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Title: Extensive epigenetic reprogramming during the life cycle of Marchantia polymorpha

Journal Article · · Genome Biology (Online)
 [1];  [1];  [1];  [1];  [2];  [1]
  1. Univ. of Zurich (Switzerland). Department of Plant and Microbial Biology and Zurich-Basel Plant Science Center
  2. Monash Univ., Melbourne, VIC (Australia). Biological Sciences

Background In plants, the existence and possible role of epigenetic reprogramming has been questioned because of the occurrence of stably inherited epialleles. Evidence suggests that epigenetic reprogramming does occur during land plant reproduction, but there is little consensus on the generality and extent of epigenetic reprogramming in plants. We studied DNA methylation dynamics during the life cycle of the liverwort Marchantia polymorpha. We isolated thalli and meristems from male and female gametophytes, archegonia, antherozoids, as well as sporophytes at early and late developmental stages, and compared their DNA methylation profiles. Results Of all cytosines tested for differential DNA methylation, 42% vary significantly in their methylation pattern throughout the life cycle. However, the differences are limited to few comparisons between specific stages of the life cycle and suggest four major epigenetic states specific to sporophytes, vegetative gametophytes, antherozoids, and archegonia. Further analyses indicated clear differences in the mechanisms underlying reprogramming in the gametophytic and sporophytic generations, which are paralleled by differences in the expression of genes involved in DNA methylation. Differentially methylated cytosines with a gain in methylation in antherozoids and archegonia are enriched in the CG and CHG contexts, as well as in gene bodies and gene flanking regions. In contrast, gain of DNA methylation during sporophyte development is mostly limited to the CHH context, LTR retrotransposons, DNA transposons, and repeats. Conclusion We conclude that epigenetic reprogramming occurs at least twice during the life cycle of M. polymorpha and that the underlying mechanisms are likely different between the two events.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); USDOE
Contributing Organization:
University of Zurich; Swiss National Science Foundation; European Research Council
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1618925
Alternate ID(s):
OSTI ID: 1626941
Journal Information:
Genome Biology (Online), Vol. 19, Issue 1; ISSN 1474-760X
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 42 works
Citation information provided by
Web of Science

References (96)

Active DNA Demethylation in Plant Companion Cells Reinforces Transposon Methylation in Gametes journal September 2012
Gene body DNA methylation in plants journal April 2017
Chromatin dynamics during plant sexual reproduction journal July 2014
DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation journal May 2015
Transgenerational epigenetic inheritance: how important is it? journal February 2013
Epigenetic Reprogramming in Plant Reproductive Lineages journal April 2012
Reprogramming of DNA Methylation in Pollen Guides Epigenetic Inheritance via Small RNA journal September 2012
Marchantia journal March 2016
Live-cell analysis of DNA methylation during sexual reproduction in Arabidopsis reveals context and sex-specific dynamics controlled by noncanonical RdDM journal January 2017
Evolutionary patterns of genic DNA methylation vary across land plants journal January 2016
On the origin and evolutionary consequences of gene body DNA methylation journal July 2016
Identification of Reference Genes for Real-Time Quantitative PCR Experiments in the Liverwort Marchantia polymorpha journal March 2015
Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation journal April 2010
The female gametophyte: an emerging model for cell type-specific systems biology in plant development journal November 2015
Epigenetic reprogramming in plant sexual reproduction journal July 2014
Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis journal December 2013
Marchantia polymorpha : Taxonomy, Phylogeny and Morphology of a Model System journal December 2015
Genome-Wide Demethylation of Arabidopsis Endosperm journal June 2009
Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene journal July 2001
Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system journal March 2007
Transgenerational epigenetic inheritance in plants journal August 2011
Requirement of CHROMOMETHYLASE3 for Maintenance of CpXpG Methylation journal May 2001
Unique cell-type-specific patterns of DNA methylation in the root meristem journal April 2016
Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications journal April 2011
ROS1, a Repressor of Transcriptional Gene Silencing in Arabidopsis, Encodes a DNA Glycosylase/Lyase journal December 2002
DNA methylation dynamics during early plant life journal September 2017
Walkabout on the long branches of plant evolution journal February 2013
Improved scoring of functional groups from gene expression data by decorrelating GO graph structure journal April 2006
Parent-of-Origin Effects on Gene Expression and DNA Methylation in the Maize Endosperm journal December 2011
Fast gapped-read alignment with Bowtie 2 journal March 2012
Epigenetic differences between shoots and roots in Arabidopsis reveals tissue-specific regulation journal October 2013
Natural CMT2 Variation Is Associated With Genome-Wide Methylation Changes and Temperature Seasonality journal December 2014
An evolutionary case for functional gene body methylation in plants and animals journal May 2017
The origin of a land flora, a theory based upon the facts of alternation book January 1908
Epigenetic Transitions in Germ Cell Development and Meiosis journal November 2010
DNA Methylation Dynamics during Sexual Reproduction in Arabidopsis thaliana journal October 2012
DNA demethylation is initiated in the central cells of Arabidopsis and rice journal December 2016
A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha journal May 2015
The deepest divergences in land plants inferred from phylogenomic evidence journal October 2006
Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis journal May 2011
Epigenetic reprogramming in the germline: towards the ground state of the epigenome journal August 2011
Molecular Genetic Tools and Techniques for Marchantia polymorpha Research journal June 2015
RNA-Seq Data Analysis Protocol: Combining In-House and Publicly Available Data book January 2017
Epigenetic regulation and reprogramming during gamete formation in plants journal April 2011
Plant Transgenerational Epigenetics journal November 2016
The DNA Glycosylase/Lyase ROS1 Functions in Pruning DNA Methylation Patterns in Arabidopsis journal January 2007
Transgenerational inheritance: Models and mechanisms of non-DNA sequence-based inheritance journal October 2016
The PpCMT chromomethylase affects cell growth and interacts with the homolog of LIKE HETEROCHROMATIN PROTEIN 1 in the moss Physcomitrella patens journal January 2014
Marchantia : Past, Present and Future journal February 2016
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome journal October 2017
Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality posted_content October 2014
Epigenetic regulation and reprogramming during gamete formation in plants text January 2011
Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes text January 2012
The origin of a land flora : a theory based upon the facts of alternation / journal January 1908
Generalized Linear Models journal December 2000
Chromatin dynamics during plant sexual reproduction text January 2014
The female gametophyte: an emerging model for cell type-specific systems biology in plant development text January 2015
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome text January 2017
Transgenerational epigenetic inheritance: how important is it? text January 2013
Data From: Extensive Epigenetic Reprogramming During The Life Cycle Of Marchantia Polymorpha dataset January 2017
Data From: Extensive Epigenetic Reprogramming During The Life Cycle Of Marchantia Polymorpha dataset January 2017
Transgenerational epigenetic inheritance in plants journal August 2011
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome journal October 2017
DNA Methylation Dynamics during Sexual Reproduction in Arabidopsis thaliana journal October 2012
Marchantia journal March 2016
Epigenetic regulation and reprogramming during gamete formation in plants journal April 2011
Walkabout on the long branches of plant evolution journal February 2013
Gene body DNA methylation in plants journal April 2017
Unique cell-type-specific patterns of DNA methylation in the root meristem journal April 2016
Epigenetic reprogramming in plant sexual reproduction journal July 2014
Partitioning RNAs by length improves transcriptome reconstruction from short-read RNA-seq data journal January 2022
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens journal March 2021
Inhalation exposure to cigarette smoke and inflammatory agents induces epigenetic changes in the lung journal July 2020
The deepest divergences in land plants inferred from phylogenomic evidence journal October 2006
On the origin and evolutionary consequences of gene body DNA methylation journal July 2016
DNA demethylation is initiated in the central cells of Arabidopsis and rice journal December 2016
Epigenetic Reprogramming in Plant Reproductive Lineages journal April 2012
Marchantia polymorpha : Taxonomy, Phylogeny and Morphology of a Model System journal December 2015
Marchantia : Past, Present and Future journal February 2016
Epigenetic reprogramming in the germline: towards the ground state of the epigenome journal August 2011
Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality posted_content October 2014
Live-cell analysis of DNA methylation during sexual reproduction in Arabidopsis reveals context and sex-specific dynamics controlled by noncanonical RdDM journal January 2017
Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene journal July 2001
Genome-Wide Demethylation of Arabidopsis Endosperm journal June 2009
Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation journal April 2010
Active DNA Demethylation in Plant Companion Cells Reinforces Transposon Methylation in Gametes journal September 2012
Transgenerational inheritance: Models and mechanisms of non-DNA sequence-based inheritance journal October 2016
Plant Transgenerational Epigenetics journal November 2016
An evolutionary case for functional gene body methylation in plants and animals journal May 2017
Transposon age and non-CG methylation text January 2020
Chromatin dynamics during plant sexual reproduction journal July 2014
The female gametophyte: an emerging model for cell type-specific systems biology in plant development journal November 2015
Epigenetic differences between shoots and roots in Arabidopsis reveals tissue-specific regulation journal October 2013
Epigenetics in the wild journal May 2015
Data From: Extensive Epigenetic Reprogramming During The Life Cycle Of Marchantia Polymorpha dataset January 2017
Extensive epigenetic reprogramming during the life cycle of Marchantia polymorpha collection January 2018

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A role of age-dependent DNA methylation reprogramming in regulating the regeneration capacity of Boea hygrometrica leaves journal August 2019
Contribution of epigenetic variation to adaptation in Arabidopsis journal October 2018
Building new insights in plant gametogenesis from an evolutionary perspective journal July 2019
Loss of CG methylation in Marchantia Polymorpha causes disorganization of cell division and reveals unique DNA methylation regulatory mechanisms of non-CG methylation posted_content July 2018
DNA methylation in Marchantia polymorpha journal April 2019
A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha journal December 2019
Genome-Wide Analysis of the MYB Transcription Factor Superfamily in Physcomitrella patens journal February 2020
RdDM-independent de novo and heterochromatin DNA methylation by plant CMT and DNMT3 orthologs journal April 2019
Characterization of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model posted_content August 2019
Chromatin organization in early land plants reveals an ancestral association between H3K27me3, transposons, and constitutive heterochromatin posted_content November 2019
Tissue-specific transposon-associated small RNAs in the gymnosperm tree, Norway spruce journal December 2019
Contribution of epigenetic variation to adaptation in Arabidopsis text January 2018
A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha text January 2020
Evidence for rapid evolution in a grassland biodiversity experiment text January 2019
Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin journal February 2020
Loss of CG methylation in Marchantia polymorpha causes disorganization of cell division and reveals unique DNA methylation regulatory mechanisms of non-CG methylation journal August 2018
Characterisation of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model journal April 2020
Contribution of epigenetic variation to adaptation in Arabidopsis text January 2018
A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha text January 2020
Contribution of epigenetic variation to adaptation in Arabidopsis journal October 2018
RdDM-independent de novo and heterochromatin DNA methylation by plant CMT and DNMT3 orthologs journal April 2019
DNA Methylation and the Evolution of Developmental Complexity in Plants journal October 2018
Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) journal September 2019


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