Abstract

BackgroundHistone variants alter the composition of nucleosomes and play crucial roles in transcription, chromosome segregation, DNA repair, and sperm compaction. Modification of metazoan histone variant lineages occurs on a background of genome architecture that shows global similarities from sponges to vertebrates, but the urochordate, Oikopleura dioica, a member of the sister group to vertebrates, exhibits profound modification of this ancestral architecture.ResultsWe show that a histone complement of 47 gene loci encodes 31 histone variants, grouped in distinct sets of developmental expression profiles throughout the life cycle. A particularly diverse array of 15 male-specific histone variants was uncovered, including a testes-specific H4t, the first metazoan H4 sequence variant reported. Universal histone variants H3.3, CenH3, and H2A.Z are present but O. dioica lacks homologs of macroH2A and H2AX. The genome encodes many H2A and H2B variants and the repertoire of H2A.Z isoforms is expanded through alternative splicing, incrementally regulating the number of acetylatable lysine residues in the functionally important N-terminal "charge patch". Mass spectrometry identified 40 acetylation, methylation and ubiquitylation posttranslational modifications (PTMs) and showed that hallmark PTMs of "active" and "repressive" chromatin were present in O. dioica. No obvious reduction in silent heterochromatic marks was observed despite high gene density in this extraordinarily compacted chordate genome.ConclusionsThese results show that histone gene complements and their organization differ considerably even over modest phylogenetic distances. Substantial innovation among all core and linker histone variants has evolved in concert with adaptation of specific life history traits in this rapidly evolving chordate lineage.

Highlights

  • Histone variants alter the composition of nucleosomes and play crucial roles in transcription, chromosome segregation, DNA repair, and sperm compaction

  • Three major strategies contribute to regulatory remodeling of chromatin: ATP-dependent complexes that act on nucleosomes to modify accessibility of wrapped DNA sequences to trans-acting factors [5], the deployment of histone variants that alter nucleosome dynamics, and covalent posttranslational histone modifications (PTMs) including acetylation, methylation, phosphorylation, ubiquitylation, citrullination, ADP-ribosylation, glycoslylation and sumoylation [6,7]

  • Histone gene organization in Oikopleura dioica Histone genes were dispersed throughout the O. dioica (Od) genome with most in clusters up to quintets

Read more

Summary

Introduction

Histone variants alter the composition of nucleosomes and play crucial roles in transcription, chromosome segregation, DNA repair, and sperm compaction. The highly conserved core histones, H4, H3, H2A and H2B form an octamer of two H2A/H2B dimers flanking a central H3/H4 tetramer that wrap ~147 bp of DNA in 1.7 turns to form the nucleosome core particle (NCP) [1]. Roles of histones in structural compaction must be balanced with regulatory mechanisms that permit selective access to DNA to enable functions such as transcription, replication and DNA repair. Three major strategies contribute to regulatory remodeling of chromatin: ATP-dependent complexes that act on nucleosomes to modify accessibility of wrapped DNA sequences to trans-acting factors [5], the deployment of histone variants that alter nucleosome dynamics, and covalent posttranslational histone modifications (PTMs) including acetylation, methylation, phosphorylation, ubiquitylation, citrullination, ADP-ribosylation, glycoslylation and sumoylation [6,7]. One current view is that eukaryotic genomes are indexed locally, and over broader regions, through a combination of histone variants and their diverse PTMs [8,9]

Methods
Results
Discussion
Conclusion

Talk to us

Join us for a 30 min session where you can share your feedback and ask us any queries you have

Schedule a call

Disclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.