Molecular Evolutionary Characterization of the Mussel Mytilus Histone Multigene Family: First Record of a Tandemly Repeated Unit of Five Histone Genes Containing an H1 Subtype with ?Orphon? Features

Abstract

The present work represents the first characterization of a clustered histone repetitive unit containing an H1 gene in a bivalve mollusk. To complete the knowledge on the evolutionary history of the histone multigene family in invertebrates, we undertake its characterization in five mussel Mytilus species, as an extension of our previous work on the H1 gene family. We report the quintet H4-H2B-H2A-H3-H1 as the major organization unit in the genome of Mytilus galloprovincialis with two 5S rRNA genes with interspersed nontranscribed spacer segments linked to the unit, which is not justified by their cotranscription with histone genes. Surprisingly, 3' UTR regions of histone genes show two different mRNA termination signals, a stem-loop and a polyadenylation signal, both related to the evolution of histone gene expression patterns throughout the cell cycle. The clustered H1 histones characterized share essential features with "orphon" H1 genes, suggesting a common evolutionary origin for both histone subtypes which is supported by the reconstructed phylogeny for H1 genes. The characterization of histone genes in four additional Mytilus species revealed the presence of strong purifying selection acting among the members of the family. The chromosomal location of most of the core histone genes studied was identified by FISH close to telomeric regions in M. galloprovincialis. Further analysis on nucleotide variation would be necessary to assess if H1 proteins evolve according to the birth-and-death model of evolution and if the effect of the strong purifying selection maintaining protein homogeneity could account for the homologies detected between clustered and "orphon" variants.

Chromosomal mapping of repetitive DNAs in the beetle Dichotomius geminatus provides the first evidence for an association of 5S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and A complement

“…Although the association and/or interspersion of multigene families has been reported in protostome invertebrates (Drouin and Moniz de Sá, 1995;Barzotti et al, 2000;Vitturi et al, 2002;Eirín-Ló pez et al, 2004;Vitturi et al, 2004;Cabrero et al, 2009), the significance of such association is still unclear. According to Kaplan et al (1993), the association of these sequences might have a functional role in nuclear organization, whereas other researchers (Dover, 1986;Liu and Fredga, 1999) agree that this association is important for the maintenance of conserved and multiple arrays.…”

Systematic analysis and evolution of 5S ribosomal DNA in metazoans

“…These repeats can occur in tandem forming long arrays in some species, whereas in other cases they are dispersed throughout the genome. In some organisms, 5S rDNA repeats have been found linked to other noncoding RNA (ncRNA) gene families, such as small nuclear RNAs (snRNAs) (Vahidi et al, 1988;Nilsen et al, 1989;Zeng et al, 1990;Keller et al, 1992;Pelliccia et al, 2001;Cross and Rebordinos, 2005;Manchado et al, 2006;Marz et al, 2008;Freire et al, 2010;Vierna et al, 2011;Vizoso et al, 2011) or to protein-coding genes such as histones (Eirin-Lopez et al, 2004).…”

Histone H3 gene in the Pacific oyster, Crassostrea gigas Thunberg, 1793: molecular and cytogenetic characterisations

“…Only fi ve species were studied until now: a mussel (Eirín-López et al, 2002 and four scallops (Zhang et al, 2007). In Mytilidae, FISH experiments on Mytilus galloprovincialis Lamarck, 1819 chromosomes revealed the presence of three pairs of signals in three chromosome pairs with the linker histone H1 probe (Eirín-López et al, 2002), and two pairs of signals in two chromosome pairs with a core histone gene probe (Eirín-López et al, 2004 (Zhang et al, 2007). Regarding mollusc molecular phylogenetic studies using histone genes, little information is available.…”

“…Regarding mollusc molecular phylogenetic studies using histone genes, little information is available. No studies were realised in Ostreidae, but some studies have already been performed in Pectinidae (Puslednik, Serb, 2008), Mytilidae (Eirín-López et al, 2004), Veneridae (Kappner, Bieler, 2006) and in gastropods (Colgan et al, 2000).…”