Abstract
Short interspersed nuclear elements (SINEs) are the most abundant non-autonomous retroelements in many vertebrate genomes. The events that led to their integration may have had marked effects on the evolution of host genomes. One well-investigated SINE lineage is in the pacific salmon (genusOncorhynchus). Experimental approaches and bioinformatics have been used to investigate the dynamic features and evolutionary impact of these SINEs. Four gene-relatedHpaI SINEs in theCD4L-2a, NOS, MHC andIL1B genes were identified by bioinformatics tool. To investigate these SINEs, PCR amplification and sequencing were performed on eight species of the genusOncorhynchus and one ofSalmo. Unexpectedly, theCD4L-2a, MHC andIL-1B gene loci proved to be dimorphic for theHpaI SINE insertion; this may be attributable to lineage sorting. Sequence transduction and horizontal transmission events also occurred inCD4L-2a. To elucidate the impact ofHpaI SINEs on pacific salmon genomes and the diversity of transcriptomes, 243,668 mRNA sequences from the GenBank database were analyzed. A total of 163 mRNA sequences were identified as fused withHpaI SINEs. Among these, 87 ESTs were annotated into 41 functional genes. Our data suggest that SINEs could contribute to the genomic diversity of the pacific salmon by exonization and could move more dynamically within this genome by lineage sorting, sequence transduction and horizontal transmission.
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Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z., Miller W andLipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402.
Baban S, Freeman JD andMager DL (1996) Transcripts from a novel human KRAB zinc finger gene contain splicedAlu and endogenous retroviral segments. Genomics 33: 463–472.
Claverie-Martin F, Gonzalez-Acosta H, Flores C, Anton-Gamero M andGarcia-Nieto V (2003) De novo insertion of anAlu sequence in the coding region of the CLCN5 gene results in Dent's disease. Hum. Genet. 113: 480–485.
Dagan T, Sorek R, Sharon E, Ast G andGraur D (2004) AluGene: a database ofAlu elements incorporated within protein-coding genes. Nucleic Acids Res. 32: D489–492.
Deininger PL andBatzer MA (1999)Alu repeats and human disease. Mol. Genet. Metab. 67: 183–193.
Hamada M, Kido Y, Himberg M, Reist JD, Ying C, Hasegawa M andOkada N (1997) A newly isolated family of short interspersed repetitive elements (SINEs) in coregonid fishes (whitefish) with sequences that are almost identical to those of the SmaI family of repeats: possible evidence for the horizontal transfer of SINEs. Genetics 146: 355–367.
Huh JW, Kim TH, Yi JM, Park ES, Kim WY, Shin HS, Kim DS, Min DS, Kim SS, Kim CB andKim HS (2006) Molecular evolution of the periphilin gene in relation to human endogenous retrovirus melement. J. Mol. Evol. 62: 730–737.
Jurka J (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet. 16: 418–420.
Kido Y, Aono M, Yamaki T, Matsumoto K, Murata S, Saneyoshi M andOkada N (1991) Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution. Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution. Proc. Natl. Acad. Sci. USA 88: 2326–2330.
Kido Y, Himberg M, Takasaki N andOkada N (1994) Amplification of distinct subfamilies of short interspersed elements during evolution of the Salmonidae. J. Mol. Biol. 241: 633–644.
Kido Y, Saitoh M, Murata S andOkada N (1995) Evolution of the active sequences of the HpaI short interspersed elements. J. Mol. Evol. 41: 986–995.
Kim HS, Hirai H andTakenaka O (1996) Molecular features of the TSPY gene of gibbons and Old World monkeys. Chrom. Res. 4: 500–506.
Kreahling J andGraveley BR (2004) The origins and implications ofAluternative splicing. Trends Genet. 20: 1–4.
Kutsche K, Ressler B, Katzera HG, Orth U, Gillessen-Kaesbach G, Morlot S, Schwinger E andGal A (2002) Characterization of breakpoint sequences of five rearrangements in L1CAM and ABCD1 (ALD) genes. Hum. Mutat. 19: 526–535.
Lev-Maor G, Sorek R, Shomron N andAst G (2003) The birth of an alternatively spliced exon: 3′ splice-site selection inAlu exons. Science 300: 1288–1291.
Li WH, Gu Z, Wang H andNekrutenko A (2001) Evolutionary analyses of the human genome. Nature 409: 847–849.
Matsumoto K, Murakami K andOkada N (1986) Gene for lysine tRNA1 may be a progenitor of the highly repetitive and transcribable sequences present in the salmon genome. Proc. Natl. Acad. Sci. USA 83: 3156–3160.
Medstrand P, Landry JR andMager DL (2001) Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-1 genes in human. J. Biol. Chem. 276: 1896–1903.
Mighell AJ, Markham AF andRobinson PA (1997)Alu sequences. FEBS Lett. 417: 1–5.
Murata S, Takasaki N, Saitoh M andOkada 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.
Nishihara H, Smit AF andOkada N (2006) Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res. 16: 864–874.
Okada N (1991) SINEs: short interspersed repeated elements of the eukaryotic genome. Trends Ecol. Evol. 6: 358–361.
Oldridge M, Zackai EH, McDonald-McGinn DM, Iseki S, Morriss-Kay GG, Twigg SR, Johnson D, Wall SA, Jiang W, Theda C, Jabs EW andWilkie AO (1999) De novoalu-element insertions in FGFR2 identify a distinct pathological basis for Apert syndrome. Am. J. Hum. Genet. 64: 446–461.
Piskurek O, Austin CC andOkada N (2006) Sauria SINEs: Novel short interspersed retroposable elements that are widespread in reptile genomes. J. Mol. Evol. 62: 630–644.
Polak P andDomany E (2006)Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics 7: 133.
Ray DA, Xing J, Salem AH andBatzer MA (2006) SINEs of a nearly perfect character. Syst. Biol. 55: 928–935.
Shedlock AM andOkada N (2000) SINE insertion: powerful tools for molecular systematics. Bioessays 22: 148–160.
Sheikh FG, Mukhopadhyay SS andGupta P (2002) Pstl repeat: a family of short interspersed nucleotide element (SINE)-like sequences in the genomes of cattle, goat, and buffalo. Genome 45: 44–50.
Sin HS, Huh JW, Kim DS, Kang DW, Min DS, Kim TH, Ha HS, Kim HH, Lee SY andKim HS (2006) Transcriptional control of the HERV-HLTR element of the GSDML gene in human tissues and cancer cells. Arch. Virol. 151: 1985–1994.
Sorek R, Ast G andGraur D (2002)Alu-containing exons are alternatively spliced. Genome Res. 12: 1060–1067.
Takahashi K, Terai Y, Nishida M andOkada N (1998) A novel family of short interspersed repetitive elements (SINEs) from cichlids: the patterns of insertion of SINEs at orthologous loci support the proposed monophyly of four major groups of cichlid fishes in Lake Tanganyika. Mol. Biol. Evol. 15: 391–407.
Takasaki N, Murata S, Saitoh M, Kobayashi T, Park L andOkada 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.
Takasaki N, Yamaki T, Hamada M, Park L andOkada N (1997) The salmon SmaI family of short interspersed repetitive elements (SINEs): interspecific and intraspecific variation of the insertion of SINEs in the genomes of chum and pink salmon. Genetics 146: 369–380.
Ullu E, Murphy S andMelli M (1982) Human 7SL RNA consists of a 140 nucleotide middle-repetitive sequence inserted in analu sequence. Cell 29: 195–202.
Wang T, Johnson N, Zou J, Bols N andSecombes CJ (2004) Sequencing and expression of the second allele of the interleukin-1beta1 gene in rainbow trout (Oncorhynchus mykiss): identification of a novel SINE in the third intron. Fish Shellfish Immunol. 16: 335–358.
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Huh, JW., Kim, DS., Noh, YN. et al. Dynamic evolution of tRNAThr-derivedHpaI SINEs and effect on genomes ofOncorhynchus species. Genes & Genomics 31, 217–226 (2009). https://doi.org/10.1007/BF03191193
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DOI: https://doi.org/10.1007/BF03191193