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The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity

BACKGROUND: Multicellularity evolved multiple times in eukaryotes. In all cases, this required an elaboration of the regulatory mechanisms controlling gene expression. Amongst the conserved eukaryotic transcription factor families, the basic leucine zipper (bZIP) superfamily is one of the most ancie...

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Autores principales: Jindrich, Katia, Degnan, Bernard M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4736632/
https://www.ncbi.nlm.nih.gov/pubmed/26831906
http://dx.doi.org/10.1186/s12862-016-0598-z
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author Jindrich, Katia
Degnan, Bernard M.
author_facet Jindrich, Katia
Degnan, Bernard M.
author_sort Jindrich, Katia
collection PubMed
description BACKGROUND: Multicellularity evolved multiple times in eukaryotes. In all cases, this required an elaboration of the regulatory mechanisms controlling gene expression. Amongst the conserved eukaryotic transcription factor families, the basic leucine zipper (bZIP) superfamily is one of the most ancient and best characterised. This gene family plays a diversity of roles in the specification, differentiation and maintenance of cell types in plants and animals. bZIPs are also involved in stress responses and the regulation of cell proliferation in fungi, amoebozoans and heterokonts. RESULTS: Using 49 sequenced genomes from across the Eukaryota, we demonstrate that the bZIP superfamily has evolved from a single ancestral eukaryotic gene and undergone multiple independent expansions. bZIP family diversification is largely restricted to multicellular lineages, consistent with bZIPs contributing to the complex regulatory networks underlying differential and cell type-specific gene expression in these lineages. Analyses focused on the Metazoa suggest an elaborate bZIP network was in place in the most recent shared ancestor of all extant animals that was comprised of 11 of the 12 previously recognized families present in modern taxa. In addition this analysis identifies three bZIP families that appear to have been lost in mammals. Thus the ancestral metazoan and eumetazoan bZIP repertoire consists of 12 and 16 bZIPs, respectively. These diversified from 7 founder genes present in the holozoan ancestor. CONCLUSIONS: Our results reveal the ancestral opisthokont, holozoan and metazoan bZIP repertoire and provide insights into the progressive expansion and divergence of bZIPs in the five main eukaryotic kingdoms, suggesting that the early diversification of bZIPs in multiple eukaryotic lineages was a prerequisite for the evolution of complex multicellular organisms. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0598-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-47366322016-02-03 The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity Jindrich, Katia Degnan, Bernard M. BMC Evol Biol Research Article BACKGROUND: Multicellularity evolved multiple times in eukaryotes. In all cases, this required an elaboration of the regulatory mechanisms controlling gene expression. Amongst the conserved eukaryotic transcription factor families, the basic leucine zipper (bZIP) superfamily is one of the most ancient and best characterised. This gene family plays a diversity of roles in the specification, differentiation and maintenance of cell types in plants and animals. bZIPs are also involved in stress responses and the regulation of cell proliferation in fungi, amoebozoans and heterokonts. RESULTS: Using 49 sequenced genomes from across the Eukaryota, we demonstrate that the bZIP superfamily has evolved from a single ancestral eukaryotic gene and undergone multiple independent expansions. bZIP family diversification is largely restricted to multicellular lineages, consistent with bZIPs contributing to the complex regulatory networks underlying differential and cell type-specific gene expression in these lineages. Analyses focused on the Metazoa suggest an elaborate bZIP network was in place in the most recent shared ancestor of all extant animals that was comprised of 11 of the 12 previously recognized families present in modern taxa. In addition this analysis identifies three bZIP families that appear to have been lost in mammals. Thus the ancestral metazoan and eumetazoan bZIP repertoire consists of 12 and 16 bZIPs, respectively. These diversified from 7 founder genes present in the holozoan ancestor. CONCLUSIONS: Our results reveal the ancestral opisthokont, holozoan and metazoan bZIP repertoire and provide insights into the progressive expansion and divergence of bZIPs in the five main eukaryotic kingdoms, suggesting that the early diversification of bZIPs in multiple eukaryotic lineages was a prerequisite for the evolution of complex multicellular organisms. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0598-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-02-01 /pmc/articles/PMC4736632/ /pubmed/26831906 http://dx.doi.org/10.1186/s12862-016-0598-z Text en © Jindrich and Degnan. 2016 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
Jindrich, Katia
Degnan, Bernard M.
The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
title The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
title_full The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
title_fullStr The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
title_full_unstemmed The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
title_short The diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
title_sort diversification of the basic leucine zipper family in eukaryotes correlates with the evolution of multicellularity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4736632/
https://www.ncbi.nlm.nih.gov/pubmed/26831906
http://dx.doi.org/10.1186/s12862-016-0598-z
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