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

Title: The landscape of Chlamydomonas histone H3 lysine 4 methylation reveals both constant features and dynamic changes during the diurnal cycle

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.15948· OSTI ID:1893123
ORCiD logo [1];  [2];  [3];  [3];  [2];  [3]; ORCiD logo [4];  [5]
  1. Univ. of California, Berkeley, CA (United States)
  2. Univ. of California, Los Angeles, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). DOE Joint Genome Institute
  4. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Division of Environmental Genomics and Systems Biology
  5. Donald Danforth Plant Science Center, St. Louis, MO (United States)

SUMMARY Chromatin modifications are epigenetic regulatory features with major roles in various cellular events, yet they remain understudied in algae. We interrogated the genome‐wide distribution pattern of mono‐ and trimethylated histone H3 lysine 4 (H3K4) using chromatin‐immunoprecipitation followed by deep‐sequencing (ChIP‐seq) during key phases of the Chlamydomonas cell cycle: early G 1 phase, Zeitgeber Time 1 (ZT1), when cells initiate biomass accumulation, S/M phase (ZT13) when cells are replicating DNA and undergoing mitosis, and late G 0 phase (ZT23) when they are quiescent. Tri‐methylated H3K4 was predominantly enriched at transcription start sites of the majority of protein coding genes (85%). The likelihood of a gene being marked by H3K4me3 correlated with it being transcribed at some point during the life cycle but not necessarily by continuous active transcription, as exemplified by early zygotic genes, which may remain transcriptionally dormant for thousands of generations between sexual cycles. The exceptions to this rule were around 120 loci, some of which encode non‐poly‐adenylated transcripts, such as small nuclear RNAs and replication‐dependent histones that had H3K4me3 peaks only when they were being transcribed. Mono‐methylated H3K4 was the default state for the vast majority of histones that were bound outside of transcription start sites and terminator regions of genes. A small fraction of the genome that was depleted of any H3 lysine 4 methylation was enriched for DNA cytosine methylation and the genes within these DNA methylation islands were poorly expressed. Besides marking protein coding genes, H3K4me3 ChIP‐seq data served also as a annotation tool for validation of hundreds of long non‐coding RNA genes.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); USDOE Laboratory Directed Research and Development (LDRD) Program; National Institutes of Health (NIH); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231; FC02-02ER63421; R01GM126557; MCB 1515220; DE‐AC02‐05CH11231; DE‐FC02‐02ER63421
OSTI ID:
1893123
Alternate ID(s):
OSTI ID: 1888071
Journal Information:
The Plant Journal, Vol. 112, Issue 2; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (79)

Structure and dynamic behavior of nucleosomes journal April 2003
Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences journal December 2002
Alteration of Nucleosome Structure as a Mechanism of Transcriptional Regulation journal June 1998
Model-based Analysis of ChIP-Seq (MACS) journal January 2008
Genome-wide Map of Nucleosome Acetylation and Methylation in Yeast journal August 2005
The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4 journal December 2001
Single-Nucleosome Mapping of Histone Modifications in S. cerevisiae journal August 2005
Molecular coupling of DNA methylation and histone methylation journal October 2010
COMPASS: A complex of proteins associated with a trithorax-related SET domain protein journal October 2001
Chlamydomonas U2, U4 and U6 snRNAs. An evolutionary conserved putative third interaction between U4 and U6 snRNAs which has a counterpart in the U4atac−U6atac snRNA duplex journal July 1997
Genome-wide long non-coding RNA screening, identification and characterization in a model microorganism Chlamydomonas reinhardtii journal September 2016
Characterization of Chlamydomonas reinhardtii Core Histones by Top-Down Mass Spectrometry Reveals Unique Algae-Specific Variants and Post-Translational Modifications journal November 2017
Genomic Maps and Comparative Analysis of Histone Modifications in Human and Mouse journal January 2005
Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates journal May 2013
An Improved Top-Down Mass Spectrometry Characterization of Chlamydomonas reinhardtii Histones and Their Post-translational Modifications journal June 2021
The organization structure and regulatory elements of Chlamydomonas histone genes reveal features linking plant and animal genes journal September 1995
Dynamic changes in the human methylome during differentiation journal February 2010
Spatial Distribution of Di- and Tri-methyl Lysine 36 of Histone H3 at Active Genes journal May 2005
The uni chromosome ofChlamydomonas: histone genes and nucleosome structure journal January 1995
Epigenetic balance of gene expression by Polycomb and COMPASS families journal June 2016
H3K4me1 Distribution Predicts Transcription State and Poising at Promoters journal May 2020
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
High-Resolution Profiling of Histone Methylations in the Human Genome journal May 2007
Histone H3 lysine 4 methylation patterns in higher eukaryotic genes journal December 2003
Interactions between core histone marks and DNA methyltransferases predict DNA methylation patterns observed in human cells and tissues journal September 2019
Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome journal February 2007
Histones of Chlamydomonas reinhardtii (Synthesis, Acetylation, and Methylation) journal October 1995
Crystal structure of the nucleosome core particle at 2.8 Å resolution journal September 1997
Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism journal April 2014
Comparative study of DNA methylation in three unicellular eucaryotes. journal January 1978
Lineage-specific chromatin signatures reveal a regulator of lipid metabolism in microalgae journal July 2015
Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana journal January 2009
Physical Association and Coordinate Function of the H3 K4 Methyltransferase MLL1 and the H4 K16 Acetyltransferase MOF journal June 2005
Nucleotide sequence of U5 RNA from a green alga,Chiamydomonas reinhrdtii journal January 1992
Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress journal November 2012
Genome-scale DNA methylation maps of pluripotent and differentiated cells journal July 2008
Co-expression networks in Chlamydomonas reveal significant rhythmicity in batch cultures and empower gene function discovery journal February 2021
BLAT---The BLAST-Like Alignment Tool journal March 2002
The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote journal June 2004
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions journal October 2007
Genome-Wide and Organ-Specific Landscapes of Epigenetic Modifications and Their Relationships to mRNA and Small RNA Transcriptomes in Maize journal April 2009
Active genes are tri-methylated at K4 of histone H3 journal September 2002
Gene Regulatory Networks for the Haploid-to-Diploid Transition of Chlamydomonas reinhardtii journal July 2017
Protocol: methodology for chromatin immunoprecipitation (ChIP) in Chlamydomonas reinhardtii journal January 2011
deepTools2: a next generation web server for deep-sequencing data analysis journal April 2016
Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail journal November 2008
Dynamic Changes in Genome-Wide Histone H3 Lysine 4 Methylation Patterns in Response to Dehydration Stress in Arabidopsis thaliana journal January 2010
Menin Associates with a Trithorax Family Histone Methyltransferase Complex and with the Hoxc8 Locus journal February 2004
Organization and transcription of Volvox histone-encoding genes: similarities between algal and animal genes journal January 1990
An epigenetic gene silencing pathway selectively acting on transgenic DNA in the green alga Chlamydomonas journal December 2020
RNA-Seq Analysis of Sulfur-Deprived Chlamydomonas Cells Reveals Aspects of Acclimation Critical for Cell Survival journal June 2010
Set2 Is a Nucleosomal Histone H3-Selective Methyltransferase That Mediates Transcriptional Repression journal March 2002
Long non-coding RNAs: insights into functions journal March 2009
Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals journal February 2009
BEDTools: a flexible suite of utilities for comparing genomic features journal January 2010
A Chromatin Landmark and Transcription Initiation at Most Promoters in Human Cells journal July 2007
Histone methylation marks play important roles in predicting the methylation status of CpG islands journal September 2008
Coordinated Chromatin Control: Structural and Functional Linkage of DNA and Histone Methylation journal March 2010
Regulation of chromatin by histone modifications journal February 2011
Expression switching in thestevorandPfmc-2TMsuperfamilies inPlasmodium falciparum journal May 2007
Genome-wide positioning of bivalent mononucleosomes journal September 2016
Systems and Trans -System Level Analysis Identifies Conserved Iron Deficiency Responses in the Plant Lineage journal October 2012
Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX–DNMT3–DNMT3L domain journal September 2009
Coordinated regulation of cellular identity–associated H3K4me3 breadth by the COMPASS family journal June 2020
Monomethyl Histone H3 Lysine 4 as an Epigenetic Mark for Silenced Euchromatin in Chlamydomonas journal August 2005
Global Epigenetic and Transcriptional Trends among Two Rice Subspecies and Their Reciprocal Hybrids journal January 2010
Long intronic noncoding RNA transcription: Expression noise or expression choice? journal April 2009
Methylation of histone H3 Lys 4 in coding regions of active genes journal June 2002
Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps journal April 2011
Targeted Recruitment of Set1 Histone Methylase by Elongating Pol II Provides a Localized Mark and Memory of Recent Transcriptional Activity journal March 2003
Heat shock factor 1 counteracts epigenetic silencing of nuclear transgenes in Chlamydomonas reinhardtii journal April 2013
The language of covalent histone modifications journal January 2000
Predictive chromatin signatures in the mammalian genome journal October 2009
Generation of Chlamydomonas strains that efficiently express nuclear transgenes journal March 2009
Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II‐mediated transcription initiation journal January 2007
Tri-methylation of histone H3 lysine 4 facilitates gene expression in ageing cells journal October 2018
Genic and Global Functions for Paf1C in Chromatin Modification and Gene Expression in Arabidopsis journal August 2008
Multiomics resolution of molecular events during a day in the life of Chlamydomonas journal January 2019
A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3 journal December 2001