The Arabidopsis thaliana mobilome and its impact at the species level

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Abstract

Transposable elements (TEs) are powerful motors of genome evolution yet a comprehensive assessment of recent transposition activity at the species level is lacking for most organisms. Here, using genome sequencing data for 211 Arabidopsis thaliana accessions taken from across the globe, we identify thousands of recent transposition events involving half of the 326 TE families annotated in this plant species. We further show that the composition and activity of the 'mobilome' vary extensively between accessions in relation to climate and genetic factors. Moreover, TEs insert equally throughout the genome and are rapidly purged by natural selection from gene-rich regions because they frequently affect genes, in multiple ways. Remarkably, loci controlling adaptive responses to the environment are the most frequent transposition targets observed. These findings demonstrate the pervasive, species-wide impact that a rich mobilome can have and the importance of transposition as a recurrent generator of large-effect alleles.

DOI: http://dx.doi.org/10.7554/eLife.15716.001

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Most cited references 55

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Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.

Shawn Cokus, Suhua Feng, Xiaoyu Zhang … (2008)

Cytosine DNA methylation is important in regulating gene expression and in silencing transposons and other repetitive sequences. Recent genomic studies in Arabidopsis thaliana have revealed that many endogenous genes are methylated either within their promoters or within their transcribed regions, and that gene methylation is highly correlated with transcription levels. However, plants have different types of methylation controlled by different genetic pathways, and detailed information on the methylation status of each cytosine in any given genome is lacking. To this end, we generated a map at single-base-pair resolution of methylated cytosines for Arabidopsis, by combining bisulphite treatment of genomic DNA with ultra-high-throughput sequencing using the Illumina 1G Genome Analyser and Solexa sequencing technology. This approach, termed BS-Seq, unlike previous microarray-based methods, allows one to sensitively measure cytosine methylation on a genome-wide scale within specific sequence contexts. Here we describe methylation on previously inaccessible components of the genome and analyse the DNA methylation sequence composition and distribution. We also describe the effect of various DNA methylation mutants on genome-wide methylation patterns, and demonstrate that our newly developed library construction and computational methods can be applied to large genomes such as that of mouse.

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A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.

Paul Scheet, Matthew Stephens (2006)

We present a statistical model for patterns of genetic variation in samples of unrelated individuals from natural populations. This model is based on the idea that, over short regions, haplotypes in a population tend to cluster into groups of similar haplotypes. To capture the fact that, because of recombination, this clustering tends to be local in nature, our model allows cluster memberships to change continuously along the chromosome according to a hidden Markov model. This approach is flexible, allowing for both "block-like" patterns of linkage disequilibrium (LD) and gradual decline in LD with distance. The resulting model is also fast and, as a result, is practicable for large data sets (e.g., thousands of individuals typed at hundreds of thousands of markers). We illustrate the utility of the model by applying it to dense single-nucleotide-polymorphism genotype data for the tasks of imputing missing genotypes and estimating haplotypic phase. For imputing missing genotypes, methods based on this model are as accurate or more accurate than existing methods. For haplotype estimation, the point estimates are slightly less accurate than those from the best existing methods (e.g., for unrelated Centre d'Etude du Polymorphisme Humain individuals from the HapMap project, switch error was 0.055 for our method vs. 0.051 for PHASE) but require a small fraction of the computational cost. In addition, we demonstrate that the model accurately reflects uncertainty in its estimates, in that probabilities computed using the model are approximately well calibrated. The methods described in this article are implemented in a software package, fastPHASE, which is available from the Stephens Lab Web site.

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Mobile elements: drivers of genome evolution.

Haig H. Kazazian (2004)

Mobile elements within genomes have driven genome evolution in diverse ways. Particularly in plants and mammals, retrotransposons have accumulated to constitute a large fraction of the genome and have shaped both genes and the entire genome. Although the host can often control their numbers, massive expansions of retrotransposons have been tolerated during evolution. Now mobile elements are becoming useful tools for learning more about genome evolution and gene function.

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Author and article information

Contributors

Daniel Zilberman

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (hwp): eLife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 03 June 2016

Publication date Collection: 2016

Volume: 5

Electronic Location Identifier: e15716

Affiliations

[1 ]Institut de Biologie de l’Ecole Normale Supérieure, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, Ecole Normale Supérieure , Paris, France

[2 ]Roche NimbleGen, Inc , Madison, United States

[3 ]deptDepartment of Molecular, Cellular and Developmental Biology , Yale University , New Haven, United States

[4 ]deptWatson School of Biological Sciences , Howard Hughes Medical Institute, Gordon and Betty Moore Foundation , Palo Alto, United States

[5 ]Cold Spring Harbor Laboratory , Cold Spring Harbor, United States

[6]University of California , Berkeley, United States

[7]University of California , Berkeley, United States

Author notes

colot@ 123456biologie.ens.fr

Author information

Leandro Quadrana http://orcid.org/0000-0001-6279-211X

Vincent Colot http://orcid.org/0000-0002-6382-1610

Article

Publisher ID: 15716

DOI: 10.7554/eLife.15716

PMC ID: 4917339

PubMed ID: 27258693

SO-VID: cfc279f5-a54b-4830-b4bf-5991833ed575

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This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 02 March 2016

Date accepted : 01 June 2016

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-10-LABX-54 MEMO LIFE

Award Recipient : Vincent Colot

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-11-IDEX-0001-02 PSL* Research University

Award Recipient : Vincent Colot

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: ANR-12-ADAP-0020-01

Award Recipient : Vincent Colot

Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;

Award ID: EpiGeneSys (Award 257082)

Award Recipient : Vincent Colot

Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;

Award Recipient : Amanda Bortolini Silveira

Funded by: Chaire Blaise Pascal;

Award Recipient : Robert A Martienssen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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elife-xml-version 2.5

Author impact statement Population genomics in Arabidopsis thaliana uncovers an extensive repertoire of active transposable element families at the species level and reveals their importance as a source of rare alleles with large effects.

ScienceOpen disciplines: Life sciences

Keywords: transposable elements,dna methylation spreading,gwas,climate,adaptation,large effect alleles,a. thaliana

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ScienceOpen disciplines: Life sciences

Keywords: transposable elements, dna methylation spreading, gwas, climate, adaptation, large effect alleles, a. thaliana

The Arabidopsis thaliana mobilome and its impact at the species level

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Abstract

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Arabidopsis genomics

Most cited references 55

Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.

A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.

Mobile elements: drivers of genome evolution.

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