Journal of Molecular Evolution

, Volume 42, Issue 2, pp 103–116 | Cite as

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

  • Nobuyoshi Takasaki
  • Linda Park
  • Masahide Kaeriyama
  • Anthony J. Gharrett
  • Norihiro Okada


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.

Key words

Salmon SINE Retroposition 


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  1. 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 18:6793–6798Google Scholar
  2. Batzer MA, Deininger PL (1991) A human-specific subfamily of Alu sequences. Genomics 9:481–487Google Scholar
  3. 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 19:3619–3623Google Scholar
  4. 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 91:12288–12292Google Scholar
  5. Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3:2303–2308Google Scholar
  6. Brains W, Temple-Smith K (1989) Similarity and divergence among rodent repetitive DNA sequences. J Mol Evol 28:191–199Google Scholar
  7. Britten RJ, Baron WF, Stout DB, Davidson EH (1988) Sources and evolution of humanAlu repeated sequences. Proc Natl Acad Sci USA 85:4770–4774Google Scholar
  8. 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 40:13–24Google Scholar
  9. 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 39:519–527Google Scholar
  10. Deininger PL, Batzer MA, Hutchison CA III, Edgell MH (1992) Master genes in mammalian repetitive DNA amplification. Trends Genet 8:307–311Google Scholar
  11. Deininger PL, Batzer MA (1993) Evolution of retroposons. In: Hecht MK et al. (eds) Evolutionary biology, vol 27. Plenum Press, New York, pp 157–196Google Scholar
  12. 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 39:378–386Google Scholar
  13. Endoh H, Nagahashi S, Okada N (1990) A highly repetitive and transcribable sequence in the tortoise genome is probably a retroposon. Eur J Biochem 189:25–31Google Scholar
  14. Goodier JL, Davidson WS (1994) Tc1 transposon-like sequences are widely distributed in salmonids. J Mol Biol 241:26–34Google Scholar
  15. 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 79:1497–1500Google Scholar
  16. 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 26:141–142Google Scholar
  17. Jurka J, Smith T (1988) A fundamental division in theAlu family of repeated sequences. Proc Natl Acad Sci USA 85:4775–4778Google Scholar
  18. Jurka J, Milosavljevic A (1991) Reconstruction and analysis of human Alu genes. J Mol Evol 32:105–121Google Scholar
  19. Jurka J, Zeitkiewicz E, Labuda D (1995) Ubiquitous mammalian-wide interspersed repeats (MIRs) are molecular fossils from the mesozoic era. Nucleic Acids Res 23:170–175Google Scholar
  20. 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 11:2177–2184Google Scholar
  21. 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 88:2326–2330Google Scholar
  22. 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 241:633–644Google Scholar
  23. Kido Y, Saitoh M, Murata S, Okada N (1995) Evolution of the source sequences ofHpa I short interspersed elements. J Mol Evol (in press)Google Scholar
  24. Kidwell MG (1993) Lateral transfer in natural populations of eukaryotes. Annu Rev Genet 27:235–256Google Scholar
  25. 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 32:43–52Google Scholar
  26. Krane DE, Clark AG, Cheng J-F, Hardison RC (1991) Subfamily relationships and clustering of rabbit C repeats. Mol Biol Evol 8:1–30Google Scholar
  27. Leeflang EP, Liu W-M, Hashimoto C, Choudary PV, Schmid CW (1992) Phylogenetic evidence for multiple Alu source genes. J Mol Evol 35:7–16Google Scholar
  28. 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 37:559–565Google Scholar
  29. Leeflang EP, Chesnokov IN, Schmid CW (1993b) Mobility of short interspersed repeats within the chimpanzee lineage. J Mol Evol 37:566–572Google Scholar
  30. Lui W-M, Schmid CW (1993) Proposed roles for DNA methylation inAlu transcriptional repression and mutational inactivation. Nucleic Acids Res 21:1351–1359Google Scholar
  31. Maraia, RJ (1991) The subset of mouse B1 (Alu-equivalent) sequences expressed as small processed cytoplasmic transcripts. Nucleic Acids Res 19:5695–5702Google Scholar
  32. Matera AG, Hellmann U, Hintz MF, Schmid CW (1990) Recently transposed Alu repeats result from multiple source genes. Nucleic Acids Res 18:6019–6023Google Scholar
  33. Minghetti P, Dugaiczyk A (1993) The emergence of new DNA repeats and the divergence of primates. Proc Natl Acad Sci USA 90:1872–1876Google Scholar
  34. Mochizuki K, Umeda M, Ohtsubo H, Ohtsubo E (1992) Characterization of a plant SINE, p-SINE1, in rice genome. Jpn J Genet 67:155–166Google Scholar
  35. 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 90:6995–6999Google Scholar
  36. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  37. 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 16:1431–1452Google Scholar
  38. 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. 90:6260–6264Google Scholar
  39. 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 243:25–37Google Scholar
  40. Okada N (1991a) SINEs: short interspersed repeated elements of the eukaryotic genome. Trends Ecol Evol 6:358–361Google Scholar
  41. Okada N (1991b) SINEs. Curr Opin Genet Dev 1:498–504Google Scholar
  42. Philippe H, Douzery E (1994) The pitfalls of molecular phylogeny based on four species, as illustrated by the Cetacea/Artiodactyla relationships. J Mammalian Evol 2:133–152Google Scholar
  43. Perna NT, Batzer MA, Deininger PL, Stoneking M (1992) Alu insertion polymorphism: a new type of marker for human population studies. Hum Biol 64:641–648Google Scholar
  44. Quentin Y (1988) The Alu family developed through successive waves of fixation closely connected with primate lineage history. J Mol Evol 27:194–202Google Scholar
  45. Quentin Y (1989) Successive waves of fixation of B1 variants in rodent lineage history. J Mol Evol 28:299–305Google Scholar
  46. 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 244:606–612Google Scholar
  47. Rogers JH (1985) The origin and evolution of retroposons. Int Rev Cytol 93:187–279Google Scholar
  48. 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 239:731–735Google Scholar
  49. Shen MR, Batzer MA, Deininger PL (1991) Evolution of the master Alu gene(s). J Mol Evol 33:311–320Google Scholar
  50. Schmid CW (1991) Human Alu subfamilies and their methylation revealed by blot hybridization. Nucleic Acids Res 19:5613–5617Google Scholar
  51. Schmid C, Maraia R (1992) Transcriptional regulation and transpositional selection of active SINE sequences. Curr Opin Genet Dev 2:874–882Google Scholar
  52. Singer MF (1982) SINEs and LINEs: highly repeated short and long interspersed sequences in mammalian genomes. Cell 28:433–434Google Scholar
  53. 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 226:689–706Google Scholar
  54. 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 4:19–29Google Scholar
  55. Smith GR, Stearly RF (1989) The classification and scientific names of rainbow and cutthroat trouts. Fisheries 14:4–10Google Scholar
  56. Smit AFA, Riggs AD (1995) MIRs are classic, tRNA-derived SINEs that amplified before the mammalian radiation. Nucleic Acids Res 23:98–102Google Scholar
  57. 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 97:421–428Google Scholar
  58. 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 91:10153–10157Google Scholar
  59. 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 25:288–291Google Scholar
  60. Ullu E, Tschudi C (1984)Alu sequences are processed 7SL RNA genes. Nature 312:171–172Google Scholar
  61. Van Arsdell SW, Denison RA, Bernstein LB, Weiner AM (1981) Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell 26:11–17Google Scholar
  62. Weiner AM (1980) An abundant cytoplasmic 7S RNA is complementary to the dominant interspersed middle repetitive DNA sequence family in the human genome. Cell 22:209–218Google Scholar
  63. 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 55:631–661Google Scholar
  64. Willard C, Nguyen HT, Schmid CW (1987) Existence of at least three distinct Alu subfamilies. J Mol Evol 26:180–186Google Scholar
  65. 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 90:6562–6566Google Scholar
  66. 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 22:5608–5612Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1996

Authors and Affiliations

  • Nobuyoshi Takasaki
    • 1
  • Linda Park
    • 2
  • Masahide Kaeriyama
    • 3
  • Anthony J. Gharrett
    • 4
  • Norihiro Okada
    • 1
  1. 1.Faculty of Bioscience and BiotechnologyTokyo Institute of TechnologyYokohamaJapan
  2. 2.Northwest Fisheries Science CenterCoastal Zone and Estuarine Studies DivisionSeattleUSA
  3. 3.Hokkaido Salmon HatcheryFisheries Agency of JapanSapporoJapan
  4. 4.Juneau Center, School of Fisheries and Ocean SciencesUniversity of Alaska FairbanksJuneauUSA

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