Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae

BackgroundRetrotransposons are an abundant component of eukaryotic genomes. The high quality of the Arabidopsis thaliana genome sequence makes it possible to comprehensively characterize retroelement populations and explore factors that contribute to their genomic distribution.ResultsWe identified the full complement of A. thaliana long terminal repeat (LTR) retroelements using RetroMap, a software tool that iteratively searches genome sequences for reverse transcriptases and then defines retroelement insertions. Relative ages of full-length elements were estimated by assessing sequence divergence between LTRs: the Pseudoviridae were significantly younger than the Metaviridae. All retroelement insertions were mapped onto the genome sequence and their distribution was distinctly non-uniform. Although both Pseudoviridae and Metaviridae tend to cluster within pericentromeric heterochromatin, this association is significantly more pronounced for all three Metaviridae sublineages (Metavirus, Tat and Athila). Among these, Tat and Athila are strictly associated with pericentromeric heterochromatin.ConclusionsThe non-uniform genomic distribution of the Pseudoviridae and the Metaviridae can be explained by a variety of factors including target-site bias, selection against integration into euchromatin and pericentromeric accumulation of elements as a result of suppression of recombination. However, comparisons based on the age of elements and their chromosomal location indicate that integration-site specificity is likely to be the primary factor determining distribution of the Athila and Tat sublineages of the Metaviridae. We predict that, like retroelements in yeast, the Athila and Tat elements target integration to pericentromeric regions by recognizing a specific feature of pericentromeric heterochromatin.

[1]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[2]  R. de Frutos,et al.  Structural and evolutionary analysis of the copia-like elements in the Arabidopsis thaliana genome. , 2001, Molecular biology and evolution.

[3]  E. Ganko,et al.  Retrotransposon-gene associations are widespread among D. melanogaster populations. , 2004, Molecular biology and evolution.

[4]  R. Wing,et al.  Genome Dynamics and Evolution of the Mla (Powdery Mildew) Resistance Locus in Barley Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002238. , 2002, The Plant Cell Online.

[5]  S. Jackson,et al.  Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. , 1998, Genetics.

[6]  Wolfgang Stephan,et al.  The evolutionary dynamics of repetitive DNA in eukaryotes , 1994, Nature.

[7]  R. Allshire,et al.  Hairpin RNAs and Retrotransposon LTRs Effect RNAi and Chromatin-Based Gene Silencing , 2003, Science.

[8]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[9]  J. Bennetzen,et al.  Plant retrotransposons. , 1999, Annual review of genetics.

[10]  R. Hudson,et al.  On the role of unequal exchange in the containment of transposable element copy number. , 1988, Genetical research.

[11]  H. Okamoto,et al.  Efficient insertion mutagenesis of Arabidopsis by tissue culture-induced activation of the tobacco retrotransposon Tto1. , 2000, The Plant journal : for cell and molecular biology.

[12]  J. Thompson,et al.  Multiple sequence alignment with Clustal X. , 1998, Trends in biochemical sciences.

[13]  Shawn M. Burgess,et al.  Transcription Start Regions in the Human Genome Are Favored Targets for MLV Integration , 2003, Science.

[14]  F. Bushman Targeting Survival Integration Site Selection by Retroviruses and LTR-Retrotransposons , 2003, Cell.

[15]  Sudhir Kumar,et al.  MEGA2: molecular evolutionary genetics analysis software , 2001, Bioinform..

[16]  L. Duret,et al.  Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. , 2000, Genetics.

[17]  R. Wilson,et al.  What is finished, and why does it matter. , 2002, Genome research.

[18]  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.

[19]  M GREENWOOD,et al.  The statistical study of infectious diseases. , 1946, Journal of the Royal Statistical Society. Series A.

[20]  C. Dean,et al.  Integrated Cytogenetic Map of Chromosome Arm 4S of A. thaliana Structural Organization of Heterochromatic Knob and Centromere Region , 2000, Cell.

[21]  A. Eschstruth,et al.  Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. , 2003, The Plant journal : for cell and molecular biology.

[22]  T. Langdon,et al.  Retrotransposon evolution in diverse plant genomes. , 2000, Genetics.

[23]  J. Stoye,et al.  REPuter: the manifold applications of repeat analysis on a genomic scale. , 2001, Nucleic acids research.

[24]  V. Pereira Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome , 2004, Genome Biology.

[25]  John F. McDonald,et al.  LTR_STRUC: a novel search and identification program for LTR retrotransposons , 2003, Bioinform..

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

[27]  S. Devine,et al.  Yeast Retrotransposons: Finding a Nice Quiet Neighborhood , 1998, Cell.

[28]  M. Marra,et al.  Genetic definition and sequence analysis of Arabidopsis centromeres. , 1999, Science.

[29]  E. Ganko,et al.  Evolutionary history of Oryza sativa LTR retrotransposons: a preliminary survey of the rice genome sequences , 2004, BMC Genomics.

[30]  D. Charlesworth,et al.  Substitution rates in the X- and Y-linked genes of the plants, Silene latifolia and S. dioica. , 2002, Molecular biology and evolution.

[31]  J. Jurka Repbase update: a database and an electronic journal of repetitive elements. , 2000, Trends in genetics : TIG.

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

[33]  Martin J Lercher,et al.  Gene expression, synteny, and local similarity in human noncoding mutation rates. , 2004, Molecular biology and evolution.

[34]  C. Topp,et al.  Centromeric Retroelements and Satellites Interact with Maize Kinetochore Protein CENH3 , 2002, The Plant Cell Online.

[35]  James K. M. Brown,et al.  Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. , 2002, Genome research.

[36]  R. Wilson,et al.  The Complete Sequence of a Heterochromatic Island from a Higher Eukaryote , 2000, Cell.

[37]  M. A. Koch,et al.  Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). , 2000, Molecular biology and evolution.

[38]  S. Eddy,et al.  Automated de novo identification of repeat sequence families in sequenced genomes. , 2002, Genome research.

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

[40]  D. Voytas,et al.  Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. , 1998, Genome research.

[41]  P. Dimitri,et al.  Revising the selfish DNA hypothesis: new evidence on accumulation of transposable elements in heterochromatin. , 1999, Trends in genetics : TIG.

[42]  Thomas L. Madden,et al.  BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. , 1999, FEMS microbiology letters.

[43]  Vikram Bhattacharjee,et al.  Evidence for the contribution of LTR retrotransposons to C. elegans gene evolution. , 2003, Molecular biology and evolution.

[44]  S. Wright,et al.  Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. , 2003, Genome research.

[45]  Vladimir V. Kapitonov,et al.  Molecular paleontology of transposable elements from Arabidopsis thaliana , 2004, Genetica.

[46]  D. Voytas,et al.  Genes of the Pseudoviridae (Ty1/copia retrotransposons). , 2002, Molecular biology and evolution.

[47]  B. Sherman,et al.  A Random Variable Related to the Spacing of Sample Values , 1950 .

[48]  V. Wood,et al.  Retrotransposons and their recognition of pol II promoters: a comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. , 2003, Genome research.

[49]  Phillip SanMiguel,et al.  The paleontology of intergene retrotransposons of maize , 1998, Nature Genetics.

[50]  S. Sandmeyer,et al.  Integration by design , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[52]  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.

[53]  David A Wright,et al.  Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. , 2002, Genome research.