölgyi, Claudio Scazzocchio, Zsuzsanna Hamari
Format: Article
Language:English
Published: The Royal Society 2021-09-01
Series:Open Biology
Subjects:
Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.210099
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spelling doaj-2716c5548857477483e71e1ac93cee592021-09-28T23:05:13ZengThe Royal SocietyOpen Biology2046-24412021-09-0111910.1098/rsob.210099Genome organization and evolution of a eukaryotic nicotinate co-inducible pathwayEszter Bokor0Michel Flipphi1Sándor Kocsubé2Judit Ámon3Csaba Vágvölgyi4Claudio Scazzocchio5Zsuzsanna Hamari6Department of Microbiology, University of Szeged Faculty of Science and Informatics, Szeged, HungaryInstitute de Génétique et Microbiologie, Université Paris-Sud, Orsay, FranceDepartment of Microbiology, University of Szeged Faculty of Science and Informatics, Szeged, HungaryDepartment of Microbiology, University of Szeged Faculty of Science and Informatics, Szeged, HungaryDepartment of Microbiology, University of Szeged Faculty of Science and Informatics, Szeged, HungaryDepartment of Microbiology, Imperial College, London, UKDepartment of Microbiology, University of Szeged Faculty of Science and Informatics, Szeged, HungaryIn Aspergillus nidulans a regulon including 11 hxn genes (hxnS, T, R, P, Y, Z, X, W, V, M and N) is inducible by a nicotinate metabolic derivative, repressible by ammonium and under stringent control of the nitrogen-state-sensitive GATA factor AreA and the specific transcription factor HxnR. This is the first report in a eukaryote of the genomic organization of a possibly complete pathway of nicotinate utilization. In A. nidulans the regulon is organized in three distinct clusters, this organization is variable in the Ascomycota. In some Pezizomycotina species all 11 genes map in a single cluster; in others they map in two clusters. This variable organization sheds light on cluster evolution. Instances of gene duplication followed by or simultaneous with integration in the cluster, partial or total cluster loss, and horizontal gene transfer of several genes (including an example of whole cluster re-acquisition in Aspergillus of section Flavi) were detected, together with the incorporation in some clusters of genes not found in the A. nidulans co-regulated regulon, which underlie both the plasticity and the reticulate character of metabolic cluster evolution. This study provides a comprehensive phylogeny of six members of the cluster across representatives of all Ascomycota classes.https://royalsocietypublishing.org/doi/10.1098/rsob.210099Aspergillus nidulansascomyceteseukaryotic nicotinate utilizationgene cluster evolutiongene cluster co-regulationhorizontal gene transmission
collection DOAJ
language English
format Article
sources DOAJ
author Eszter Bokor
Michel Flipphi
Sándor Kocsubé
Judit Ámon
Csaba Vágvölgyi
Claudio Scazzocchio
Zsuzsanna Hamari
spellingShingle Eszter Bokor
Michel Flipphi
Sándor Kocsubé
Judit Ámon
Csaba Vágvölgyi
Claudio Scazzocchio
Zsuzsanna Hamari
Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
Open Biology
Aspergillus nidulans
ascomycetes
eukaryotic nicotinate utilization
gene cluster evolution
gene cluster co-regulation
horizontal gene transmission
author_facet Eszter Bokor
Michel Flipphi
Sándor Kocsubé
Judit Ámon
Csaba Vágvölgyi
Claudio Scazzocchio
Zsuzsanna Hamari
author_sort Eszter Bokor
title Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
title_short Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
title_full Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
title_fullStr Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
title_full_unstemmed Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
title_sort genome organization and evolution of a eukaryotic nicotinate co-inducible pathway
publisher The Royal Society
series Open Biology
issn 2046-2441
publishDate 2021-09-01
description In Aspergillus nidulans a regulon including 11 hxn genes (hxnS, T, R, P, Y, Z, X, W, V, M and N) is inducible by a nicotinate metabolic derivative, repressible by ammonium and under stringent control of the nitrogen-state-sensitive GATA factor AreA and the specific transcription factor HxnR. This is the first report in a eukaryote of the genomic organization of a possibly complete pathway of nicotinate utilization. In A. nidulans the regulon is organized in three distinct clusters, this organization is variable in the Ascomycota. In some Pezizomycotina species all 11 genes map in a single cluster; in others they map in two clusters. This variable organization sheds light on cluster evolution. Instances of gene duplication followed by or simultaneous with integration in the cluster, partial or total cluster loss, and horizontal gene transfer of several genes (including an example of whole cluster re-acquisition in Aspergillus of section Flavi) were detected, together with the incorporation in some clusters of genes not found in the A. nidulans co-regulated regulon, which underlie both the plasticity and the reticulate character of metabolic cluster evolution. This study provides a comprehensive phylogeny of six members of the cluster across representatives of all Ascomycota classes.
topic Aspergillus nidulans
ascomycetes
eukaryotic nicotinate utilization
gene cluster evolution
gene cluster co-regulation
horizontal gene transmission
url https://royalsocietypublishing.org/doi/10.1098/rsob.210099
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