Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata.

The plant genome evolves with rapid proliferation of LTR-type retrotransposons, which is associated with their clustered accumulation in gene-poor regions, such as centromeres. Despite their major role for plant genome evolution, no mobile LTR element with targeted integration into gene-poor regions has been identified in plants. Here, we report such targeted integrations de novo. We and others have previously shown that an ATCOPIA93 family retrotransposon in Arabidopsis thaliana is mobilized when the DNA methylation machinery is compromised. Although ATCOPIA93 family elements are low copy number in the wild-type A. thaliana genome, high-copy-number related elements are found in the wild-type Arabidopsis lyrata genome, and they show centromere-specific localization. To understand the mechanisms for the clustered accumulation of the A. lyrata elements directly, we introduced one of them, named Tal1 (Transposon of Arabidopsis lyrata 1), into A. thaliana by transformation. The introduced Tal1 was retrotransposed in A. thaliana, and most of the retrotransposed copies were found in centromeric repeats of A. thaliana, suggesting targeted integration. The targeted integration is especially surprising because the centromeric repeat sequences differ considerably between A. lyrata and A. thaliana. Our results revealed unexpectedly dynamic controls for evolution of the transposon-rich heterochromatic regions.

[1]  Richard M. Clark,et al.  The Arabidopsis lyrata genome sequence and the basis of rapid genome size change , 2011, Nature Genetics.

[2]  R. Slotkin The epigenetic control of the Athila family of retrotransposons in Arabidopsis , 2010, Epigenetics.

[3]  D. Voytas,et al.  Retrotransposon vectors for gene delivery in plants , 2010, Mobile DNA.

[4]  Jianxin Ma,et al.  Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. , 2010, The Plant journal : for cell and molecular biology.

[5]  D. Weigel,et al.  Selective epigenetic control of retrotransposition in Arabidopsis , 2009, Nature.

[6]  T. Kakutani,et al.  Bursts of retrotransposition reproduced in Arabidopsis , 2009, Nature.

[7]  R. Dawe,et al.  Centromeres: long intergenic spaces with adaptive features , 2009, Functional & Integrative Genomics.

[8]  Daniel F Voytas,et al.  Chromodomains direct integration of retrotransposons to heterochromatin. , 2008, Genome research.

[9]  M. Grandbastien,et al.  Distribution dynamics of the Tnt1 retrotransposon in tobacco , 2007, Molecular Genetics and Genomics.

[10]  F. Han,et al.  Construction and behavior of engineered minichromosomes in maize , 2007, Proceedings of the National Academy of Sciences.

[11]  S. Grewal,et al.  Heterochromatin revisited , 2007, Nature Reviews Genetics.

[12]  J. Bennetzen,et al.  Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution , 2006, Proceedings of the National Academy of Sciences.

[13]  Rod A Wing,et al.  Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. , 2006, Genome research.

[14]  D. Charlesworth,et al.  Centromere Locations and Associated Chromosome Rearrangements in Arabidopsis lyrata and A. thaliana , 2006, Genetics.

[15]  S. Jackson,et al.  Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. , 2005, Genome research.

[16]  L. Schauser,et al.  LORE1, an active low-copy-number TY3-gypsy retrotransposon family in the model legume Lotus japonicus. , 2005, The Plant journal : for cell and molecular biology.

[17]  Jiming Jiang,et al.  Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. , 2005, Molecular biology and evolution.

[18]  S. Nasuda,et al.  Structure and genomic organization of centromeric repeats in Arabidopsis species , 2005, Molecular Genetics and Genomics.

[19]  Dan Nettleton,et al.  Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae , 2004, Genome Biology.

[20]  Michael Black,et al.  Role of transposable elements in heterochromatin and epigenetic control , 2004, Nature.

[21]  J. Deragon,et al.  Athila, a new retroelement from Arabidopsis thaliana , 1995, Plant Molecular Biology.

[22]  T. Schwarzacher,et al.  Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species , 2004, Chromosome Research.

[23]  R. Dawe,et al.  Plant neocentromeres: fast, focused, and driven , 2004, Chromosome Research.

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

[25]  S. Henikoff,et al.  Conflict begets complexity: the evolution of centromeres. , 2002, Current opinion in genetics & development.

[26]  S. Jacobsen,et al.  DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis , 2002, The EMBO journal.

[27]  F. Blattner,et al.  Functional Rice Centromeres Are Marked by a Satellite Repeat and a Centromere-Specific Retrotransposon Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003079. , 2002, The Plant Cell Online.

[28]  R. Martienssen,et al.  Dependence of Heterochromatic Histone H3 Methylation Patterns on the Arabidopsis Gene DDM1 , 2002, Science.

[29]  H. Kotani,et al.  Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3. , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[30]  T. Kakutani,et al.  Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis , 2001, Nature.

[31]  S. Yamamoto,et al.  The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets , 2001, Zeitschrift für Induktive Abstammungs- und Vererbungslehre.

[32]  R. Martienssen,et al.  Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). , 2001, Genes & development.

[33]  C. Camilleri,et al.  Tnt1 transposition events are induced by in vitro transformation of Arabidopsis thaliana, and transposed copies integrate into genes , 2001, Molecular Genetics and Genomics.

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

[35]  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.

[36]  J. Paszkowski,et al.  Endogenous Targets of Transcriptional Gene Silencing in Arabidopsis , 2000, Plant Cell.

[37]  S Wright,et al.  Transposon diversity in Arabidopsis thaliana. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  T. Kakutani,et al.  Silencing of Retrotransposons in Arabidopsis and Reactivation by the ddm1 Mutation , 2000, Plant Cell.

[39]  Robert A. Martienssen,et al.  Differential methylation of genes and retrotransposons facilitates shotgun sequencing of the maize genome , 1999, Nature Genetics.

[40]  J. Jeddeloh,et al.  Maintenance of genomic methylation requires a SWI2/SNF2-like protein , 1999, Nature Genetics.

[41]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

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

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

[44]  T. Kakutani,et al.  Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[45]  H. Hirochika,et al.  Retrotransposons of rice involved in mutations induced by tissue culture. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Martienssen,et al.  Arabidopsis thaliana DNA methylation mutants. , 1993, Science.

[47]  D. Chalker,et al.  Integration specificity of retrotransposons and retroviruses. , 1990, Annual review of genetics.

[48]  D. Hickey Selfish DNA: a sexually-transmitted nuclear parasite. , 1982, Genetics.