Histone complement of a rapidly evolving chordate Oikopleura dioica: Developmental and sex-specific deployment of novel and universal histone variants and their posttranslational modifications

Abstract

The packaging of DNA into nucleosomes is a fundamentally conserved property of the eukaryotic nucleus which is evident in the conservation of histone sequences. Nevertheless, it is now clear that histone sequence variants have diversified in many species to assume crucial roles in the regulation of gene expression, DNA repair, chromosome segregation and other processes. While considerable data exist on coding sequences of histones and some selected histone variants in a wide variety of organisms, the information available on total histone gene complements is much more limited. Oikopleura dioica (Od) is a dioecious marine urochordate that occupies a key phylogenetic position near the invertebrate-vertebrate transition with the smallest genome ever found in a chordate (70 Mb). Its short life cycle is characterized by a developmental switch between mitotic and endocycling cells, making O. dioica an attractive model to study the spatial and temporal use of histone variants and posttranslational histone modifications (PTMs) throughout development and in different cell cycle types. We have characterized the complete histone gene complement and the developmental expression of histone genes present in the first assembly of the O. dioica draft genome and identified the major Od PTMs by massspectrometric analysis. Furthermore, we analyzed the dynamics and distribution of phosphorylated H3 variants during mitosis and meiosis of O. dioica and the deposition of the centromeric variant OdCenH3 in mitotic and endocycling cells with respect to centromeric PTMs. The Od histone gene complement displays several features not known from other chordates, including male-specific variants in all of the core histone families, N-terminal H2A.Z splice variants, and a diverse array of H2A variants but absence of the near universal variant H2AX. The results here suggest significant plasticity in histone gene organization, the variation within histone families and the chromosomal distribution of mitotic PTMs within the chordate lineage. This further supports the view that histone gene complements may also evolve adaptively to the specific life history traits, cell cycle regulation and genome architecture of organisms.