Assessing the Impact of Transgenerational Epigenetic Variation on Complex Traits
Publication Date
June 26, 2009
Journal
PLOS Genetics
Authors
Frank Johannes, Emmanuelle Porcher, Felipe K. Teixeira, Vera Saliba Colombani, et al
Volume
5
Issue
6
Pages
e1000530
DOI
https://dx.plos.org/10.1371/journal.pgen.1000530
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1000530
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/19557164
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2696037
Europe PMC
http://europepmc.org/abstract/MED/19557164
Web of Science
000268444600005
Scopus
67651227407
Mendeley
http://www.mendeley.com/research/assessing-impact-transgenerational-epigenetic-variation-complex-traits
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CiteULike | Further Information

Mendeley | Further Information

{"title"=>"Assessing the impact of transgenerational epigenetic variation on complex traits", "type"=>"journal", "authors"=>[{"first_name"=>"Frank", "last_name"=>"Johannes", "scopus_author_id"=>"34770287600"}, {"first_name"=>"Emmanuelle", "last_name"=>"Porcher", "scopus_author_id"=>"12775372000"}, {"first_name"=>"Felipe K.", "last_name"=>"Teixeira", "scopus_author_id"=>"26421877400"}, {"first_name"=>"Vera", "last_name"=>"Saliba-Colombani", "scopus_author_id"=>"8209080500"}, {"first_name"=>"Matthieu", "last_name"=>"Simon", "scopus_author_id"=>"35389790400"}, {"first_name"=>"Nicolas", "last_name"=>"Agier", "scopus_author_id"=>"22952909800"}, {"first_name"=>"Agnès", "last_name"=>"Bulski", "scopus_author_id"=>"8558513400"}, {"first_name"=>"Juliette", "last_name"=>"Albuisson", "scopus_author_id"=>"16633280300"}, {"first_name"=>"Fabiana", "last_name"=>"Heredia", "scopus_author_id"=>"26660495100"}, {"first_name"=>"Pascal", "last_name"=>"Audigier", "scopus_author_id"=>"34874583400"}, {"first_name"=>"David", "last_name"=>"Bouchez", "scopus_author_id"=>"7003903349"}, {"first_name"=>"Christine", "last_name"=>"Dillmann", "scopus_author_id"=>"6602674417"}, {"first_name"=>"Philippe", "last_name"=>"Guerche", "scopus_author_id"=>"6602744588"}, {"first_name"=>"Frédéric", "last_name"=>"Hospital", "scopus_author_id"=>"55952256500"}, {"first_name"=>"Vincent", "last_name"=>"Colot", "scopus_author_id"=>"6701570802"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-67651227407", "pui"=>"354995719", "sgr"=>"67651227407", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "issn"=>"15537390", "pmid"=>"19557164", "doi"=>"10.1371/journal.pgen.1000530"}, "id"=>"297181ed-59e5-3d04-8fee-99389b150bd7", "abstract"=>"Loss or gain of DNA methylation can affect gene expression and is sometimes transmitted across generations. Such epigenetic alterations are thus a possible source of heritable phenotypic variation in the absence of DNA sequence change. However, attempts to assess the prevalence of stable epigenetic variation in natural and experimental populations and to quantify its impact on complex traits have been hampered by the confounding effects of DNA sequence polymorphisms. To overcome this problem as much as possible, two parents with little DNA sequence differences, but contrasting DNA methylation profiles, were used to derive a panel of epigenetic Recombinant Inbred Lines (epiRILs) in the reference plant Arabidopsis thaliana. The epiRILs showed variation and high heritability for flowering time and plant height ( approximately 30%), as well as stable inheritance of multiple parental DNA methylation variants (epialleles) over at least eight generations. These findings provide a first rationale to identify epiallelic variants that contribute to heritable variation in complex traits using linkage or association studies. More generally, the demonstration that numerous epialleles across the genome can be stable over many generations in the absence of selection or extensive DNA sequence variation highlights the need to integrate epigenetic information into population genetics studies.", "link"=>"http://www.mendeley.com/research/assessing-impact-transgenerational-epigenetic-variation-complex-traits", "reader_count"=>441, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>36, "Researcher"=>117, "Student > Doctoral Student"=>15, "Student > Ph. D. 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Student"=>136, "Student > Postgraduate"=>18, "Student > Master"=>45, "Other"=>9, "Student > Bachelor"=>35, "Lecturer"=>4, "Lecturer > Senior Lecturer"=>3, "Professor"=>19}, "reader_count_by_subject_area"=>{"Unspecified"=>11, "Agricultural and Biological Sciences"=>349, "Arts and Humanities"=>1, "Chemistry"=>1, "Computer Science"=>5, "Earth and Planetary Sciences"=>4, "Engineering"=>3, "Environmental Science"=>6, "Biochemistry, Genetics and Molecular Biology"=>46, "Mathematics"=>2, "Medicine and Dentistry"=>6, "Physics and Astronomy"=>1, "Psychology"=>2, "Social Sciences"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Social Sciences"=>{"Social Sciences"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>2}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>11}, "Environmental Science"=>{"Environmental Science"=>6}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Engineering"=>{"Engineering"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>4}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>349}, "Computer Science"=>{"Computer Science"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>46}}, "reader_count_by_country"=>{"United States"=>13, "Uruguay"=>1, "Philippines"=>1, "United Kingdom"=>7, "Portugal"=>2, "Spain"=>2, "India"=>1, "New Zealand"=>2, "Canada"=>2, "Austria"=>2, "Netherlands"=>3, "Belgium"=>1, "Norway"=>2, "Qatar"=>1, "Brazil"=>5, "Denmark"=>1, "Mexico"=>1, "South Africa"=>1, "Italy"=>2, "France"=>3, "Australia"=>1, "Chile"=>1, "Peru"=>1, "Germany"=>2}, "group_count"=>22}

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/892737"], "description"=>"<p>Top panels: density histograms of raw phenotypic values for flowering time and plant height for the Col-<i>ddm1</i> parental line, the Col-wt epiRILs, and the Col-wt parental line. The units on the x-axis are given in <i>days</i> and <i>cm</i> for these traits, respectively; the y-axis shows the density. Bottom panels: box-whisker plots for the three populations (a: Col-wt parental line; b: Col-<i>ddm1</i> parental line; c: Col-wt epiRILs) with sample median; the whiskers mark off ±3 standard deviations from the mean; outlier data points are represented by open circles. A total of 16 individual Col-wt epiRIL plants were outliers (>3SD) for flowering time and 52 for plant height. These outliers mainly belong to a few Col-wt epiRILs lines (3 and 8 for flowering time and plant height, respectively) and were removed for subsequent heritability analysis.</p>", "links"=>[], "tags"=>["evolutionary biology/genomics", "genetics and genomics", "genetics and genomics/complex traits", "genetics and genomics/epigenetics", "genetics and genomics/genomics", "genetics and genomics/plant genetics and gene expression", "genetics and genomics/population genetics", "molecular biology", "molecular biology/dna methylation", "plant biology", "plant biology/agricultural biotechnology", "plant biology/plant genetics and gene expression"], "article_id"=>563171, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phenotypic_distributions_/563171", "title"=>"Phenotypic distributions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 00:52:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/892830"], "description"=>"<p>(A) Flowering time. (B) Plant height. The different populations are color-coded as indicated in the top left panel. * <i>p</i>-value (<i>p<sub>B</sub></i>)<0.05; ** <i>p</i>-value (<i>p<sub>B</sub></i>)<0.01; The effective sample sizes are indicated below each bar plot.</p>", "links"=>[], "tags"=>["phenotypic", "means"], "article_id"=>563275, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_phenotypic_means_and_variances_/563275", "title"=>"Comparison of phenotypic means and variances.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 00:54:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/893218"], "description"=>"<p>(A,B) Southern blot analysis of two TE families (<i>MULE</i> and <i>CACTA</i>, respectively) in three individuals of each parental line (Col-wt and Col-<i>ddm1</i>), as well as in four early- and four late-flowering Col-wt epiRILs (F9). Genomic DNA was digested using <i>Hin</i>dIII and hybridized after gel electrophoresis and transfer to a nylon membrane using previously described probes <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#pgen.1000530-Miura1\" target=\"_blank\">[19]</a>,<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#pgen.1000530-Singer1\" target=\"_blank\">[20]</a>. Question marks indicate possible new insertion sites for <i>MULE</i>. For CACTA, white and black stars designate excision events and new insertions, respectively. The five <i>CACTA</i> copies present in wt Columbia <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#pgen.1000530-Miura2\" target=\"_blank\">[42]</a> are indicated on the right.</p>", "links"=>[], "tags"=>["blot", "te"], "article_id"=>563660, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Southern_blot_analysis_of_TE_mobilization_/563660", "title"=>"Southern blot analysis of TE mobilization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 01:01:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/892649"], "description"=>"<p>Grey bars represent the <i>A. thaliana</i> genome, and triangles represent DNA methylation. Except at the <i>DDM1</i> locus (black and white squares) located on chromosome 5, the two parents (Col-wt and Col-<i>ddm1</i>) are near isogenic; they differ however in their levels of DNA methylation. An F1 individual was backcrossed to the Col-wt parental line, and 509 <i>DDM/DDM1</i> BC1 individuals were selfed. After three more selfing (BC1-S4), three independent sublines were established and selfed once to obtain the Col-wt epiRIL population (See <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#s4\" target=\"_blank\">Materials and Methods</a>).</p>", "links"=>[], "tags"=>["col-wt"], "article_id"=>563087, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Construction_of_the_Col_wt_epiRILs_/563087", "title"=>"Construction of the Col-wt epiRILs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 00:51:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/442452", "https://ndownloader.figshare.com/files/442488", "https://ndownloader.figshare.com/files/442508", "https://ndownloader.figshare.com/files/442534", "https://ndownloader.figshare.com/files/442561", "https://ndownloader.figshare.com/files/442597", "https://ndownloader.figshare.com/files/442627"], "description"=>"<div><p>Loss or gain of DNA methylation can affect gene expression and is sometimes transmitted across generations. Such epigenetic alterations are thus a possible source of heritable phenotypic variation in the absence of DNA sequence change. However, attempts to assess the prevalence of stable epigenetic variation in natural and experimental populations and to quantify its impact on complex traits have been hampered by the confounding effects of DNA sequence polymorphisms. To overcome this problem as much as possible, two parents with little DNA sequence differences, but contrasting DNA methylation profiles, were used to derive a panel of epigenetic Recombinant Inbred Lines (epiRILs) in the reference plant <em>Arabidopsis thaliana</em>. The epiRILs showed variation and high heritability for flowering time and plant height (∼30%), as well as stable inheritance of multiple parental DNA methylation variants (epialleles) over at least eight generations. These findings provide a first rationale to identify epiallelic variants that contribute to heritable variation in complex traits using linkage or association studies. More generally, the demonstration that numerous epialleles across the genome can be stable over many generations in the absence of selection or extensive DNA sequence variation highlights the need to integrate epigenetic information into population genetics studies.</p></div>", "links"=>[], "tags"=>["assessing", "transgenerational", "epigenetic", "traits"], "article_id"=>147190, "categories"=>["Genetics", "Cell Biology", "Evolutionary Biology", "Molecular Biology", "Cancer", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000530.s001", "https://dx.doi.org/10.1371/journal.pgen.1000530.s002", "https://dx.doi.org/10.1371/journal.pgen.1000530.s003", "https://dx.doi.org/10.1371/journal.pgen.1000530.s004", "https://dx.doi.org/10.1371/journal.pgen.1000530.s005", "https://dx.doi.org/10.1371/journal.pgen.1000530.s006", "https://dx.doi.org/10.1371/journal.pgen.1000530.s007"], "stats"=>{"downloads"=>8, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Assessing_the_Impact_of_Transgenerational_Epigenetic_Variation_on_Complex_Traits/147190", "title"=>"Assessing the Impact of Transgenerational Epigenetic Variation on Complex Traits", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-06-26 01:59:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/893012"], "description"=>"<p>Name and position of probed sequences are indicated at the top. Horizontal bars underneath indicate closely linked sequences. Black and white rectangles represent high (wt) methylation, and absence of methylation or <i>ddm1</i>-induced hypomethylation, respectively. Sectored rectangles represent intermediate methylation levels between Col-wt and Col-<i>ddm1</i> (for examples of actual methylation measurements, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#pgen.1000530.s001\" target=\"_blank\">Figure S1</a>). Segregation of methylation states among the 22 Col-wt epiRILs (F9) is summarized for each sequence at the bottom of the graph.</p>", "links"=>[], "tags"=>["dna", "methylation", "flowering", "col-wt"], "article_id"=>563448, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Segregation_analysis_of_DNA_methylation_in_a_sample_of_early_and_late_flowering_Col_wt_epiRILs_/563448", "title"=>"Segregation analysis of DNA methylation in a sample of early and late flowering Col-wt epiRILs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 00:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/892912"], "description"=>"<p>(A,B) Percent of phenotypic variance explained by each of the tested variables and their 95% confidence intervals; G = Greenhouse effect; M = Micro-environment effect; L = Line-effect; S = Subline-effect. The effective samples sizes were 2856 and 2813 for flowering time and plant height, respectively. Outliers (>3SD) were removed from the analyses. (C,D) For the two traits, density histograms (red) of Col-wt epiRILs line means (‘genetic’ values) are superimposed over a density histogram of the total phenotypic variation (grey histogram with blue density line). By visual inspection, the distribution of the line means is continuous, suggestive of ‘polygenic’ variation for these traits. (E) Bivariate plot and least-squares fit (black line) of Col-wt epiRILs line means between plant height (<i>x</i>-axis) and flowering time (<i>y</i>-axis) reveals a negligible ‘genetic’ correlation, suggesting that these two traits have a largely distinct heritable basis; * <i>p</i>-value<0.0001; ns = not significant at <i>α</i> = 0.05 (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#pgen.1000530.s006\" target=\"_blank\">Table S5</a>).</p>", "links"=>[], "tags"=>["heritable", "phenotypic"], "article_id"=>563354, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Estimates_of_heritable_phenotypic_variance_/563354", "title"=>"Estimates of heritable phenotypic variance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 00:55:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/893119"], "description"=>"<p>(A) McrBC-QPCR analysis of DNA methylation. (B) RT–QPCR analysis of transcript levels. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#s2\" target=\"_blank\">Results</a> are expressed as % of expression relative to the average of three control genes (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000530#s4\" target=\"_blank\">Materials and Methods</a>).</p>", "links"=>[], "tags"=>["methylation"], "article_id"=>563563, "categories"=>["Genetics", "Plant Biology", "Evolutionary Biology", "Molecular Biology", "Infectious Diseases", "Medicine"], "users"=>["Frank Johannes", "Emmanuelle Porcher", "Felipe K. Teixeira", "Vera Saliba-Colombani", "Matthieu Simon", "Nicolas Agier", "Agnès Bulski", "Juliette Albuisson", "Fabiana Heredia", "Pascal Audigier", "David Bouchez", "Christine Dillmann", "Philippe Guerche", "Frédéric Hospital", "Vincent Colot"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000530.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_methylation_and_expression_analysis_of_the_FWA_locus_/563563", "title"=>"DNA methylation and expression analysis of the <i>FWA</i> locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-06-26 00:59:23"}

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Relative Metric

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