Divergent evolutionary behavior of H3 histone gene and rDNA clusters in venerid clams

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Abstract

Background: Histone H3 gene clusters have been described as highly conserved chromosomal markers in invertebrates. Surprisingly, in bivalves remarkable interspecific differences were found among the eight mussels and between the two clams in which histone H3 gene clusters have already been located. Although the family Veneridae comprises 10 % of the species of marine bivalves, their chromosomes are poorly studied. The clams belonging to this family present 2n∈=∈38 chromosomes and similar karyotypes showing chromosome pairs gradually decreasing in length. In order to assess the evolutionary behavior of histone and rRNA multigene families in bivalves, we mapped histone H3 and ribosomal RNA probes to chromosomes of ten species of venerid clams. Results: In contrast with the reported conservation of histone H3 gene clusters and their intercalary location in invertebrates, these loci varied in number and were mostly subterminal in venerid clams. On the other hand, while a single 45S rDNA cluster, highly variable in location, was found in these organisms, 5S rDNA clusters showed interspecific differences in both number and location. The distribution patterns of these sequences were species-specific and mapped to different chromosomal positions in all clams but Ruditapes decussatus, in which one of the minor rDNA clusters and the major rDNA cluster co-located. Conclusion: The diversity in the distribution patterns of histone H3 gene, 5S rDNA and 28S rDNA clusters found in venerid clams, together with their different evolutionary behaviors in other invertebrate taxa, strongly suggest that the control of the spreading of these multigene families in a group of organisms relies upon a combination of evolutionary forces that operate differently depending not only on the specific multigene family but also on the particular taxa. Our data also showed that H3 histone gene and rDNA clusters are useful landmarks to integrate nex-generation sequencing (NGS) and evolutionary genomic data in non-model species.

Figures

  • Fig. 1 Chromosomal location of H3 histone genes in venerid clams. H3 histone gene (H3) probes mapped by FISH to mitotic chomosomes of Ruditapes philippinarum (RPH), Ruditapes decussatus (RDE), Venerupis corrugata (VCO), Venus verrucosa (VVE) and Dosinia exoleta (DEX). To ascertain the chromosomal position of core histone gene clusters in relation to rDNA clusters, the same metaphases were rehybridized using 5S rDNA (5S) and major rDNA (28S) probes. Excluding 5S and major rDNA in RDE (arrows), all signals are on different chromosome pairs. Scale bars, 5 μm
  • Fig. 2 Chromosomal location of H3 histone genes (H3), 5S rDNA (5S) and major rDNA (28S) in venerid clams. Single FISH using H3 histone gene probes mapped to chromosomes of Clausinella fasciata (CFA), Chamelea gallina (CGA), Venus casina (VCA), Dosinia lupinus (DLU), and Petricola litophaga (PLI), followed by double-FISH using 5S rDNA (5S) and major rDNA (28S) probes on the same metaphase plates. All signals for the different probes appear at different chromosome pairs with the exception of H3 histone gene and major rDNA in Clausinella fasciata (CFA, first row). Scale bars, 5 μm
  • Fig. 3 Subterminal H3 histone gene clusters in venerid clams. Examples of FISH to surface spread synaptonemal complexes of Ruditapes philippinarum (RPH) and Venerupis corrugata (VCO) clearly denote the subterminal location of the H3 histone gene clusters (H3, green). 5S rDNA clusters (5S, red) are also subterminal in VCO but intercalary in RPH. Scale bars, 5 μm
  • Table 1 Chromosomal location of core histone gene and rDNA clusters in venerid clams
  • Fig. 4 5S rDNA clusters on Petricola litophaga. FISH of H3 histone gene (H3), 5S (5S) and 28S (28S) rDNA probes to prophase I meiotic bivalents of Petricola litophaga (PLI) clearly show the presence of two distinct 5S rDNA signals (arrows) on a single bivalent. Scale bars, 5 μm
  • Fig. 5 Ideograms showing the chromosomal location of H3 histone genes, 5S rDNA and major rDNA in thirteen species of Veneridae. The green areas represent the H3 histone gene clusters, the red areas the 5S rDNA clusters and the yellow areas the major rDNA clusters. The magenta area in Ruditapes decussatus indicates overlapping of major and 5S rDNA signals

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García-Souto, D., Pérez-García, C., Morán, P., & Pasantes, J. J. (2015). Divergent evolutionary behavior of H3 histone gene and rDNA clusters in venerid clams. Molecular Cytogenetics, 8(1). https://doi.org/10.1186/s13039-015-0150-7

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