Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence.

We conducted a genome-wide survey of Saccharomyces cerevisiae retrotransposons and identified a total of 331 insertions, including 217 Ty1, 34 Ty2, 41 Ty3, 32 Ty4, and 7 Ty5 elements. Eighty-five percent of insertions were solo long terminal repeats (LTRs) or LTR fragments. Overall, retrotransposon sequences constitute >377 kb or 3.1% of the genome. Independent evolution of retrotransposon sequences was evidenced by the identification of a single-base pair insertion/deletion that distinguishes the highly similar Ty1 and Ty2 LTRs and the identification of a distinct Ty1 subfamily (Ty1'). Whereas Ty1, Ty2, and Ty5 LTRs displayed a broad range of sequence diversity (typically ranging from 70%-99% identity), Ty3 and Ty4 LTRs were highly similar within each element family (most sharing >96% nucleotide identity). Therefore, Ty3 and Ty4 may be more recent additions to the S. cerevisiae genome and perhaps entered through horizontal transfer or past polyploidization events. Distribution of Ty elements is distinctly nonrandom: 90% of Ty1, 82% of Ty2, 95% of Ty3, and 88% of Ty4 insertions were found within 750 bases of tRNA genes or other genes transcribed by RNA polymerase III. tRNA genes are the principle determinant of retrotransposon distribution, and there is, on average, 1.2 insertions per tRNA gene. Evidence for recombination was found near many Ty elements, particularly those not associated with tRNA gene targets. For these insertions, 5'- and 3'-flanking sequences were often duplicated and rearranged among multiple chromosomes, indicating that recombination between retrotransposons can influence genome organization. S. cerevisiae offers the first opportunity to view organizational and evolutionary trends among retrotransposons at the genome level, and we hope our compiled data will serve as a starting point for further investigation and for comparison to other, more complex genomes.

[1]  F. Bushman,et al.  The influence of DNA and nucleosome structure on integration events directed by HIV integrase. , 1994, The Journal of biological chemistry.

[2]  F. Bushman,et al.  Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Levis,et al.  Transposons in place of telomeric repeats at a Drosophila telomere , 1993, Cell.

[4]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[5]  D. Voytas,et al.  The Saccharomyces retrotransposon Ty5 influences the organization of chromosome ends. , 1996, Nucleic acids research.

[6]  A. Pavesi,et al.  Identification of new eukaryotic tRNA genes in genomic DNA databases by a multistep weight matrix analysis of transcriptional control regions. , 1994, Nucleic acids research.

[7]  T. Eickbush,et al.  Origin and evolution of retroelements based upon their reverse transcriptase sequences. , 1990, The EMBO journal.

[8]  H. Fujiwara,et al.  A new family of site-specific retrotransposons, SART1, is inserted into telomeric repeats of the silkworm, Bombyx mori. , 1997, Nucleic acids research.

[9]  J. Bennetzen,et al.  Nested Retrotransposons in the Intergenic Regions of the Maize Genome , 1996, Science.

[10]  H. Biessmann,et al.  Addition of telomere-associated HeT DNA sequences “heals” broken chromosome ends in Drosophila , 1990, Cell.

[11]  G. Fink,et al.  Pseudogenes in yeast? , 1987, Cell.

[12]  D. Garfinkel,et al.  Influences of histone stoichiometry on the target site preference of retrotransposons Ty1 and Ty2 in Saccharomyces cerevisiae. , 1996, Genetics.

[13]  D. Voytas,et al.  The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. , 1996, Genes & development.

[14]  H. Bussey,et al.  The nucleotide sequence of chromosome I from Saccharomyces cerevisiae. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Boeke,et al.  Replication infidelity during a single cycle of Ty1 retrotransposition. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Daniel F. Voytas,et al.  Yeast retrotransposon revealed , 1992, Nature.

[17]  L. Derr,et al.  A role for reverse transcripts in gene conversion , 1993, Nature.

[18]  T. Dingermann,et al.  Genomic organization of the transposable element Tdd-3 from Dictyostelium discoideum. , 1990, Nucleic Acids Research.

[19]  Takashi Yamada,et al.  Zepp, a LINE‐like retrotransposon accumulated in the Chlorella telomeric region , 1997, The EMBO journal.

[20]  S. Devine,et al.  Integration of the yeast retrotransposon Ty1 is targeted to regions upstream of genes transcribed by RNA polymerase III. , 1996, Genes & development.

[21]  K. H. Wolfe,et al.  Molecular evidence for an ancient duplication of the entire yeast genome , 1997, Nature.

[22]  J. Boeke,et al.  High-frequency deletion between homologous sequences during retrotransposition of Ty elements in Saccharomyces cerevisiae. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G. Fink,et al.  Ty elements transpose through an RNA intermediate , 1985, Cell.

[24]  D. Chalker,et al.  Ty3 integrates within the region of RNA polymerase III transcription initiation. , 1992, Genes & development.

[25]  D. Voytas,et al.  Silent chromatin determines target preference of the Saccharomyces retrotransposon Ty5. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Fink,et al.  The Saccharomyces cerevisiae genome contains functional and nonfunctional copies of transposon Ty1 , 1988, Molecular and cellular biology.

[27]  H. Fujiwara,et al.  Structural analysis of TRAS1, a novel family of telomeric repeat-associated retrotransposons in the silkworm, Bombyx mori , 1995, Molecular and cellular biology.

[28]  A. Smit,et al.  Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. , 1995, Journal of molecular biology.

[29]  G. Natsoulis,et al.  Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences , 1993, Cell.

[30]  T. Dingermann,et al.  Transfer RNA genes: landmarks for integration of mobile genetic elements in Dictyostelium discoideum , 1989, Science.

[31]  G. Fink,et al.  The mechanism and consequences of retrotransposition , 1986 .

[32]  G. Fink,et al.  Saccharomyces cerevisiae SPT3 gene is required for transposition and transpositional recombination of chromosomal Ty elements , 1986, Molecular and cellular biology.

[33]  Sudhir Kumar,et al.  MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers , 1994, Comput. Appl. Biosci..

[34]  T. Eickbush,et al.  Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects. , 1991, Proceedings of the National Academy of Sciences of the United States of America.