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Molecular Organization and Evolution of 5S rDNA in the Genus Merluccius and Their Phylogenetic Implications

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Abstract

The molecular organization of the 5S rRNA gene family has been studied in a wide variety of animal taxa, including many bony fish species. It is arranged in tandemly repeated units consisting of a highly conserved 120 base pair–long region, which encodes for the 5S rRNA, and a nontranscribed spacer (NTS) of variable length, which contains regulatory elements for the transcription of the coding sequence. In this work, a comparative analysis of 5S ribosomal DNA (rDNA) organization and evolution in the 12 species of the genus Merluccius, which are distributed in the Atlantic and Pacific oceans, was carried out. Two main types of 5S rDNA (types A and M) were identified, as differentiated by the absence or presence of a simple sequence repeat within the NTS. Four species exhibited the 2 types of 5S rDNA, whereas the rest showed only 1 type. In addition, the species M. albidus and M. bilinearis showed 2 variants (S and L) of type-M 5S rDNA, which differentiated by length. The results obtained here support the hypothesis of a 5S rRNA dual system as an ancient condition of the Piscine genome. In contrast, some inconsistencies were found between the phylogeny of the genus Merluccius based on mitochondrial genes and that obtained from nuclear markers (5S rDNA, microsatellite loci, and allozyme data). Hybrid origin of the American species M. australis is suggested based on these results.

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References

  • Amici A, Rollo F (1991) The nucleotide sequence of the 5s ribosomal RNA gene of Pyrenophora graminea. Nucleic Acids Res 19:5073

    Article  PubMed  CAS  Google Scholar 

  • Baack EJ, Rieseberg LH (2007) A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17:513–518

    Article  PubMed  CAS  Google Scholar 

  • Bogenhagen DF, Brown DD (1981) Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell 14:261–270

    Article  Google Scholar 

  • Bogenhagen DF, Sakonju S, Brown DD (1980) A control region in the center of the 5S RNA gene directs specific initiation of transcription. II. The 3′border of the region. Cell 19:27–35

    Article  PubMed  CAS  Google Scholar 

  • Brown DD, Carroll F, Brown RD (1977) The isolation and characterization of a second oocyte 5S DNA from Xenopus laevis. Cell 12:1045–1056

    Article  PubMed  CAS  Google Scholar 

  • Campo D, Machado-Schiaffino G, Perez J, García-Vázquez E (2007) Phylogeny of the genus Merluccius based on mitochondrial and nuclear genes. Gene 406:171–179

    PubMed  CAS  Google Scholar 

  • Cassidy JR, Pukkila PJ (1987) Inversion of 5S ribosomal RNA genes within the genus Coprinus. Curr Genet 12:33–36

    Article  PubMed  CAS  Google Scholar 

  • Castillo AGF, Martinez JL, Garcia-Vazquez E (2004) Fine spatial structure of Atlantic hake (Merluccius merluccius) stocks revealed by variation at microsatellite loci. Mar Biotechnol 6:299–306

    Article  PubMed  CAS  Google Scholar 

  • Cihlar RL, Sypherd PS (1980) The organization of the ribosomal RNA genes in the fugus Mucor racemosus. Nucleic Acids Res 8:793–804

    PubMed  CAS  Google Scholar 

  • Cimmaruta R, Bondanelli P, Nascetti G (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Mol Ecol 14:2577–2591

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Duchesne LC, Anderson JB (1990) Location and direction of the 5S rRNA gene in Armillaria. Mycol Res 94:266–269

    Article  Google Scholar 

  • Egger B, Koblmüller S, Sturmbauer C, Sefc KM (2007) Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus. BMC Evol Biol 7:137

    Article  PubMed  Google Scholar 

  • Estoup A, Largiadèr CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic marker and transgenes. Mol Mar Biol Biotechnol 5:295–298

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Felsenstein J (1989) PHYLIP-Phylogenty Inference Package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Ganal MW, Lapitan NLV, Tanksley SD (1988) A molecular and cytogenetic survey of repeated DNA sequences in tomato (Lycopersicon esculentum). Mol Gen Genet 213:262–268

    Article  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 

  • Grant WS, Leslie RW (2001) Inter-ocean dispersal is an important mechanism in the zoogeography of hakes (Pisces: Merluccius spp.). J Biogeogr 28:699–721

    Article  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 

  • 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  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist FR (2001) Mrbayes: Bayesian inference of phylogeny. Bioinformatics 17:754

    Article  PubMed  CAS  Google Scholar 

  • Koblmüller S, Duftner N, Sefc KM, Aibara M, Stipacek M, Blanc M, Egger B, Sturmbauer C (2007) Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika—the result of repeated introgressive hybridization. BMC Evol Biol 7:7

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kramer R, Philippsen P, Davis RW (1978) Divergent transcription in the yeast ribosomal RNA coding region as shown by hybridization to separated strands and sequence analysis of cloned DNA. J Mol Biol 123:405–416

    Article  PubMed  CAS  Google Scholar 

  • Leaché AD, McGuire JA (2006) Phylogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: evidence for a misleading mitochodnrial gene tree. Mol Phylogenet Evol 39:628–644

    Article  PubMed  Google Scholar 

  • Lundy CJ, Moran P, Rico C, Milner RS, Hewitt GM (1999) Macrogeographical population differentiation in oceanic environments: a case study of European hake (Merluccius merluccius), a commercially important fish. Mol Ecol 8:1889–1898

    Article  PubMed  CAS  Google Scholar 

  • Machado-Schiaffino G, Garcia-Vazquez E (2009) Isolation and characterization of microsatellite loci in Merluccius australis and cross-species amplification. Mol Ecol Res 9:585–587

    Google Scholar 

  • Martins C, Galetti M Jr (2001) Organization of 5S rDNA in species of the fish Leporinus: Two different genomic locations are characterized by distinct nontranscribed spacers. Genome 44:903–910

    Article  PubMed  CAS  Google Scholar 

  • Morán P, Martínez JL, García-Vázquez E, Pendás AM (1996) Sex linkage of 5S rDNA in rainbow trout (Oncorhynchus mykiss). Cytogenet Cell Genet 75:145–150

    Article  PubMed  Google Scholar 

  • Morán P, Lundy CJ, Rico C, Hewitt GM (1999) Isolation and characterization of microsatellite loci in European hake, Merluccius merluccius (Merluccidae, Teleostei). Mol Ecol 8:1357–1358

    Article  PubMed  Google Scholar 

  • Müller K (2005) SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics 4:65–69

    Article  PubMed  Google Scholar 

  • Nedi MS, Rajagopal J, Chauhan N, Cronn R, Lakshmikumaran M (2002) Length and sequence heterogeneity in 5S rDNA of Populus deltoides. Genome 45:1181–1188

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

  • Pasolini P, Costagliola D, Rocco L, Tinti F (2006) Molecular organization of 5S rDNA in Rajidae (Chondrichthyes): structural features and evolution of Piscine 5S rRNA genes and nontranscribed intergenic spacers. J Mol Evol 62:564–574

    Article  PubMed  CAS  Google Scholar 

  • Pendás AM, Morán P, Freije JP, García-Vázquez E (1994) Chromosomal mapping and nucleotide sequence of two tandem repeats of Atlantic salmon 5S rDNA. Cytogenet Cell Genet 67:31–36

    Article  PubMed  Google Scholar 

  • Pérez J, García-Vázquez E (2004) Genetic identification of nine hake species for detection of commercial fraud. J Food Prot 67:2792–2796

    PubMed  Google Scholar 

  • Pérez M, Vieites JM, Presa P (2005) ITS1-rDNA-based methodology to identify world-wide hake species of the genus Merluccius. J Agric Food Chem 53:5239–5247

    Article  PubMed  Google Scholar 

  • Pitcher TJ, Alheit J (1995) What makes a hake? A review of the critical biological features that sustain global hake fisheries. In: Alheit J, Pitcher TJ (eds) Hake: biology, fisheries and markets. Chapman & Hall, London

    Google Scholar 

  • Quinteiro J, Vidal R, Rey-Méndez M (2000) Phylogeny and biogeographic history of hake (genus Merluccius) inferred from mirochondrial DNA control region sequences. Mar Biol 136:163–174

    Article  CAS  Google Scholar 

  • Rambaut A (2008) FigTree v1.1.2. Available at: http://tree.bio.ed.ac.uk/software/figtree

  • Rico C, Ibrahim KM, Rico I, Hewitt GM (1997) Stock composition in North Atlantic populations of whiting using microsatellite markers. J Fish Biol 51:462–475

    Article  CAS  Google Scholar 

  • Robles F, de la Herrán R, Ludwig A, Rejón CR, Rejón MR, 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 

  • Roldán MI, García-Marín JL, Utter FM, Pla C (1999) Genetic relationships among Merluccius species. Heredity 83:79–86

    Article  PubMed  Google Scholar 

  • Sajdak SL, Reed KM, Phillips RB (1998) Intraindividual and interspecies variation in the 5S rDNA of coregonid fish. J Mol Evol 46:680–688

    Article  PubMed  CAS  Google Scholar 

  • Simmons MP, Ochoterna H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  PubMed  CAS  Google Scholar 

  • Sola L, Rossi AR, Annesi F, Gornung E (2003) Cytogenetic studies in Sparus aurata (Pisces, Perciformes): molecular organization of 5S rDNA and chromosomal mapping of 5S and 45S ribosomal genes and of telomeric repeats. Hereditas 139:232–236

    Article  PubMed  CAS  Google Scholar 

  • Stepien C, Rosenblatt RH (1996) Genetic divergence in antitropical pelagic marine fishes (Trachurus, Merluccius and Scomber) between North and South America. Copeia 3:586–589

    Article  Google Scholar 

  • Swofford DL (2003) PAUP*: phylogenetics analysis using Parsimony (and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tabata S (1980) Structure of the 5S ribosomal RNA gene and its adjacent regions in Torulopsis utilis. Eur J Biochem 110:107–114

    Article  PubMed  CAS  Google Scholar 

  • Teletchea F, Laudet V, Hänni C (2006) Phylogeny of the Gadidae (sensu Svetovidov 1948) based on their morphology and two mitochondrial genes. Mol Phylogenet Evol 38:189–199

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Ting N, Tosi AJ, Li Y, Zhang Y, Disotell TR (2008) Phylogenetic incongruence between nuclear and mitochondrial markers in the Asian colobines and the evolution of the langurs and leaf monkeys. Mol Phylogenet Evol 46:466–474

    Article  PubMed  CAS  Google Scholar 

  • von der Heyden S, Lipinski MR, Matthee CA (2007) Mitochondrial DNA analyses of the Cape hakes reveal an expanding, panmictic population for Merluccius capensis and population structuring for mature fish in Merluccius paradoxus. Mol Phylogenet Evol 42:517–527

    Article  Google Scholar 

  • Wasko AP, Martins C, Wright JM, Galetti PM Jr (2001) Molecular organization of 5S rDNA in fishes of the genus Brycon. Genome 44:893–902

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Hake samples were kindly provided by Francis Juanes (University of Massachusetts), Ignacio Sobrino (Instituto Español de Oceanografia Cadiz, Spain), Luis O. Bala (Consejo Nacional de Investigaciones Cientificas y Tecnicas, Argentina), Mauricio Ponte (University of Santiago, Chile), Francisco Sanchez (Instituto Español de Oceanografia Santander, Spain), Robin Tilney (Department of Environmental Affairs, Cape Town, South Africa), and Eduardo Vallarino (University of Mar del Plata, Argentina).

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Correspondence to Daniel Campo.

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Campo, D., Machado-Schiaffino, G., Horreo, J.L. et al. Molecular Organization and Evolution of 5S rDNA in the Genus Merluccius and Their Phylogenetic Implications. J Mol Evol 68, 208–216 (2009). https://doi.org/10.1007/s00239-009-9207-8

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  • DOI: https://doi.org/10.1007/s00239-009-9207-8

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