skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population

Journal Article · · Genome Research
 [1];  [2];  [3];  [4];  [5];  [6];  [6];  [7];  [5];  [8];  [9]
  1. Salk Institute for Biological Studies, La Jolla, CA (United States). Plant Biology Lab.; Salk Institute for Biological Studies, La Jolla, CA (United States). Genomic Analysis Lab.
  2. Salk Institute for Biological Studies, La Jolla, CA (United States). Genomic Analysis Lab.; Univ. of California, San Diego, CA (United States). Bioinformatics Program
  3. Univ. of Missouri, Columbia, MO (United States). Christopher S. Bond Life Sciences Center
  4. Univ. of Missouri, Columbia, MO (United States). Christopher S. Bond Life Sciences Center; Univ. of Missouri, Columbia, MO (United States). Informatics Inst.
  5. Univ. of Missouri, Columbia, MO (United States). Christopher S. Bond Life Sciences Center; Univ. of Missouri, Columbia, MO (United States). Informatics Inst.; Univ. of Missouri, Columbia, MO (United States). Dept. of Computer Science ; Univ. of Missouri, Columbia, MO (United States). National Center for Soybean Biotechnology
  6. Salk Institute for Biological Studies, La Jolla, CA (United States). Genomic Analysis Lab.
  7. Univ. of Illinois at Urbana-Champaign, IL (United States). Dept. of Crop Sciences
  8. Univ. of Missouri, Columbia, MO (United States). Christopher S. Bond Life Sciences Center; Univ. of Missouri, Columbia, MO (United States). National Center for Soybean Biotechnology; Univ. of Missouri, Columbia, MO (United States). Divisions of Plant Science and Biochemistry
  9. Salk Institute for Biological Studies, La Jolla, CA (United States). Plant Biology Lab.; Salk Institute for Biological Studies, La Jolla, CA (United States). Genomic Analysis Lab.; Salk Institute for Biological Studies, La Jolla, CA (United States). Howard Hughes Medical Inst.

Cytosine DNA methylation is one avenue for passing information through cell divisions. Here, we present epigenomic analyses of soybean recombinant inbred lines (RILs) and their parents. Identification of differentially methylated regions (DMRs) revealed that DMRs mostly cosegregated with the genotype from which they were derived, but examples of the uncoupling of genotype and epigenotype were identified. Linkage mapping of methylation states assessed from whole-genome bisulfite sequencing of 83 RILs uncovered widespread evidence for local methylQTL. This epigenomics approach provides a comprehensive study of the patterns and heritability of methylation variants in a complex genetic population over multiple generations, paving the way for understanding how methylation variants contribute to phenotypic variation.

Research Organization:
Univ. of Missouri, Columbia, MO (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
FG02-02ER15309
OSTI ID:
1625624
Journal Information:
Genome Research, Vol. 23, Issue 10; ISSN 1088-9051
Publisher:
Cold Spring Harbor Laboratory PressCopyright Statement
Country of Publication:
United States
Language:
English

References (78)

Analysis of the genome sequence of the flowering plant Arabidopsis thaliana journal December 2000
Paramutation in maize: RNA mediated trans-generational gene silencing journal April 2010
Estimation of False Discovery Rate Using Sequential Permutation p -Values : Sequential Permutation journal February 2013
Spontaneous epigenetic variation in the Arabidopsis thaliana methylome journal September 2011
R/qtl: QTL mapping in experimental crosses journal May 2003
Rhg1 alleles from soybean PI 437654 and PI 88788 respond differentially to isolates of Heterodera glycines in the greenhouse journal May 2005
Reprogramming of DNA Methylation in Pollen Guides Epigenetic Inheritance via Small RNA journal September 2012
Role of the DRM and CMT3 Methyltransferases in RNA-Directed DNA Methylation journal December 2003
Whole-genome sequencing of multiple Arabidopsis thaliana populations journal August 2011
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w journal April 2012
Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning journal February 2008
An epigenetic mutation responsible for natural variation in floral symmetry journal September 1999
Registration of LD00-2817P Soybean Germplasm Line with Resistance to Soybean Cyst Nematode from PI 437654 journal May 2010
Widespread dynamic DNA methylation in response to biotic stress journal June 2012
Dual Binding of Chromomethylase Domains to H3K9me2-Containing Nucleosomes Directs DNA Methylation in Plants journal September 2012
Rapid Establishment of Genetic Incompatibility through Natural Epigenetic Variation journal February 2012
Heritable Epigenetic Variation among Maize Inbreds journal November 2011
Conservation and divergence of methylation patterning in plants and animals journal April 2010
Multiple reference genomes and transcriptomes for Arabidopsis thaliana journal August 2011
Divergence in Expression between Duplicated Genes in Arabidopsis journal August 2007
Molecular and Chromosomal Evidence for Allopolyploidy in Soybean journal July 2009
Trans Chromosomal Methylation in Arabidopsis hybrids journal February 2012
Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor journal January 2011
DAGchainer: a tool for mining segmental genome duplications and synteny journal July 2004
Global Epigenetic and Transcriptional Trends among Two Rice Subspecies and Their Reciprocal Hybrids journal January 2010
Inheritance of a Cancer-Associated MLH1 Germ-Line Epimutation journal February 2007
A map of rice genome variation reveals the origin of cultivated rice journal October 2012
Active DNA Demethylation in Plant Companion Cells Reinforces Transposon Methylation in Gametes journal September 2012
Differential Accumulation of Retroelements and Diversification of NB-LRR Disease Resistance Genes in Duplicated Regions following Polyploidy in the Ancestor of Soybean journal October 2008
Assessing the Impact of Transgenerational Epigenetic Variation on Complex Traits journal June 2009
Release Factor One Is Nonessential in Escherichia coli journal May 2012
Stacking Resistance Alleles from Wild and Domestic Soybean Sources Improves Soybean Cyst Nematode Resistance journal May 2011
Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection journal November 2010
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome journal January 2009
Establishing, maintaining and modifying DNA methylation patterns in plants and animals journal February 2010
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
Epigenetic reprogramming during vegetative phase change in maize journal December 2010
Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis journal May 2008
Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells journal February 2011
Genomic Distribution of Maize Facultative Heterochromatin Marked by Trimethylation of H3K27 journal March 2013
A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening journal July 2006
Developmental relaxation of transposable element silencing in plants: functional or byproduct? journal November 2012
Transgenerational Stability of the Arabidopsis Epigenome Is Coordinated by CG Methylation journal September 2007
Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.): Global gene expression in the maize SAM journal August 2007
Sequencing of natural strains of Arabidopsis thaliana with short reads journal October 2008
The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana journal December 2009
Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. journal November 1993
Meiotically Stable Natural Epialleles of Sadhu, a Novel Arabidopsis Retroposon journal March 2006
Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes journal April 2009
Inherited epigenetic variation — revisiting soft inheritance journal March 2006
Demethylation-Induced Developmental Pleiotropy in Arabidopsis journal August 1996
Genome-Wide Epigenetic Perturbation Jump-Starts Patterns of Heritable Variation Found in Nature journal May 2011
Epigenetic and epigenomic variation in Arabidopsis thaliana journal March 2012
High-throughput approaches for plant epigenomic studies journal April 2011
Transgenerational Epigenetic Instability Is a Source of Novel Methylation Variants journal September 2011
Patterns of population epigenomic diversity journal March 2013
Genome sequence of the palaeopolyploid soybean journal January 2010
‘Leveling’ the playing field for analyses of single-base resolution DNA methylomes journal December 2012
Spontaneous Mutational Effects on Reproductive Traits of Arabidopsis thaliana journal May 2000
Genome-Wide Analysis of DNA Methylation and Gene Expression Changes in Two Arabidopsis Ecotypes and Their Reciprocal Hybrids journal March 2012
Extensive Natural Epigenetic Variation at a De Novo Originated Gene journal April 2013
Epigenetic Reprogramming and Small RNA Silencing of Transposable Elements in Pollen journal February 2009
Relationships Among Phaseoloid Legumes Based on Sequences from Eight Chloroplast Regions journal March 2009
Testing the polyploid past of soybean using a low-copy nuclear gene—Is Glycine (Fabaceae: Papilionoideae) an auto- or allopolyploid? journal May 2006
Gene body methylation is conserved between plant orthologs and is of evolutionary consequence journal January 2013
A Role for RNAi in the Selective Correction of DNA Methylation Defects journal March 2009
TopHat: discovering splice junctions with RNA-Seq journal March 2009
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation journal May 2010
Endogenous, Tissue-Specific Short Interfering RNAs Silence the Chalcone Synthase Gene Family in Glycine max Seed Coats journal October 2009
Epigenetic Natural Variation in Arabidopsis thaliana journal June 2007
Epialleles in plant evolution journal January 2012
Determining the conservation of DNA methylation in Arabidopsis journal February 2009
VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization journal February 2007
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense journal January 2013
Local DNA hypomethylation activates genes in rice endosperm journal October 2010
Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation journal April 2010
Global Analysis of Genetic, Epigenetic and Transcriptional Polymorphisms in Arabidopsis thaliana Using Whole Genome Tiling Arrays journal March 2008

Cited By (86)

Genome-wide epigenetic variation among ash trees differing in susceptibility to a fungal disease journal June 2018
Contribution of epigenetic variation to adaptation in Arabidopsis text January 2018
Genome-wide sampling suggests island divergence accompanied by cryptic epigenetic plasticity in Canada lynx posted_content January 2018
Opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics journal August 2018
An epigenetic breeding system in soybean for increased yield and stability journal May 2018
Emerging Genomic Tools for Legume Breeding: Current Status and Future Prospects journal May 2016
Evolution of DNA Methylation Patterns in the Brassicaceae is Driven by Differences in Genome Organization journal November 2014
Transgenerational effects alter plant defence and resistance in nature journal February 2017
Genomic and epigenomic immunity in common bean: the unusual features of NB-LRR gene family journal November 2017
Contribution of epigenetic variation to adaptation in Arabidopsis text January 2018
Unravelling the epigenomic interactions between parental inbreds resulting in an altered hybrid methylome in pigeonpea journal March 2018
Chromatin dynamics during interphase and cell division: similarities and differences between model and crop plants journal October 2019
Genetic sources of population epigenomic variation journal May 2016
Stable inheritance of DNA methylation allows creation of epigenotype maps and the study of epiallele inheritance patterns in the absence of genetic variation journal August 2017
Quantitative resistance to clubroot infection mediated by transgenerational epigenetic variation in Arabidopsis journal November 2018
High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development journal June 2017
Genome-wide DNA methylation profile in mungbean journal January 2017
Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana text January 2018
TET-mediated epimutagenesis of the Arabidopsis thaliana methylome journal March 2018
Divergent cytosine DNA methylation patterns in single-cell, soybean root hairs journal January 2017
Climate Change Impacts on Seagrass Meadows and Macroalgal Forests: An Integrative Perspective on Acclimation and Adaptation Potential journal June 2018
More Than DNA Methylation: Does Pleiotropy Drive the Complex Pattern of Evolution of Dnmt1? journal January 2020
Mobile small RNAs regulate genome-wide DNA methylation journal January 2016
Transposable elements, a treasure trove to decipher epigenetic variation: insights from Arabidopsis and crop epigenomes journal April 2014
Transgenerational response to stress in plants and its application for breeding journal March 2016
Dynamic DNA methylation reconfiguration during seed development and germination journal September 2017
Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation journal July 2016
An epigenetic breeding system in soybean for increased yield and stability posted_content December 2017
Inter-individual variation in DNA methylation is largely restricted to tissue-specific differentially methylated regions in maize journal February 2017
TET-mediated epimutagenesis of the Arabidopsis thaliana methylome posted_content January 2018
Soybean domestication: the origin, genetic architecture and molecular bases journal January 2017
CG methylation covaries with differential gene expression between leaf and floral bud tissues of Brachypodium distachyon posted_content August 2015
Contrasting DNA methylation responses of inbred fish lines to different rearing environments text January 2019
MethylC-seq library preparation for base-resolution whole-genome bisulfite sequencing journal February 2015
Regulation of genome-wide DNA methylation by mobile small RNAs journal November 2017
Contrasting DNA methylation responses of inbred fish lines to different rearing environments journal June 2019
Methylome evolution in plants journal December 2016
Evolution and selection of R hg1, a copy‐number variant nematode‐resistance locus journal March 2015
Similarity between soybean and Arabidopsis seed methylomes and loss of non-CG methylation does not affect seed development journal October 2017
CG Methylation Covaries with Differential Gene Expression between Leaf and Floral Bud Tissues of Brachypodium distachyon journal March 2016
Substantial Epigenetic Variation Causing Flower Color Chimerism in the Ornamental Tree Prunus mume Revealed by Single Base Resolution Methylome Detection and Transcriptome Sequencing journal August 2018
DNA methylation footprints during soybean domestication and improvement journal September 2018
Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids journal October 2016
The DNA Methylome and Association of Differentially Methylated Regions with Differential Gene Expression during Heat Stress in Brassica rapa journal May 2018
Exploring the extent and scope of epigenetic inheritance journal April 2018
Proximal methylation features associated with nonrandom changes in gene body methylation journal April 2017
Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression journal November 2015
Full-length autonomous transposable elements are preferentially targeted by expression-dependent forms of RNA-directed DNA methylation journal August 2016
Genomic Distribution of H3K9me2 and DNA Methylation in a Maize Genome journal August 2014
Dynamic Changes of Genome-Wide DNA Methylation during Soybean Seed Development journal September 2017
Epigenetic Mechanisms of Abiotic Stress Response and Memory in Plants book April 2019
Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana journal June 2018
Landscape and evolutionary dynamics of terminal repeat retrotransposons in miniature in plant genomes journal January 2016
Uncovering Differentially Methylated Regions (DMRs) in a Salt-Tolerant Rice Variety under Stress: One Step towards New Regulatory Regions for Enhanced Salt Tolerance journal January 2019
Genome-wide comparative analysis of DNA methylation between soybean cytoplasmic male-sterile line NJCMS5A and its maintainer NJCMS5B journal August 2017
Contribution of epigenetic variation to adaptation in Arabidopsis journal October 2018
Genome-wide characterization of DNA methylation, small RNA expression, and histone H3 lysine nine di-methylation in Brassica rapa L. journal June 2018
Widespread natural variation of DNA methylation within angiosperms journal September 2016
Genome-Wide DNA Methylation Profiling in the Lotus (Nelumbo nucifera) Flower Showing its Contribution to the Stamen Petaloid journal May 2019
Recent advancement in modern genomic tools for adaptation of Lablab purpureus L to biotic and abiotic stresses: present mechanisms and future adaptations journal August 2018
Translational genomics for plant breeding with the genome sequence explosion journal August 2015
Genome-wide analysis of DNA methylation to identify genes and pathways associated with male sterility in soybean journal September 2018
Rational development of transformation in Clostridium thermocellum ATCC 27405 via complete methylome analysis and evasion of native restriction–modification systems journal July 2019
Evolutionary patterns of genic DNA methylation vary across land plants journal January 2016
Epigenetic mutations can both help and hinder adaptive evolution journal July 2015
Contrasting DNA methylation responses of inbred fish lines to different rearing environments text January 2019
Base-resolution detection of N 4 -methylcytosine in genomic DNA using 4mC-Tet-assisted-bisulfite- sequencing journal July 2015
Extending the Genotype in Brachypodium by Including DNA Methylation Reveals a Joint Contribution with Genetics on Adaptive Traits journal May 2020
Epigenetic map and genetic map basis of complex traits in cassava population journal January 2017
Constructing a linkage–linkage disequilibrium map using dominant-segregating markers journal November 2015
The Genome and Methylome of a Beetle with Complex Social Behavior, Nicrophorus vespilloides (Coleoptera: Silphidae) journal October 2015
Soybean knowledge base (SoyKB): a web resource for integration of soybean translational genomics and molecular breeding journal October 2013
Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea journal January 2014
DNA methylation and gene expression in Mimulus guttatus journal July 2015
Prodigious plant methylomes journal September 2016
Diversity and dynamics of DNA methylation: epigenomic resources and tools for crop breeding journal January 2019
Three Groups of Transposable Elements with Contrasting Copy Number Dynamics and Host Responses in the Maize (Zea mays ssp. mays) Genome journal April 2014
Genetic Analysis of the Cardiac Methylome at Single Nucleotide Resolution in a Model of Human Cardiovascular Disease journal December 2014
Dynamic Roles for Small RNAs and DNA Methylation during Ovule and Fiber Development in Allotetraploid Cotton journal December 2015
The LSH/DDM1 Homolog MUS-30 Is Required for Genome Stability, but Not for DNA Methylation in Neurospora crassa journal January 2016
Heritable DNA Methylation in CD4+ Cells among Complex Families Displays Genetic and Non-Genetic Effects journal October 2016
Epigenomic diversification within the genus Lupinus journal June 2017
Histone H1 Limits DNA Methylation in Neurospora crassa journal July 2016
Methylated DNA is over-represented in whole-genome bisulfite sequencing data journal October 2014
Transgenerational inheritance or resetting of stress-induced epigenetic modifications: two sides of the same coin journal September 2015
The Dynamics of DNA Methylation in Maize Roots under Pb Stress journal December 2014