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Evolutionary Dynamics of the 5S rDNA Gene Family in the Mussel Mytilus: Mixed Effects of Birth-and-Death and Concerted Evolution

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Abstract

In higher eukaryotes, the gene family encoding the 5S ribosomal RNA (5S rRNA) has been used (together with histones) to showcase the archetypal example of a gene family subject to concerted evolution. However, recent studies have revealed conspicuous features challenging the predictions of this model, including heterogeneity of repeat units, the presence of functional 5S gene variants as well as the existence of 5S rDNA divergent pseudogenes lacking traces of homogenization. In the present work, we have broadened the scope in the evolutionary study of ribosomal gene families by studying the 5S rRNA family in mussels, a model organism which stands out among other animals due to the heterogeneity it displays regarding sequence and organization. To this end, 48 previously unknown 5S rDNA units (coding and spacer regions) were sequenced in five mussel species, leading to the characterization of two new types of units (referred to here as small-β 5S rDNA and γ-5S rDNA) coexisting in the genome with α and β rDNA units. The intense genetic dynamics of this family is further supported by the first description of an association between γ-5S rDNA units and tRNA genes. Molecular evolutionary and phylogenetic analyses revealed an extensive lack of homology among spacer sequences belonging to different rDNA types, suggesting the presence of independent evolutionary pathways leading to their differentiation. Overall, our results suggest that the long-term evolution of the 5S rRNA gene family in mussels is most likely mediated by a mixed mechanism involving the generation of genetic diversity through birth-and-death, followed by a process of local homogenization resulting from concerted evolution in order to maintain the genetic identities of the different 5S units, probably after their transposition to independent chromosomal locations.

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References

  • Acker J, Ozanne C, Kachouri-Lafond R, Gaillardin C, Neuveglise C, Marck C (2008) Dicistronic tRNA-5S rRNA genes in Yarrowia lipolytica: an alternative TFIIIA-independent way for expression of 5S rRNA genes. Nucl Acids Res 36:5832–5844

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Alves-Costa FA, Wasko AP, Oliveira C, Foresti F, Martins C (2006) Genomic organization and evolution of the 5S ribosomal DNA in Tilapiini fishes. Genetica 127:243–252

    Article  CAS  PubMed  Google Scholar 

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer Associates, Sunderland, MA, pp 38–61

    Google Scholar 

  • Barsotti G, Meluzzi C (1968) Osservazioni su Mytilus edulis L. e Mytilus galloprovincialis Lamarck. Conchiglie 4:50–58

    Google Scholar 

  • Baum BR, Edwards T, Johnson DA (2009) Phylogenetic relationships among diploid Aegilops species inferred from 5S rDNA units. Mol Phylogenet Evol 53:34–44

    Article  CAS  PubMed  Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkalyne procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Article  CAS  PubMed  Google Scholar 

  • Chichvarkhin AY, Kartavtsev YF, Kafanov AI (2000) Genetic relationships among some species of mytilidae (mollusca: Bivalvia) from the northern pacific ocean. Genetika 36:1206–1220

    PubMed  Google Scholar 

  • Cronn RC, Zhao X, Patterson AH, Wendel JF (1996) Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons. J Mol Evol 42:685–705

    Article  CAS  PubMed  Google Scholar 

  • Cross I, Rebordinos L (2005) 5S rDNA and U2 snRNA are linked in the genome of Crassostrea angulata and Crassostrea gigas oysters: does the (CT)n(GA)n microsatellite stabilize this novel linkage of large tandem arrays? Genome 48:1116–1119

    Article  CAS  PubMed  Google Scholar 

  • Dover G (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117

    Article  CAS  PubMed  Google Scholar 

  • Drouin G, Moniz de Sá MM (1995) The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Mol Biol Evol 12:481–493

    CAS  PubMed  Google Scholar 

  • Eirín-López JM, Ruiz MF, González-Tizón AM, Martínez A, Sánchez L, Méndez J (2004) 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. J Mol Evol 58:131–144

    Article  PubMed  Google Scholar 

  • Eirín-López JM, González-Romero R, Dryhurst D, Méndez J, Ausió J (2009) Long-term evolution of histone families: old notions and new insights into their diversification mechanisms across eukaryotes. In: Pontarotti P (ed) Evolutionary biology: concept, modeling, and application. Springer-Verlag, Berlin Heidelberg, pp 139–162

    Google Scholar 

  • Fang BL, De Baere R, Vandenberghe A, De Watcher R (1982) Sequences of three molluscan 5S ribosomal RNAs confirm the validity of a dynamic secondary structure model. Nucl Acids Res 10:4679–4685

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fernandez-Tajes J, Mendez J (2009) Two different size classes of 5S rDNA units coexisting in the same tandem array in the razor clam Ensis macha: is this region suitable for phylogeographic studies? Biochem Genet 47:775–788

    Article  CAS  Google Scholar 

  • Frederiksen S, Cao H, Levan G, Hallenberg C (1997) The rat 5S rRNA bona fide gene repeat maps to chromosome19q12-qter and the pseudogene repeat maps to 12q12. Cytogenet Cell Genet 76:101–106

    Article  CAS  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Gerbi SA (1985) Evolution of ribosomal RNA. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 419–517

    Google Scholar 

  • Gosling EM (1992) Genetics of Mytilus. In: Gosling EM (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp 309–382

    Google Scholar 

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

    CAS  Google Scholar 

  • Hasegawa M, Kishino K, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Ide S, Miyazaki T, Maki H, Kobayashi T (2010) Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327:693–696

    Article  CAS  PubMed  Google Scholar 

  • Insua A, Freire R, Méndez J (1999) The 5S rDNA of the bivalve Cerastoderma edule: nucleotide sequence of the repeat unit and chromosomal location relative to 18S–28S rDNA. Genet Sel Evol 31:509–518

    Article  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  CAS  PubMed  Google Scholar 

  • Kellogg EA, Appels R (1995) Intraspecific and interspecific variation in 5S RNA genes are decoupled in diploid wheat relatives. Genetics 140:325–343

    CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Komiya H, Hasegawa M, Takemura S (1986) Differentiation of oocyte- and somatic-type 5S rRNAs in animals. J Biochem (Tokyo) 100:369–374

    CAS  Google Scholar 

  • Lazar E, Haendler B, Jacob M (1983) Two 5S genes are expressed in chicken somatic cells. Nucleic Acids Res 11:7735–7741

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Long EO, Dawid IB (1980) Repeated genes in eukaryotes. Annu Rev Biochem 49:727–764

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Piñon MJ, Freire R, Insua A, Mendez 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 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25:955–964

    Article  CAS  PubMed  Google Scholar 

  • Manchado M, Zuasti E, Cross I, Merlo A, Infante C, Rebordinos L (2006) Molecular characterization and chromosomal mapping of the 5S rRNA gene in Solea senegalensis: a new linkage to the U1, U2, and U5 small nuclear RNA genes. Genome 49:79–86

    Article  CAS  PubMed  Google Scholar 

  • Marck C, Kachouri-Lafond R, Lafontaine I, Westhof E, Dujon B, Grosjean H (2006) The RNA polymerase III-dependent family of genes in hemiascomycetes: comparative RNomics, decoding strategies, transcription and evolutionary implications. Nucl Acids Res 34:1816–1835

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Lage A, Rodriguez-Farina F, Gonzalez-Tizon A, Mendez J (2005) Origin and evolution of Mytilus mussel satellite DNAs. Genome 48:247–256

    CAS  PubMed  Google Scholar 

  • Martins C, Wasko AP, Oliveira C, Porto-Foresti F, Parise-Maltempi PP, Wright JM, Foresti F (2002) Dynamics of 5S rDNA in the tilapia (Oreochromis niloticus) genome: repeat units, inverted sequences, pseudogenes and chromosome loci. Cytogenet Genome Res 98:78–85

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Rooney AP (2006) Concerted and birth-and-death evolution in multigene families. Annu Rev Genet 39:121–152

    Article  Google Scholar 

  • Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) Gene Doc: Analysis and visualization of genetic variation. EMBNEW NEWS 4:14

    Google Scholar 

  • Nielsen JN, Hallenberg C, Frederiksen S, Sorensen PD, Lomolt B (1993) Transcription of human 5S rRNA genes is influenced by an upstream DNA sequence. Nucl Acids Res 21:3631–3636

    Article  CAS  PubMed  Google Scholar 

  • Paule MR, White RJ (2000) Transcription by RNA polymerases I and III. Nucl Acids Res 28:1283–1298

    Article  CAS  PubMed  Google Scholar 

  • Pieler T, J. H, Roeder RG (1987) The 5S gene internal control region is composed of three distinct sequence elements, organized as two functional domains with variable spacing. Cell 48:91–100

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Rooney AP (2003) Selection for highly biased amino acid frequency in the TolA cell envelope protein of proteobacteria. J Mol Evol 57:731–736

    Article  CAS  PubMed  Google Scholar 

  • Rooney AP, Ward TJ (2005) Evolution of a large ribosomal RNA multigene family in filamentous fungi: birth and death of a concerted evolution paradigm. Proc Natl Acad Sci USA 102:5084–5089

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Samson M-L, Wegnez M (1988) Bipartite structure of the 5S ribosomal gene family in a Drosophila melanogaster strain, and its evolutionary implications. Genetics 118:685–691

    CAS  PubMed  Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Department of Mathematics, Washington University, St. Louis, MO

    Google Scholar 

  • Sharp S, Garcia A (1988) Transcription of the Drosophila melanogaster 5S RNA gene requires an upstream promoter and four intragenic sequence elements. Mol Cell Biol 8:1266–1274

    CAS  PubMed  Google Scholar 

  • Sharp S, Garcia A, Cooley L, Saavedra C, Soll D (1984) Transcriptionally active and inactive gene repeats within the D. melanogaster 5S RNA gene cluster. Nucl Acids Res 12:7617–7632

    Article  CAS  PubMed  Google Scholar 

  • Sitnikova T (1996) Bootstrap method of interior-branch test for phylogenetic trees. Mol Biol Evol 13:605–611

    CAS  PubMed  Google Scholar 

  • Sitnikova T, Rzhetsky A, Nei M (1995) Interior-branch and bootstrap tests of phylogenetic trees. Mol Biol Evol 12:319–333

    CAS  PubMed  Google Scholar 

  • Szostak JW, Wu R (1980) Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature 284:426–430

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Vierna J, Gonzalez-Tizon A, Martinez-Lage A (2009) 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

    Article  CAS  PubMed  Google Scholar 

  • Winnepenninckx B, Backeljau T, De Watcher R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407

    Article  CAS  PubMed  Google Scholar 

  • Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant within the Ramon y Cajal Subprogramme (MICINN, Spanish Government) awarded to JME-L. RF was supported by an Isabel Barreto contract from the Xunta de Galicia (SPAIN).

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Correspondence to José M. Eirín-López.

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Freire, R., Arias, A., Ínsua, A.M. et al. Evolutionary Dynamics of the 5S rDNA Gene Family in the Mussel Mytilus: Mixed Effects of Birth-and-Death and Concerted Evolution. J Mol Evol 70, 413–426 (2010). https://doi.org/10.1007/s00239-010-9341-3

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