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      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.

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          Most cited references 52

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          Extraction of high molecular weight DNA from molluscs.

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            Genome architecture, rearrangements and genomic disorders.

            An increasing number of human diseases are recognized to result from recurrent DNA rearrangements involving unstable genomic regions. These are termed genomic disorders, in which the clinical phenotype is a consequence of abnormal dosage of gene(s) located within the rearranged genomic fragments. Both inter- and intrachromosomal rearrangements are facilitated by the presence of region-specific low-copy repeats (LCRs) and result from nonallelic homologous recombination (NAHR) between paralogous genomic segments. LCRs usually span approximately 10-400 kb of genomic DNA, share >or= 97% sequence identity, and provide the substrates for homologous recombination, thus predisposing the region to rearrangements. Moreover, it has been suggested that higher order genomic architecture involving LCRs plays a significant role in karyotypic evolution accompanying primate speciation.
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              Finely orchestrated movements: evolution of the ribosomal RNA genes.

              Evolution of the tandemly repeated ribosomal RNA (rRNA) genes is intriguing because in each species all units within the array are highly uniform in sequence but that sequence differs between species. In this review we summarize the origins of the current models to explain this process of concerted evolution, emphasizing early studies of recombination in yeast and more recent studies in Drosophila and mammalian systems. These studies suggest that unequal crossover is the major driving force in the evolution of the rRNA genes with sister chromatid exchange occurring more often than exchange between homologs. Gene conversion is also believed to play a role; however, direct evidence for its involvement has not been obtained. Remarkably, concerted evolution is so well orchestrated that even transposable elements that insert into a large fraction of the rRNA genes appear to have little effect on the process. Finally, we summarize data that suggest that recombination in the rDNA locus of higher eukaryotes is sufficiently frequent to monitor changes within a few generations.
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                Author and article information

                Contributors
                danielgarciasouto@gmail.com
                concepcionperezgar@gmail.com
                paloma@uvigo.es
                +34 986 812 577 , pasantes@uvigo.es
                Journal
                Mol Cytogenet
                Mol Cytogenet
                Molecular Cytogenetics
                BioMed Central (London )
                1755-8166
                24 June 2015
                24 June 2015
                2015
                : 8
                Affiliations
                Departamento Bioquímica, Xenética e Inmunoloxía, Universidade de Vigo, E-36310 Vigo, Spain
                Article
                150
                10.1186/s13039-015-0150-7
                4477615
                © García-Souto et al. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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                © The Author(s) 2015

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