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Long-Term Evolution of 5S Ribosomal DNA Seems to Be Driven by Birth-and-Death Processes and Selection in Ensis Razor Shells (Mollusca: Bivalvia)

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Abstract

A study of nucleotide sequence variation of 5S ribosomal DNA from six Ensis species revealed that several 5S ribosomal DNA variants, based on differences in their nontranscribed spacers (NTS), occur in Ensis genomes. The 5S rRNA gene was not very polymorphic, compared with the NTS region. The phylogenetic analyses performed showed a between-species clustering of 5S ribosomal DNA variants. Sequence divergence levels between variants were very large, revealing a lack of sequence homogenization. These results strongly suggest that the long-term evolution of Ensis 5S ribosomal DNA is driven by birth-and-death processes and selection.

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References

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  PubMed  CAS  Google Scholar 

  • Brown DD, Sugimoto K (1974) The structure and evolution of ribosomal and 5S DNAs in Xenopus laevis and Xenopus mulleri. Cold Spring Harb Symp Quant Biol 38:501–505

    PubMed  CAS  Google Scholar 

  • Caradonna F, Bellavia D, Clemente AM, Sisino G, Barbieri R (2007) Chromosomal localization and molecular characterization of three different 5S ribosomal DNA clusters in the sea urchin Paracentrotus lividus. Genome 50:867–870

    Article  PubMed  CAS  Google Scholar 

  • Daniels LM, Delany ME (2003) Molecular and cytogenetic organization of the 5S ribosomal DNA array in chicken (Gallus gallus). Chromosome Res 11:305–317

    Article  PubMed  CAS  Google Scholar 

  • Danna KJ, Workman R, Coryell V, Keim P (1996) 5S rRNA genes in tribe Phaseoleae: array size, number, and dynamics. Genome 39:445–455

    Article  PubMed  CAS  Google Scholar 

  • Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fernández-Tajes J, Méndez J (2007) Identification of the razor clam species Ensis arcuatus, E. siliqua, E. directus, E. macha, and Solen marginatus using PCR-RFLP analysis of the 5S rDNA region. J Agric Food Chem 55:7278–7282

    Article  PubMed  Google Scholar 

  • Freire R, Insua A, Méndez J (2005) Cerastoderma glaucum 5S ribosomal DNA: characterization of the repeat unit, divergence with respect to Cerastoderma edule, and PCR-RFLPs for the identification of both cockles. Genome 48:427–442

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara M, Inafuku J, Takeda A, Watanabe A, Fujiwara A, Kohno S, Kubota S (2009) Molecular organization of 5S rDNA in bitterlings (Cyprinidae). Genetica 135:355–365

    Article  PubMed  CAS  Google Scholar 

  • Giegerich R, Meyer F, Schleiermacher C (1996) GeneFisher: software support for the detection of postulated genes. Proc Int Conf Intell Syst Mol Biol 4:68–77

    PubMed  CAS  Google Scholar 

  • Gornung E, Colangelo P, Annesi F (2007) 5S ribosomal RNA genes in six species of Mediterranean grey mullets: genomic organization and phylogenetic inference. Genome 50:787–795

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Insua A, Freire R, Ríos J, Méndez J (2001) The 5S rDNA of mussels Mytilus galloprovincialis and M. edulis: sequence variation and chromosomal location. Chromosome Res 9:495–505

    Article  PubMed  CAS  Google Scholar 

  • Keller I, Chintauan-Marquier IC, Veltsos P, Nichols RA (2006) Ribosomal DNA in the grasshopper Podisma pedestris: escape from concerted evolution. Genetics 174:863–874

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) Mega3: integrated software for molecular evolutionary genetic analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Leo NP, Barker SC (2002) Intragenomic variation in ITS2 rDNA in the louse of humans, Pediculus humanus: ITS2 is not a suitable marker for population studies in this species. Insect Mol Biol 11:651–657

    Article  PubMed  CAS  Google Scholar 

  • Li WH (1989) A statistical test of phylogenies estimated from sequence data. Mol Biol Evol 6:424–435

    PubMed  CAS  Google Scholar 

  • Li Z, Huang S, Jin W, Ning S, Song Y, Li L (2002) Determination of copy number for 5S rDNA and centromeric sequence RCS2 in rice by Fiber-FISH. Chin Sci Bull 47:214–217

    Article  Google Scholar 

  • Little RD, Braaten BC (1989) Genomic organization of human 5S rDNA and sequence of one tandem repeat. Genomics 4:376–383

    Article  PubMed  CAS  Google Scholar 

  • López-Piñón MJ, Freire R, Insua A, Méndez J (2008) Sequence characterization and phylogenetic analysis of the 5S ribosomal DNA in some scallops (Bivalvia: Pectinidae). Hereditas 145:9–19

    Article  PubMed  Google Scholar 

  • Martins C, Galetti PM (2001) Two 5S rDNA arrays in Neotropical fish species: is it a general rule for fishes? Genetica 111:439–446

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Hughes AL (1992) Balanced polymorphism and evolution by the birth-and-death process in the MHC loci. In: Tsuji K, Aizawa M, Sasazuki T (eds) 11th Histocompatibility workshop and conference. Oxford University Press, Oxford (UK), pp 27–38

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Stephens JC, Saitou N (1985) Methods for computing the standard errors of branching points in an evolutionary tree and their application to molecular data from humans and apes. Mol Biol Evol 2:66–85

    PubMed  CAS  Google Scholar 

  • Robles F, de la Herrán R, Ludwig A, Ruiz Rejón C, Ruiz Rejón M, Garrido-Ramos MA (2005) Genomic organization and evolution of the 5S ribosomal DNA in the ancient fish sturgeon. Genome 48:18–28

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP (2004) Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Mol Biol Evol 21:1704–1711

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP, Ward TJ (2005) Evolution of large ribosomal RNA multigene family in filamentous fungi: birth and death of a concerted evolution paradigm. Proc Natl Acad Sci USA 102:5084–5098

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-Del Barrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sword GA, Senior LB, Gaskin JF, Joern A (2007) Double trouble for grasshopper molecular systematics: intra-individual heterogeneity of both mitochondrial 12S-valine-16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acrididae). Syst Entomol 32:420–428

    Article  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S et al (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank K. Thomas Jensen, Anne S. Lousdal, Ana de la Torriente, Rudo von Cosel, Virginie Héros, and Barbara Buge for providing us with some of the specimens studied. We are in debt to Ángeles Cid for her invaluable help. The support of the Consellería de Educación e Ordenación Universitaria (Xunta de Galicia, Spain) is greatly appreciated.

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Correspondence to Andrés Martínez-Lage.

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Vierna, J., González-Tizón, A.M. & Martínez-Lage, A. Long-Term Evolution of 5S Ribosomal DNA Seems to Be Driven by Birth-and-Death Processes and Selection in Ensis Razor Shells (Mollusca: Bivalvia). Biochem Genet 47, 635–644 (2009). https://doi.org/10.1007/s10528-009-9255-1

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  • DOI: https://doi.org/10.1007/s10528-009-9255-1

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