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The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA

BACKGROUND: Cnidarians are a group of early branching animals including corals, jellyfish and hydroids that are renowned for their high regenerative ability, growth plasticity and longevity. Because cnidarian genomes are conventional in terms of protein-coding genes, their remarkable features are li...

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Autores principales: Török, Anna, Schiffer, Philipp H., Schnitzler, Christine E., Ford, Kris, Mullikin, James C., Baxevanis, Andreas D., Bacic, Antony, Frank, Uri, Gornik, Sebastian G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5011920/
https://www.ncbi.nlm.nih.gov/pubmed/27602058
http://dx.doi.org/10.1186/s13072-016-0085-1
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author Török, Anna
Schiffer, Philipp H.
Schnitzler, Christine E.
Ford, Kris
Mullikin, James C.
Baxevanis, Andreas D.
Bacic, Antony
Frank, Uri
Gornik, Sebastian G.
author_facet Török, Anna
Schiffer, Philipp H.
Schnitzler, Christine E.
Ford, Kris
Mullikin, James C.
Baxevanis, Andreas D.
Bacic, Antony
Frank, Uri
Gornik, Sebastian G.
author_sort Török, Anna
collection PubMed
description BACKGROUND: Cnidarians are a group of early branching animals including corals, jellyfish and hydroids that are renowned for their high regenerative ability, growth plasticity and longevity. Because cnidarian genomes are conventional in terms of protein-coding genes, their remarkable features are likely a consequence of epigenetic regulation. To facilitate epigenetics research in cnidarians, we analysed the histone complement of the cnidarian model organism Hydractinia echinata using phylogenomics, proteomics, transcriptomics and mRNA in situ hybridisations. RESULTS: We find that the Hydractinia genome encodes 19 histones and analyse their spatial expression patterns, genomic loci and replication-dependency. Alongside core and other replication-independent histone variants, we find several histone replication-dependent variants, including a rare replication-dependent H3.3, a female germ cell-specific H2A.X and an unusual set of five H2B variants, four of which are male germ cell-specific. We further confirm the absence of protamines in Hydractinia. CONCLUSIONS: Since no protamines are found in hydroids, we suggest that the novel H2B variants are pivotal for sperm DNA packaging in this class of Cnidaria. This study adds to the limited number of full histone gene complements available in animals and sets a comprehensive framework for future studies on the role of histones and their post-translational modifications in cnidarian epigenetics. Finally, it provides insight into the evolution of spermatogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13072-016-0085-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-50119202016-09-07 The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA Török, Anna Schiffer, Philipp H. Schnitzler, Christine E. Ford, Kris Mullikin, James C. Baxevanis, Andreas D. Bacic, Antony Frank, Uri Gornik, Sebastian G. Epigenetics Chromatin Research BACKGROUND: Cnidarians are a group of early branching animals including corals, jellyfish and hydroids that are renowned for their high regenerative ability, growth plasticity and longevity. Because cnidarian genomes are conventional in terms of protein-coding genes, their remarkable features are likely a consequence of epigenetic regulation. To facilitate epigenetics research in cnidarians, we analysed the histone complement of the cnidarian model organism Hydractinia echinata using phylogenomics, proteomics, transcriptomics and mRNA in situ hybridisations. RESULTS: We find that the Hydractinia genome encodes 19 histones and analyse their spatial expression patterns, genomic loci and replication-dependency. Alongside core and other replication-independent histone variants, we find several histone replication-dependent variants, including a rare replication-dependent H3.3, a female germ cell-specific H2A.X and an unusual set of five H2B variants, four of which are male germ cell-specific. We further confirm the absence of protamines in Hydractinia. CONCLUSIONS: Since no protamines are found in hydroids, we suggest that the novel H2B variants are pivotal for sperm DNA packaging in this class of Cnidaria. This study adds to the limited number of full histone gene complements available in animals and sets a comprehensive framework for future studies on the role of histones and their post-translational modifications in cnidarian epigenetics. Finally, it provides insight into the evolution of spermatogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13072-016-0085-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-06 /pmc/articles/PMC5011920/ /pubmed/27602058 http://dx.doi.org/10.1186/s13072-016-0085-1 Text en © The Author(s) 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
Török, Anna
Schiffer, Philipp H.
Schnitzler, Christine E.
Ford, Kris
Mullikin, James C.
Baxevanis, Andreas D.
Bacic, Antony
Frank, Uri
Gornik, Sebastian G.
The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA
title The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA
title_full The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA
title_fullStr The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA
title_full_unstemmed The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA
title_short The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA
title_sort cnidarian hydractinia echinata employs canonical and highly adapted histones to pack its dna
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5011920/
https://www.ncbi.nlm.nih.gov/pubmed/27602058
http://dx.doi.org/10.1186/s13072-016-0085-1
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