Abstract
Retrotransposons, which proliferate by reverse transcription of RNA intermediates, comprise a major portion of plant genomes. Plants often change the genome size and organization during evolution by rapid proliferation and deletion of long terminal repeat (LTR) retrotransposons. Precise transposon sequences throughout the Arabidopsis thaliana genome and the trans-acting mutations affecting epigenetic states make it an ideal model organism with which to study transposon dynamics. Here we report the mobilization of various families of endogenous A. thaliana LTR retrotransposons identified through genetic and genomic approaches with high-resolution genomic tiling arrays and mutants in the chromatin-remodelling gene DDM1 (DECREASE IN DNA METHYLATION 1). Using multiple lines of self-pollinated ddm1 mutant, we detected an increase in copy number, and verified this for various retrotransposons in a gypsy family (ATGP3) and copia families (ATCOPIA13, ATCOPIA21, ATCOPIA93), and also for a DNA transposon of a Mutator family, VANDAL21. A burst of retrotransposition occurred stochastically and independently for each element, suggesting an additional autocatalytic process. Furthermore, comparison of the identified LTR retrotransposons in related Arabidopsis species revealed that a lineage-specific burst of retrotransposition of these elements did indeed occur in natural Arabidopsis populations. The recent burst of retrotransposition in natural population is targeted to centromeric repeats, which is presumably less harmful than insertion into genes. The ddm1-induced retrotransposon proliferations and genome rearrangements mimic the transposon-mediated genome dynamics during evolution and provide experimental systems with which to investigate the controlling molecular factors directly.
MeSH Terms
Arabidopsis/classification,genetics
Arabidopsis Proteins/genetics
Centromere/genetics
DNA Methylation
DNA Transposable Elements/genetics
DNA, Satellite/genetics
DNA-Binding Proteins/genetics
Epigenesis, Genetic
Evolution, Molecular
Gene Dosage/genetics
Genome, Plant/genetics
Genomic Instability
Genomics
Mutagenesis, Insertional/genetics
Phenotype
Phylogeny
Recombination, Genetic/genetics
Retroelements/genetics
Stochastic Processes
Transcription Factors/genetics
Chemicals
Arabidopsis Proteins
DDM1 protein, Arabidopsis
DNA Transposable Elements
DNA, Satellite
DNA-Binding Proteins
Retroelements
Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Tsukahara Sayuri
Department of Integrated Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan.
Kobayashi Akie
Kawabe Akira
Mathieu Olivier
Miura Asuka
Kakutani Tetsuji
References (30)
30 references, click to expand
-
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
Nature. 2000 Dec 14;408(6814):796-815
PMID: 11130711
-
Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae.
Genome Biol. 2004;5(10):R78
PMID: 15461796
-
DNA methylation and epigenetics.
Annu Rev Plant Biol. 2004;55:41-68
PMID: 15725056
-
Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1).
Genes Dev. 2001 Mar 1;15(5):591-602
PMID: 11238379
-
Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana.
Plant J. 1997 Dec;12(6):1447-51
PMID: 9450349
-
Arabidopsis MET1 cytosine methyltransferase mutants.
Genetics. 2003 Mar;163(3):1109-22
PMID: 12663548
-
Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.
Nature. 2008 Mar 13;452(7184):215-9
PMID: 18278030
-
Selective epigenetic control of retrotransposition in Arabidopsis.
Nature. 2009 Sep 17;461(7262):427-30
PMID: 19734882
-
Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene.
Genes Dev. 2001 Jul 15;15(14):1753-8
PMID: 11459824
-
Arabidopsis thaliana DNA methylation mutants.
Science. 1993 Jun 25;260(5116):1926-8
PMID: 8316832
-
The diversity of LTR retrotransposons.
Genome Biol. 2004;5(6):225
PMID: 15186483
-
Gardening the genome: DNA methylation in Arabidopsis thaliana.
Nat Rev Genet. 2005 May;6(5):351-60
PMID: 15861207
-
FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems.
Cell. 2001 Jan 12;104(1):131-42
PMID: 11163246
-
Plant retrotransposons.
Annu Rev Genet. 1999;33:479-532
PMID: 10690416
-
Endogenous targets of transcriptional gene silencing in Arabidopsis.
Plant Cell. 2000 Jul;12(7):1165-78
PMID: 10899982
-
Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution.
Genetics. 2000 Dec;156(4):2019-31
PMID: 11102392
-
Transposon diversity in Arabidopsis thaliana.
Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7376-81
PMID: 10861007
-
Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis.
Curr Biol. 2003 Mar 4;13(5):421-6
PMID: 12620192
-
Developmental abnormalities and epimutations associated with DNA hypomethylation mutations.
Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12406-11
PMID: 8901594
-
Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis.
Nature. 2001 May 10;411(6834):212-4
PMID: 11346800
-
Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation.
Plant Cell. 2000 Mar;12(3):357-69
PMID: 10715322
-
Patterns of DNA variation among three centromere satellite families in Arabidopsis halleri and A. lyrata.
J Mol Evol. 2007 Feb;64(2):237-47
PMID: 17160639
-
Maintenance of genomic methylation requires a SWI2/SNF2-like protein.
Nat Genet. 1999 May;22(1):94-7
PMID: 10319870
-
Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification.
PLoS Biol. 2003 Dec;1(3):E67
PMID: 14691539
-
Highly integrated single-base resolution maps of the epigenome in Arabidopsis.
Cell. 2008 May 2;133(3):523-36
PMID: 18423832
-
Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development.
Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8449-54
PMID: 8710891
-
Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution.
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17638-43
PMID: 17101966
-
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
Mol Biol Evol. 2007 Aug;24(8):1596-9
PMID: 17488738
-
RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana.
EMBO J. 1995 May 15;14(10):2364-73
PMID: 7774594
-
Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium.
Genome Res. 2006 Oct;16(10):1252-61
PMID: 16954538