Abstract
BackgroundCnidarians 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.ResultsWe 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.ConclusionsSince 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 materialThe online version of this article (doi:10.1186/s13072-016-0085-1) contains supplementary material, which is available to authorized users.
Highlights
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
The Hydractinia genome encodes 19 histones and no protamines We identified a total of 19 histones in the genome of Hydractinia echinata using sequence alignment and phylogenomics
This study adds to the limited data available for histone gene complements in metazoans and provides a framework for studies on the role of histones and their post-translational modifications in cnidarian epigenetics
Summary
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. Most eukaryotes package and order their nuclear DNA into chromatin using a class of proteins called histones [1,2,3,4]. The histones form an octameric core complex containing two of each of the four core histones (H2A, H2B, H3 and H4); in turn, DNA wraps around this histone core complex to form the basic unit of chromatin compaction called nucleosome [4, 7]. Nucleosomes compact the genome while still providing dynamic access for processes such as DNA transcription, replication and repair. To bring about these regulatory functions, a diverse array of distinct, combinatorial post-translational modifications occurs on tail domains of histones [8, 9]. Hundreds of epigenetically active histone modifications have been identified, for example monoubiquitination, acetylation, mono-, di- and tri-methylation of lysines, as well as mono- and dimethylation of arginines, phosphorylation of serines, threonines and tyrosines, and isomerisation of prolines [10]
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