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Evidence of birth-and-death evolution of 5S rRNA gene in Channa species (Teleostei, Perciformes)

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Abstract

In higher eukaryotes, minor rDNA family codes for 5S rRNA that is arranged in tandem arrays and comprises of a highly conserved 120 bp long coding sequence with a variable non-transcribed spacer (NTS). Initially the 5S rDNA repeats are considered to be evolved by the process of concerted evolution. But some recent reports, including teleost fishes suggested that evolution of 5S rDNA repeat does not fit into the concerted evolution model and evolution of 5S rDNA family may be explained by a birth-and-death evolution model. In order to study the mode of evolution of 5S rDNA repeats in Perciformes fish species, nucleotide sequence and molecular organization of five species of genus Channa were analyzed in the present study. Molecular analyses revealed several variants of 5S rDNA repeats (four types of NTS) and networks created by a neighbor net algorithm for each type of sequences (I, II, III and IV) did not show a clear clustering in species specific manner. The stable secondary structure is predicted and upstream and downstream conserved regulatory elements were characterized. Sequence analyses also shown the presence of two putative pseudogenes in Channa marulius. Present study supported that 5S rDNA repeats in genus Channa were evolved under the process of birth-and-death.

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References

  • Adamson EAS, Hurwood DA, Mather PB (2010) A reappraisal of the evolution of Asian snakehead fishes (Pisces, Channidae) using molecular data from multiple genes and fossil calibration. Mol Phylo Evol 56:707–717

    Article  Google Scholar 

  • Bryant D, Moulton V (2002) NeighborNet: an agglomerative method for the construction of planar phylogenetic networks. In Guigo R, Guseld D (ed) Algorithms in bioinformatics, LNCS 2452:375-391

  • Campo D, Machado-Schiaffino G, Horreo JL, Garcia-Vazquez E (2009) Molecular organization and evolution of 5S rDNA in the genus Merluccius and their phylogenetic implications. J Mol Evol 68:208–216

    Article  CAS  PubMed  Google Scholar 

  • Cioffi MdB, Bertollo LAC, Villa MA, de Oliveira EA, Tanomtong A, Yano CF, Supiwong W, Chaveerach A (2015) Genomic organization of repetitive DNA elements and its implications for the chromosomal evolution of channid fishes (Actinopterygii, Perciformes). PLoS ONE 10:e0130199

    Article  CAS  PubMed Central  Google Scholar 

  • Delihas N, Andersen J (1982) Generalized structures of the 5S ribosomal RNAs. Nucleic Acids Res 10:7323–7344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eirin-Lopez JM, Rebordinos L, Rooney AP, Rozas J (2012) The birth-and-death evolution of multigene families revisited. In: Garrido-Ramos MA (ed) Repetitive DNA, genome dynamics. Karger Medical and Scinetific Publisher, Basel, pp 170–196

    Chapter  Google Scholar 

  • Ferreira IA, Oliveira C, Venere PC, Galetti PM Jr, Martins C (2007) 5S rDNA variation and its phylogenetic inference in the genus Leporinus (Characiformes: Anostomidae). Genetica 129:253–257

    Article  CAS  PubMed  Google Scholar 

  • Fitch W (1997) Networks and viral evolution. J Mol Evol 44:S65–S75

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 

  • Hallenberg C, Nederby-Nielson J, Frederiksen S (1994) Characterization of 5S rRNA genes from mouse. Gene 142:291–295

    Article  CAS  PubMed  Google Scholar 

  • Hamada M, Huang Y, Lowe TM, Maraia RJ (2001) Widespread use of TATA elements in the core promoters for RNA polymerase III, II and I in fission yeast. Mol Cell Biol 21:6870–6881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • Inafuku J, Nabeyama M, Kikuma Y, Saitoh J, Kubota S, Kohno S (2000) Chromosomal location and nucleotide sequences of 5S ribosomal DNA of two cyprinid species (Osteichthyes, Pisces). Chromosome Res 8:193–199

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Singh M, Kushwaha B, Nagpure NS, Mani I, Lakra WS (2013) Molecular characterization of major and minor rDNA repeats and genetic variability assessment in different species of mahseer found in North India. Gene 527:248–258

    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 

  • Martins C, Wasko AP (2004) Organization and evolution of 5S ribosomal DNA in the fish genome. In: Williams CL (ed) Focus on genome research. Nova Science Publishers, Hauppauge, pp 335–363

    Google Scholar 

  • Martins C, Wasko AP, Oliveira C, Wright JM (2000) Nucleotide sequence of 5S rDNA and localization of the ribosomal RNA genes to metaphase chromosomes of the tilapiine cichlid fish, Oreochromis niloticus. Hereditas 133:39–46

    Article  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 

  • Merlo MA, Pacchiarini T, Portela-Bens S, Cross I, Manchado M, Rebordinos L (2012a) Genetic characterization of Plectorhinchus mediterraneus yields important clues about genome organization and evolution of multigene families. BMC Genet 13:33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merlo MA, Cross I, Palazon JL, Ubeda-Manzanaro M, Sarasquete C, Rebordinos L (2012b) Evidence for 5S rDNA horizontal transfer in the toadfish Halobatrachus didactylus (Schneider, 1801) based on the analysis of three multigene families. BMC Evol Biol 12:210

    Article  CAS  Google Scholar 

  • Moran P, Martinez JL, Garcia-Vazquez S, Pendas AM (1996) Sex linkage of 5S rDNA in rainbow trout (Oncorhynchus mykiss). Cytogenet Cell Genet 75:145–150

    Article  CAS  PubMed  Google Scholar 

  • Murakami M, Fujitani H (1998) Characterization of repetitive DNA sequences carrying 5S rDNA of the triploid ginbuna (Japanese silver crucian carp, Carassius auratus langsdorfi). Genes Genet Syst 73:9–20

    Article  CAS  PubMed  Google Scholar 

  • Nakajima RT, Cabral-de-Mello D, Valente GT, Venere PC, Martins C (2012) Evolutionary dynamics of rRNA gene clusters in cichlid fish. BMC Evol Biol 12:198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. PNAS 94:7799–7806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pendas AM, Moran P, Freije JP, Garcia-Vasquez E (1994) Chromosomal location and nucleotide sequence of two tandem repeats of the Atlantic salmon 5S rDNA. Cytogenet Cell Genet 67:31–36

    Article  CAS  PubMed  Google Scholar 

  • Perina A, Seoane D, Gonzalez-Tizon AM, Rodriguez-Farina F, Martinez-Lage A (2011) Molecular organization and phylogenetic analysis of 5S rDNA in crustaceans of the genus Pollicipes reveal birth-and-death evolution and strong purifying selection. BMC Evol Biol 11:304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieler T, Hamm J, 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

    Article  CAS  PubMed  Google Scholar 

  • Pinhal D, Araki CS, Gadig OB (2009) Molecular organization of 5S rDNA in sharks of the genus Rhizoprionodon: insights into the evolutionary dynamics of 5S rDNA in vertebrate genomes. Genet Res 91:61–72

    Article  CAS  Google Scholar 

  • Pinhal D, Yoshimura TS, Araki C, Martins C (2011) The 5S rDNA family evolves through concerted and birth-and-death evolution in fish genomes: an example from freshwater stingrays. BMC Evol Biol 11:151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raha D, Wang Z, Moqtaderi Z, Wu L, Zhong G, Gerstein M et al (2010) Close association of RNA polymerase II and many transcription factors with Pol III genes. PNAS 107:3639–3644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebordinos L, Cross I, Merlo A (2013) High evolutionary dynamism in 5S rDNA of fish: state of the art. Cytogenet Genome Res 141(2–3):103–113

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues DS, Rivera M, Lourenco LB (2012) Molecular organization and chromosomal localization of 5S rDNA in Amazonian Engystomops (Anura, Leiuperidae). BMC Genet 13:17

    Article  CAS  PubMed  PubMed Central  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  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. PNAS 102:5084–5089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rooney AP, Piontkivska H, Nei M (2002) Molecular evolution of the non tandemly repeated genes of the Histone 3 multigene family. Mol Biol Evol 9:68–75

    Article  Google Scholar 

  • Sambrook J, Russell I (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Plainsveiw

    Google Scholar 

  • Singh M, Kumar R, Nagpure NS, Kushwaha B, Mani I, Chauhan UK, Lakra WS (2009a) Population distribution of 45S and 5S rDNA in golden Mahseer, Tor putitora: population specific FISH marker. J Genet 88:315–320

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Kumar R, Nagpure NS, Kushwaha B, Gond I, Lakra WS (2009b) Chromosomal localization of 18S and 5S rDNA using FISH in genus Tor (Pisces, Cyprinidae). Genetica 137:245–252

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Kumar R, Nagpure NS, Kushwaha B, Mani I, Murmu K, Chauhan UK, Lakra WS (2010) Nucleotide Sequences and Chromosomal Localization of 45S and 5SrDNA in N. hexagonolepis (Pisces, Cyprinidae), using dual colour FISH. Zool Sci 27:709–716

    Article  CAS  PubMed  Google Scholar 

  • Tavare S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM (ed) Some mathematical questions in biology-DNA sequence analysis. American Mathematical Society, Providence, pp 57–86

    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  PubMed Central  Google Scholar 

  • Ubeda-Manzanaro M, Merlo MA, Palazon JL, Sarasquete C, Rebordinos L (2010) Sequence characterization and phylogenetic analysis of the ribosomal DNA in species of the family Batrachoididae. Genome 53:723–730

    Article  CAS  PubMed  Google Scholar 

  • Veldhoen N, You Q, Setzer DR, Romaniuk PJ (1994) Contribution of individual base pair to the interaction of TFIIIA with the Xenopus 5S rRNA gene. Biochemistry 33:7568–7575

    Article  CAS  PubMed  Google Scholar 

  • Vierna J, Gonzalez-Tizon AM, 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: Bivavia). Biochem Genet 47:635–644

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Authors are thankful to Vice Chancellor of Central Agricultural University, Imphal for infrastructure support. Kind helps of Dr. S. Khogen Singh and Tapas Sarkar for collection of fish samples are duly acknowledged. The authors are thankful to the Department of Biotechnology (DBT), the Ministry of Science and Technology, Government of India for research grants.

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    Authors and Affiliations

    1. College of Fisheries, Central Agricultural University, Lembucherra, Tripura (West), 799210, India

      Anindya Sundar Barman & Mamta Singh

    2. National Bureau of Fish Genetic Resources (ICAR), Canal Ring Road, P.O. Dilkusha, Lucknow, 226002, India

      Rajeev Kumar Singh & Kuldeep Kumar Lal

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    1. Anindya Sundar Barman
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    Correspondence to Anindya Sundar Barman.

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    Anindya Sundar Barman and Mamta Singh have contributed equally to this work.

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    Barman, A.S., Singh, M., Singh, R.K. et al. Evidence of birth-and-death evolution of 5S rRNA gene in Channa species (Teleostei, Perciformes). Genetica 144, 723–732 (2016). https://doi.org/10.1007/s10709-016-9938-6

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