Skip to main content
SpringerLink
Log in

Characterization of species-specifically amplified SINEs in three salmonid species—Chum salmon, pink salmon, and kokanee: The local environment of the genome may be important for the generation of a dominant source gene at a newly retroposed locus

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Short interspersed repetitive elements (SINEs), known as theHpaI family, are present in the genomes of all salmonid species (Kido et al.,Proc. Natl. Acad. Sci. USA 1991, 88: 2326–2330). Recently, we showed that the retropositional efficiency of the SINE family in the lineage of chum salmon is extraordinarily high in comparison with that in other salmonid lineages (Takasaki et al.,Proc. Natl. Acad. Sci. USA 1994, 91: 10153–10157). To investigate the reason for this high efficiency, we searched for members of theHpaI SINE family that have been amplified species-specifically in pink salmon. Since the efficiency of the species-specific amplification in pink salmon is not high and since other members of the same subfamily of SINEs were also amplified species-specifically in pink salmon, the actual sequence of this subfamily might not be the cause of the high retropositional efficiency of SINEs in chum salmon. Rather, it appears that a highly dominant source gene for the subfamily may have been newly created by retroposition, and some aspect of the local environment around the site of retroposition may have been responsible for the creation of this dominant source gene in chum salmon. Furthermore, a total of 11 sequences ofHpaI SINEs that have been amplified species-specifically in three salmon lineages was compiled and characterized. Judging from the distribution of members of the same-sequence subfamily of SINEs in different lineages and from the distribution of the different-sequence subfamilies in the same lineage, we have concluded that multiple dispersed loci are responsible for the amplification of SINEs. We also discuss the additional possibility of horizontal transmission of SINEs between species. The availability of the sets of primers used for the detection of the species-specific amplifications of the SINEs provides a convenient and reliable method for identification of these salmonid species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Batzer MA, Kilroy GE, Richard PE, Shaikh TH, Desselle TD, Hoppens CL, Deininger PL (1990) Structure and variability of recently inserted Alu family members. Nucleic Acids Res 18:6793–6798

    Google Scholar 

  • Batzer MA, Deininger PL (1991) A human-specific subfamily of Alu sequences. Genomics 9:481–487

    Google Scholar 

  • Batzer MA, Gudi VA, Mena JC, Foltz DW, Herrera RJ, Deininger PL (1991) Amplification dynamics of human-specific (HS)alu family members. Nucleic Acids Res 19:3619–3623

    Google Scholar 

  • Batzer MA, Stoneking M, Alegria-Hartman M, Bazen H, Kass DH, Shaikh TH, Novick GE, Ioannou PA, Scheer WD, Herrera RJ, Deininger PL (1994) African origin of human-specific polymorphicAlu insertions. Proc Natl Acad Sci USA 91:12288–12292

    Google Scholar 

  • Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3:2303–2308

    Google Scholar 

  • Brains W, Temple-Smith K (1989) Similarity and divergence among rodent repetitive DNA sequences. J Mol Evol 28:191–199

    Google Scholar 

  • Britten RJ, Baron WF, Stout DB, Davidson EH (1988) Sources and evolution of humanAlu repeated sequences. Proc Natl Acad Sci USA 85:4770–4774

    Google Scholar 

  • Britten RJ, McCormack TJ, Mears TL, Davidson EH (1995) Gypsy/Ty3-class retrotransposons integrated in the DNA of herring, tunicate, and echinoderms. J Mol Evol 40:13–24

    Google Scholar 

  • Cao Y, Adachi J, Janke A, Pääbo S, Hasegawa M (1994) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J Mol Evol 39:519–527

    Google Scholar 

  • Deininger PL, Batzer MA, Hutchison CA III, Edgell MH (1992) Master genes in mammalian repetitive DNA amplification. Trends Genet 8:307–311

    Google Scholar 

  • Deininger PL, Batzer MA (1993) Evolution of retroposons. In: Hecht MK et al. (eds) Evolutionary biology, vol 27. Plenum Press, New York, pp 157–196

    Google Scholar 

  • Deragon J-M, Landry BS, Pélissier T, Tutois S, Tourmente S, Picard G (1994) An analysis of retroposition in plants based on a family of SINEs fromBrassica napus. J Mol Evol 39:378–386

    Google Scholar 

  • Endoh H, Nagahashi S, Okada N (1990) A highly repetitive and transcribable sequence in the tortoise genome is probably a retroposon. Eur J Biochem 189:25–31

    Google Scholar 

  • Goodier JL, Davidson WS (1994) Tc1 transposon-like sequences are widely distributed in salmonids. J Mol Biol 241:26–34

    Google Scholar 

  • Grimaldi G, Singer MF (1982) A monkeyAlu sequence is flanked by 13-base-pair direct repeats of an interrupted α-satellite DNA sequence. Proc Natl Acad Sci USA 79:1497–1500

    Google Scholar 

  • Jagadeeswaran P, Forget BG, Weissman SM (1981) Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse transcription of RNA pol III transcripts? Cell 26:141–142

    Google Scholar 

  • Jurka J, Smith T (1988) A fundamental division in theAlu family of repeated sequences. Proc Natl Acad Sci USA 85:4775–4778

    Google Scholar 

  • Jurka J, Milosavljevic A (1991) Reconstruction and analysis of human Alu genes. J Mol Evol 32:105–121

    Google Scholar 

  • Jurka J, Zeitkiewicz E, Labuda D (1995) Ubiquitous mammalian-wide interspersed repeats (MIRs) are molecular fossils from the mesozoic era. Nucleic Acids Res 23:170–175

    Google Scholar 

  • Kalb VF, Glasser S, King D, Lingrel JB (1983) A cluster of repetitive elements within a 700 base-pair region in the mouse genome. Nucleic Acids Res 11:2177–2184

    Google Scholar 

  • Kido Y, Aono M, Yamaki T, Matsumoto K, Murata S, Saneyoshi M, Okada N (1991) Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution. Proc Natl Acad Sci USA 88:2326–2330

    Google Scholar 

  • Kido Y, Himberg M, Takasaki N, Okada N (1994) Amplification of distinct subfamilies of short interspersed elements during evolution of the Salmonidae. J Mol Biol 241:633–644

    Google Scholar 

  • Kido Y, Saitoh M, Murata S, Okada N (1995) Evolution of the source sequences ofHpa I short interspersed elements. J Mol Evol (in press)

  • Kidwell MG (1993) Lateral transfer in natural populations of eukaryotes. Annu Rev Genet 27:235–256

    Google Scholar 

  • Koishi R, Okada N (1991) Distribution of the salmonid Hpa I family in the salmonid species demonstrated by in vitro runoff transcription assay of total genomic DNA: a procedure to estimate repetitive frequency and sequence divergence of a certain repetitive family with a few known sequences. J Mol Evol 32:43–52

    Google Scholar 

  • Krane DE, Clark AG, Cheng J-F, Hardison RC (1991) Subfamily relationships and clustering of rabbit C repeats. Mol Biol Evol 8:1–30

    Google Scholar 

  • Leeflang EP, Liu W-M, Hashimoto C, Choudary PV, Schmid CW (1992) Phylogenetic evidence for multiple Alu source genes. J Mol Evol 35:7–16

    Google Scholar 

  • Leeflang EP, Liu W-M, Chesnokov IN, Schmid CW (1993a) Phylogenetic isolation of a human Alu founder gene: drift to new sub-family identity. J Mol Evol 37:559–565

    Google Scholar 

  • Leeflang EP, Chesnokov IN, Schmid CW (1993b) Mobility of short interspersed repeats within the chimpanzee lineage. J Mol Evol 37:566–572

    Google Scholar 

  • Lui W-M, Schmid CW (1993) Proposed roles for DNA methylation inAlu transcriptional repression and mutational inactivation. Nucleic Acids Res 21:1351–1359

    Google Scholar 

  • Maraia, RJ (1991) The subset of mouse B1 (Alu-equivalent) sequences expressed as small processed cytoplasmic transcripts. Nucleic Acids Res 19:5695–5702

    Google Scholar 

  • Matera AG, Hellmann U, Hintz MF, Schmid CW (1990) Recently transposed Alu repeats result from multiple source genes. Nucleic Acids Res 18:6019–6023

    Google Scholar 

  • Minghetti P, Dugaiczyk A (1993) The emergence of new DNA repeats and the divergence of primates. Proc Natl Acad Sci USA 90:1872–1876

    Google Scholar 

  • Mochizuki K, Umeda M, Ohtsubo H, Ohtsubo E (1992) Characterization of a plant SINE, p-SINE1, in rice genome. Jpn J Genet 67:155–166

    Google Scholar 

  • Murata S, Takasaki N, Saitoh M, Okada N (1993) Determination of the phylogenetic relationships among Pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. Proc Natl Acad Sci USA 90:6995–6999

    Google Scholar 

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

    Google Scholar 

  • Nisson PE, Hickey RJ, Boshar MF, Crain Jr WR (1988) Identification of a repeated sequence in the genome of the sea urchin which is transcribed by RNA polymerase III and contains the features of a retroposon. Nucleic Acids Res 16:1431–1452

    Google Scholar 

  • Ohshima K, Koishi R, Matsuo M, Okada N (1993) Several short interspersed repetitive element (SINEs) in distant species may have originated from a common ancestral retrovirus: characterization of a squid SINE and a possible mechanism for generation of tRNA-derived retroposons. Proc Natl Acad Sci U.S.A. 90:6260–6264

    Google Scholar 

  • Ohshima K, Okada N (1994) Generality of the tRNA origin of short interspersed repetitive elements (SINEs); characterization of three different tRNA-derived retroposons in the octopus. J Mol Biol 243:25–37

    Google Scholar 

  • Okada N (1991a) SINEs: short interspersed repeated elements of the eukaryotic genome. Trends Ecol Evol 6:358–361

    Google Scholar 

  • Okada N (1991b) SINEs. Curr Opin Genet Dev 1:498–504

    Google Scholar 

  • Philippe H, Douzery E (1994) The pitfalls of molecular phylogeny based on four species, as illustrated by the Cetacea/Artiodactyla relationships. J Mammalian Evol 2:133–152

    Google Scholar 

  • Perna NT, Batzer MA, Deininger PL, Stoneking M (1992) Alu insertion polymorphism: a new type of marker for human population studies. Hum Biol 64:641–648

    Google Scholar 

  • Quentin Y (1988) The Alu family developed through successive waves of fixation closely connected with primate lineage history. J Mol Evol 27:194–202

    Google Scholar 

  • Quentin Y (1989) Successive waves of fixation of B1 variants in rodent lineage history. J Mol Evol 28:299–305

    Google Scholar 

  • Radice AD, Bugaj B, Fitch DHA, Emmons SW (1994) Widespread occurrence of the Tc1 transposon family: Tc1-like transposons from teleost fish. Mol Gen Genet 244:606–612

    Google Scholar 

  • Rogers JH (1985) The origin and evolution of retroposons. Int Rev Cytol 93:187–279

    Google Scholar 

  • Sakagami M, Ohshima K, Mukoyama H, Yasue H, Okada N (1994) A novel tRNA species as an origin of short interspersed repetitive elements (SINEs); equine SINEs may have originated from tRNAser. J Mol Biol 239:731–735

    Google Scholar 

  • Shen MR, Batzer MA, Deininger PL (1991) Evolution of the master Alu gene(s). J Mol Evol 33:311–320

    Google Scholar 

  • Schmid CW (1991) Human Alu subfamilies and their methylation revealed by blot hybridization. Nucleic Acids Res 19:5613–5617

    Google Scholar 

  • Schmid C, Maraia R (1992) Transcriptional regulation and transpositional selection of active SINE sequences. Curr Opin Genet Dev 2:874–882

    Google Scholar 

  • Singer MF (1982) SINEs and LINEs: highly repeated short and long interspersed sequences in mammalian genomes. Cell 28:433–434

    Google Scholar 

  • Sinnett D, Richer C, Deragon J-M, Labuda D (1992) Alu RNA transcripts in human embryonal carcinoma cells: model of post-transcriptional selection of master sequences. J Mol Biol 226:689–706

    Google Scholar 

  • Slagel V, Flemington E, Traina-Dorge V, Bradshaw H, Deininger P (1987) Clustering and subfamily relationships of the Alu family in the human genome. Mol Biol Evol 4:19–29

    Google Scholar 

  • Smith GR, Stearly RF (1989) The classification and scientific names of rainbow and cutthroat trouts. Fisheries 14:4–10

    Google Scholar 

  • Smit AFA, Riggs AD (1995) MIRs are classic, tRNA-derived SINEs that amplified before the mammalian radiation. Nucleic Acids Res 23:98–102

    Google Scholar 

  • Spotila LD, Hirai H, Rekosh DM, LoVerde PT (1989) A retroposon-like short repetitive DNA element in the genome of the human blood fluke,Schistosoma mansoni. Chromosoma 97:421–428

    Google Scholar 

  • Takasaki N, Murata S, Saitoh M, Kobayashi T, Park L, Okada N (1994) Species-specific amplification of tRNA-derived short interspersed repetitive elements (SINEs) by retroposition: a process of parasitization of entire genomes during the evolution of salmonids. Proc Natl Acad Sci USA 91:10153–10157

    Google Scholar 

  • Trabuchet G, Chebloune Y, Savatier P, Lachuer J, Faure C, Verdier G, Nigon VM (1987) Recent insertion of an Alu sequence in the beta-globin gene cluster of the gorilla. J Mol Evol 25:288–291

    Google Scholar 

  • Ullu E, Tschudi C (1984)Alu sequences are processed 7SL RNA genes. Nature 312:171–172

    Google Scholar 

  • Van Arsdell SW, Denison RA, Bernstein LB, Weiner AM (1981) Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell 26:11–17

    Google Scholar 

  • Weiner AM (1980) An abundant cytoplasmic 7S RNA is complementary to the dominant interspersed middle repetitive DNA sequence family in the human genome. Cell 22:209–218

    Google Scholar 

  • Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55:631–661

    Google Scholar 

  • Willard C, Nguyen HT, Schmid CW (1987) Existence of at least three distinct Alu subfamilies. J Mol Evol 26:180–186

    Google Scholar 

  • Yoshioka Y, Matsumoto S, Kojima S, Ohshima K, Okada N, Machida Y (1993) Molecular characterization of a short interspersed repetitive element from tobacco that exhibits sequence homology to specific tRNAs. Proc Natl Acad Sci USA 90:6562–6566

    Google Scholar 

  • Zietkiewicz E, Richer C, Makalowski W, Jurka J, Laduda D (1994) A youngAlu subfamily amplified independently in human and African great apes lineages. Nucleic Acids Res 22:5608–5612

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku, 226, Yokohama, Japan

    Nobuyoshi Takasaki & Norihiro Okada

  2. Northwest Fisheries Science Center, Coastal Zone and Estuarine Studies Division, 2725 Montlake Boulevard East, 98112-2097, Seattle, WA, USA

    Linda Park

  3. Hokkaido Salmon Hatchery, Fisheries Agency of Japan, 2-2 Nakanoshima, Toyohira-ku, 062, Sapporo, Japan

    Masahide Kaeriyama

  4. Juneau Center, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 11120 Glacier Highway, 99801, Juneau, AK, USA

    Anthony J. Gharrett

Authors
  1. Nobuyoshi Takasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Linda Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masahide Kaeriyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anthony J. Gharrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Norihiro Okada
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takasaki, N., Park, L., Kaeriyama, M. et al. Characterization of species-specifically amplified SINEs in three salmonid species—Chum salmon, pink salmon, and kokanee: The local environment of the genome may be important for the generation of a dominant source gene at a newly retroposed locus. J Mol Evol 42, 103–116 (1996). https://doi.org/10.1007/BF02198835

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02198835

Key words

Search

Navigation