Epigenetic silencing of a multifunctional plant stress regulator

Zander, Mark; Willige, Björn C.; He, Yupeng; Nguyen, Thu A.; Langford, Amber E.; Nehring, Ramlah; Howell, Elizabeth; McGrath, Robert; Bartlett, Anna; Castanon, Rosa; Nery, Joseph R.; Chen, Huaming; Zhang, Zhuzhu; Jupe, Florian; Stepanova, Anna; Schmitz, Robert J.; Lewsey, Mathew G.; Chory, Joanne; Ecker, Joseph R.

doi:10.7554/eLife.47835

Title: Epigenetic silencing of a multifunctional plant stress regulator

Abstract

The central regulator of the ethylene (ET) signaling pathway, which controls a plethora of developmental programs and responses to environmental cues in plants, is ETHYLENE-INSENSITIVE2 (EIN2). Here we identify a chromatin-dependent regulatory mechanism at EIN2 requiring two genes: ETHYLENE-INSENSITIVE6 (EIN6), which is a H3K27me3 demethylase also known as RELATIVE OF EARLY FLOWERING6 (REF6), and EIN6 ENHANCER (EEN), the Arabidopsis homolog of the yeast INO80 chromatin remodeling complex subunit IES6 (INO EIGHTY SUBUNIT). Strikingly, EIN6 (REF6) and the INO80 complex redundantly control the level and the localization of the repressive histone modification H3K27me3 and the histone variant H2A.Z at the 5’ untranslated region (5’UTR) intron of EIN2. Concomitant loss of EIN6 (REF6) and the INO80 complex shifts the chromatin landscape at EIN2 to a repressive state causing a dramatic reduction of EIN2 expression. These results uncover a unique type of chromatin regulation which safeguards the expression of an essential multifunctional plant stress regulator.

Authors:

^[1];

^[2];

^[3]; Nguyen, Thu A. ^[2];

^[2]; Nehring, Ramlah ^[2]; Howell, Elizabeth ^[2];

^[4]; Bartlett, Anna ^[3]; Castanon, Rosa ^[3]; Nery, Joseph R. ^[3];

^[3]; Zhang, Zhuzhu ^[3];

^[3]; Stepanova, Anna ^[2];

^[2];

^[2]; Chory, Joanne ^[5];

^[1]

Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States, Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States
Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
Department of Biology, University of Pennsylvania, Philadelphia, United States
Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States, Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, United States

Publication Date:: 2019-08-16

Research Org.:: Salk Institute for Biological Studies, La Jolla, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC); National Institutes of Health (NIH)

OSTI Identifier:: 1560888

Alternate Identifier(s):: OSTI ID: 1560889; OSTI ID: 1609505

Grant/Contract Number:: FG02-04ER15517

Resource Type:: Published Article

Journal Name:: eLife

Additional Journal Information:: Journal Name: eLife Journal Volume: 8; Journal ID: ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Life Sciences & Biomedicine - Other Topics

Citation Formats


                    Zander, Mark, Willige, Björn C., He, Yupeng, Nguyen, Thu A., Langford, Amber E., Nehring, Ramlah, Howell, Elizabeth, McGrath, Robert, Bartlett, Anna, Castanon, Rosa, Nery, Joseph R., Chen, Huaming, Zhang, Zhuzhu, Jupe, Florian, Stepanova, Anna, Schmitz, Robert J., Lewsey, Mathew G., Chory, Joanne, and Ecker, Joseph R. Epigenetic silencing of a multifunctional plant stress regulator.  United States: N. p., 2019. 
Web.  doi:10.7554/eLife.47835.

Copy to clipboard


                    Zander, Mark, Willige, Björn C., He, Yupeng, Nguyen, Thu A., Langford, Amber E., Nehring, Ramlah, Howell, Elizabeth, McGrath, Robert, Bartlett, Anna, Castanon, Rosa, Nery, Joseph R., Chen, Huaming, Zhang, Zhuzhu, Jupe, Florian, Stepanova, Anna, Schmitz, Robert J., Lewsey, Mathew G., Chory, Joanne, & Ecker, Joseph R. Epigenetic silencing of a multifunctional plant stress regulator.  United States.  https://doi.org/10.7554/eLife.47835

Copy to clipboard


                    Zander, Mark, Willige, Björn C., He, Yupeng, Nguyen, Thu A., Langford, Amber E., Nehring, Ramlah, Howell, Elizabeth, McGrath, Robert, Bartlett, Anna, Castanon, Rosa, Nery, Joseph R., Chen, Huaming, Zhang, Zhuzhu, Jupe, Florian, Stepanova, Anna, Schmitz, Robert J., Lewsey, Mathew G., Chory, Joanne, and Ecker, Joseph R. Fri .  
"Epigenetic silencing of a multifunctional plant stress regulator".  United States.  https://doi.org/10.7554/eLife.47835.

Copy to clipboard


                    
@article{osti_1560888,

  title        = {Epigenetic silencing of a multifunctional plant stress regulator},

  author       = {Zander, Mark and Willige, Björn C. and He, Yupeng and Nguyen, Thu A. and Langford, Amber E. and Nehring, Ramlah and Howell, Elizabeth and McGrath, Robert and Bartlett, Anna and Castanon, Rosa and Nery, Joseph R. and Chen, Huaming and Zhang, Zhuzhu and Jupe, Florian and Stepanova, Anna and Schmitz, Robert J. and Lewsey, Mathew G. and Chory, Joanne and Ecker, Joseph R.},

  abstractNote = {The central regulator of the ethylene (ET) signaling pathway, which controls a plethora of developmental programs and responses to environmental cues in plants, is ETHYLENE-INSENSITIVE2 (EIN2). Here we identify a chromatin-dependent regulatory mechanism at EIN2 requiring two genes: ETHYLENE-INSENSITIVE6 (EIN6), which is a H3K27me3 demethylase also known as RELATIVE OF EARLY FLOWERING6 (REF6), and EIN6 ENHANCER (EEN), the Arabidopsis homolog of the yeast INO80 chromatin remodeling complex subunit IES6 (INO EIGHTY SUBUNIT). Strikingly, EIN6 (REF6) and the INO80 complex redundantly control the level and the localization of the repressive histone modification H3K27me3 and the histone variant H2A.Z at the 5’ untranslated region (5’UTR) intron of EIN2. Concomitant loss of EIN6 (REF6) and the INO80 complex shifts the chromatin landscape at EIN2 to a repressive state causing a dramatic reduction of EIN2 expression. These results uncover a unique type of chromatin regulation which safeguards the expression of an essential multifunctional plant stress regulator.},

  doi          = {10.7554/eLife.47835},

  journal      = {eLife},

  number       = ,

  volume       = 8,

  place        = {United States},

  year         = {2019},

  month        = {8}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Publisher's Version of Record
https://doi.org/10.7554/eLife.47835

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 22 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referenced in this record:

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, May 2016

O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang
Cell, Vol. 165, Issue 5
DOI: 10.1016/j.cell.2016.04.038

Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions
journal, July 2016

Kawakatsu, Taiji; Huang, Shao-shan Carol; Jupe, Florian
Cell, Vol. 166, Issue 2
DOI: 10.1016/j.cell.2016.06.044

THE ETHYLENE GAS SIGNAL TRANSDUCTION PATHWAY: A Molecular Perspective
journal, December 1998

Johnson, Phoebe R.; Ecker, Joseph R.
Annual Review of Genetics, Vol. 32, Issue 1
DOI: 10.1146/annurev.genet.32.1.227

EIN3-Dependent Regulation of Plant Ethylene Hormone Signaling by Two Arabidopsis F Box Proteins
journal, December 2003

Potuschak, Thomas; Lechner, Esther; Parmentier, Yves
Cell, Vol. 115, Issue 6, p. 679-689
DOI: 10.1016/S0092-8674(03)00968-1

Interactions between Abscisic Acid and Ethylene Signaling Cascades
journal, July 2000

Beaudoin, Nathalie; Serizet, Carine; Gosti, Françoise
The Plant Cell, Vol. 12, Issue 7
DOI: 10.1105/tpc.12.7.1103

MEME-ChIP: motif analysis of large DNA datasets
journal, April 2011

Machanick, Philip; Bailey, Timothy L.
Bioinformatics, Vol. 27, Issue 12
DOI: 10.1093/bioinformatics/btr189

Histone modifications and mitosis: countermarks, landmarks, and bookmarks
journal, April 2013

Wang, Fangwei; Higgins, Jonathan M. G.
Trends in Cell Biology, Vol. 23, Issue 4
DOI: 10.1016/j.tcb.2012.11.005

The complex architecture and epigenomic impact of plant T-DNA insertions
journal, January 2019

Jupe, Florian; Rivkin, Angeline C.; Michael, Todd P.
PLOS Genetics, Vol. 15, Issue 1
DOI: 10.1371/journal.pgen.1007819

Identification of Rice Ethylene-Response Mutants and Characterization of MHZ7/OsEIN2 in Distinct Ethylene Response and Yield Trait Regulation
journal, November 2013

Ma, Biao; He, Si-Jie; Duan, Kai-Xuan
Molecular Plant, Vol. 6, Issue 6
DOI: 10.1093/mp/sst087

STAR: ultrafast universal RNA-seq aligner
journal, October 2012

Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix
Bioinformatics, Vol. 29, Issue 1
DOI: 10.1093/bioinformatics/bts635

Clustal W and Clustal X version 2.0
journal, September 2007

Larkin, M. A.; Blackshields, G.; Brown, N. P.
Bioinformatics, Vol. 23, Issue 21, p. 2947-2948
DOI: 10.1093/bioinformatics/btm404

Relaying the Ethylene Signal: New Roles for EIN2
journal, January 2016

Zheng, Yuyu; Zhu, Ziqiang
Trends in Plant Science, Vol. 21, Issue 1
DOI: 10.1016/j.tplants.2015.11.013

Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus
journal, October 2012

Wen, Xing; Zhang, Cunli; Ji, Yusi
Cell Research, Vol. 22, Issue 11
DOI: 10.1038/cr.2012.145

Removal of H2A.Z by INO 80 promotes homologous recombination
journal, July 2015

Alatwi, Hanan E.; Downs, Jessica A.
EMBO reports, Vol. 16, Issue 8
DOI: 10.15252/embr.201540330

Divergent Roles of a Pair of Homologous Jumonji/Zinc-Finger–Class Transcription Factor Proteins in the Regulation of Arabidopsis Flowering Time
journal, September 2004

Noh, Bosl; Lee, Seung-Hee; Kim, Hyun-Jin
The Plant Cell, Vol. 16, Issue 10
DOI: 10.1105/tpc.104.025353

Aligning Short Sequencing Reads with Bowtie
journal, December 2010

Langmead, Ben
Current Protocols in Bioinformatics, Vol. 32, Issue 1
DOI: 10.1002/0471250953.bi1107s32

Processing and Subcellular Trafficking of ER-Tethered EIN2 Control Response to Ethylene Gas
journal, August 2012

Qiao, H.; Shen, Z.; Huang, S. -s. C.
Science, Vol. 338, Issue 6105
DOI: 10.1126/science.1225974

EIN2, a Bifunctional Transducer of Ethylene and Stress Responses in Arabidopsis
journal, June 1999

Alonso, J. M.
Science, Vol. 284, Issue 5423
DOI: 10.1126/science.284.5423.2148

A hydrophobic anchor mechanism defines a deacetylase family that suppresses host response against YopJ effectors
journal, December 2017

Bürger, Marco; Willige, Björn C.; Chory, Joanne
Nature Communications, Vol. 8, Issue 1
DOI: 10.1038/s41467-017-02347-w

Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells
journal, February 2011

Lister, Ryan; Pelizzola, Mattia; Kida, Yasuyuki S.
Nature, Vol. 471, Issue 7336
DOI: 10.1038/nature09798

Tyrosine Phosphorylation Regulates the Activity of Phytochrome Photoreceptors
journal, June 2013

Nito, Kazumasa; Wong, Catherine C. L.; Yates, John R.
Cell Reports, Vol. 3, Issue 6
DOI: 10.1016/j.celrep.2013.05.006

Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development
journal, January 2012

Smaczniak, C.; Immink, R. G. H.; Muino, J. M.
Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
DOI: 10.1073/pnas.1112871109

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression
journal, July 2014

Zander, Mark; Thurow, Corinna; Gatz, Christiane
Plant Physiology, Vol. 165, Issue 4
DOI: 10.1104/pp.114.243360

ANP32E is a histone chaperone that removes H2A.Z from chromatin
journal, January 2014

Obri, Arnaud; Ouararhni, Khalid; Papin, Christophe
Nature, Vol. 505, Issue 7485
DOI: 10.1038/nature12922

Arabidopsis REF6 is a histone H3 lysine 27 demethylase
journal, June 2011

Lu, Falong; Cui, Xia; Zhang, Shuaibin
Nature Genetics, Vol. 43, Issue 7
DOI: 10.1038/ng.854

Structural analyses of the chromatin remodelling enzymes INO80-C and SWR-C
journal, May 2015

Watanabe, Shinya; Tan, Dongyan; Lakshminarasimhan, Mahadevan
Nature Communications, Vol. 6, Issue 1
DOI: 10.1038/ncomms8108

deepTools: a flexible platform for exploring deep-sequencing data
journal, May 2014

Ramírez, Fidel; Dündar, Friederike; Diehl, Sarah
Nucleic Acids Research, Vol. 42, Issue W1
DOI: 10.1093/nar/gku365

Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis
journal, April 2016

Li, Chenlong; Gu, Lianfeng; Gao, Lei
Nature Genetics, Vol. 48, Issue 6
DOI: 10.1038/ng.3555

REF6 recognizes a specific DNA sequence to demethylate H3K27me3 and regulate organ boundary formation in Arabidopsis
journal, April 2016

Cui, Xia; Lu, Falong; Qiu, Qi
Nature Genetics, Vol. 48, Issue 6
DOI: 10.1038/ng.3556

The INO80 Protein Controls Homologous Recombination in Arabidopsis thaliana
journal, November 2004

Fritsch, Olivier; Benvenuto, Giovanna; Bowler, Chris
Molecular Cell, Vol. 16, Issue 3
DOI: 10.1016/j.molcel.2004.09.034

PIE1 , an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis
journal, June 2003

Noh, Yoo-Sun; Amasino, Richard M.
The Plant Cell, Vol. 15, Issue 7
DOI: 10.1105/tpc.012161

Human body epigenome maps reveal noncanonical DNA methylation variation
journal, June 2015

Schultz, Matthew D.; He, Yupeng; Whitaker, John W.
Nature, Vol. 523, Issue 7559
DOI: 10.1038/nature14465

H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis
journal, January 2010

Kumar, S. Vinod; Wigge, Philip A.
Cell, Vol. 140, Issue 1
DOI: 10.1016/j.cell.2009.11.006

EIN2 mediates direct regulation of histone acetylation in the ethylene response
journal, September 2017

Zhang, Fan; Wang, Likai; Qi, Bin
Proceedings of the National Academy of Sciences, Vol. 114, Issue 38
DOI: 10.1073/pnas.1707937114

Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis
journal, June 2013

Chang, Katherine Noelani; Zhong, Shan; Weirauch, Matthew T.
eLife, Vol. 2
DOI: 10.7554/eLife.00675

The Medicago truncatula ortholog of Arabidopsis EIN2, sickle , is a negative regulator of symbiotic and pathogenic microbial associations
journal, August 2008

Varma Penmetsa, R.; Uribe, Pedro; Anderson, Jonathan
The Plant Journal, Vol. 55, Issue 4
DOI: 10.1111/j.1365-313X.2008.03531.x

Structure and Subunit Topology of the INO80 Chromatin Remodeler and Its Nucleosome Complex
journal, September 2013

Tosi, Alessandro; Haas, Caroline; Herzog, Franz
Cell, Vol. 154, Issue 6
DOI: 10.1016/j.cell.2013.08.016

Arabidopsis actin-related protein ARP5 in multicellular development and DNA repair
journal, November 2009

Kandasamy, Muthugapatti K.; McKinney, Elizabeth C.; Deal, Roger B.
Developmental Biology, Vol. 335, Issue 1
DOI: 10.1016/j.ydbio.2009.08.006

The repressive role of Arabidopsis H2A.Z in transcriptional regulation depends on AtBMI1 activity
journal, June 2019

Gómez-Zambrano, Ángeles; Merini, Wiam; Calonje, Myriam
Nature Communications, Vol. 10, Issue 1
DOI: 10.1038/s41467-019-10773-1

Jmjd3 and UTX Play a Demethylase-Independent Role in Chromatin Remodeling to Regulate T-Box Family Member-Dependent Gene Expression
journal, November 2010

Miller, Sara A.; Mohn, Sarah E.; Weinmann, Amy S.
Molecular Cell, Vol. 40, Issue 4
DOI: 10.1016/j.molcel.2010.10.028

Exploiting the triple response of Arabidopsis to identify ethylene-related mutants.
journal, June 1990

Guzmán, P.; Ecker, J. R.
The Plant Cell, Vol. 2, Issue 6
DOI: 10.1105/tpc.2.6.513

Structural basis for ATP-dependent chromatin remodelling by the INO80 complex
journal, April 2018

Eustermann, Sebastian; Schall, Kevin; Kostrewa, Dirk
Nature, Vol. 556, Issue 7701
DOI: 10.1038/s41586-018-0029-y

The Pivotal Role of Ethylene in Plant Growth
journal, April 2018

Dubois, Marieke; Van den Broeck, Lisa; Inzé, Dirk
Trends in Plant Science, Vol. 23, Issue 4
DOI: 10.1016/j.tplants.2018.01.003

Conservation of ethylene as a plant hormone over 450 million years of evolution
journal, January 2015

Ju, Chuanli; Van de Poel, Bram; Cooper, Endymion D.
Nature Plants, Vol. 1, Issue 1
DOI: 10.1038/nplants.2014.4

EIN2-Directed Translational Regulation of Ethylene Signaling in Arabidopsis
journal, October 2015

Li, Wenyang; Ma, Mengdi; Feng, Ying
Cell, Vol. 163, Issue 3
DOI: 10.1016/j.cell.2015.09.037

Gene-Specific Translation Regulation Mediated by the Hormone-Signaling Molecule EIN2
journal, October 2015

Merchante, Catharina; Brumos, Javier; Yun, Jeonga
Cell, Vol. 163, Issue 3
DOI: 10.1016/j.cell.2015.09.036

Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP)
journal, February 2010

Kaufmann, Kerstin; Muiño, Jose M.; Østerås, Magne
Nature Protocols, Vol. 5, Issue 3
DOI: 10.1038/nprot.2009.244

Plant Responses to Ethylene Gas Are Mediated by SCF^EBF1/EBF2-Dependent Proteolysis of EIN3 Transcription Factor
journal, December 2003

Guo, Hongwei; Ecker, Joseph R
Cell, Vol. 115, Issue 6, p. 667-677
DOI: 10.1016/S0092-8674(03)00969-3

The Human Genome Browser at UCSC
journal, May 2002

Kent, W. J.; Sugnet, C. W.; Furey, T. S.
Genome Research, Vol. 12, Issue 6
DOI: 10.1101/gr.229102

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009

Robinson, M. D.; McCarthy, D. J.; Smyth, G. K.
Bioinformatics, Vol. 26, Issue 1
DOI: 10.1093/bioinformatics/btp616

The Chromatin Remodelers PKL and PIE1 Act in an Epigenetic Pathway That Determines H3K27me3 Homeostasis in Arabidopsis
journal, May 2018

Carter, Benjamin; Bishop, Brett; Ho, Kwok Ki
The Plant Cell, Vol. 30, Issue 6
DOI: 10.1105/tpc.17.00867

Multiple modes of regulation of the human Ino80 SNF2 ATPase by subunits of the INO80 chromatin-remodeling complex
journal, December 2013

Chen, L.; Conaway, R. C.; Conaway, J. W.
Proceedings of the National Academy of Sciences, Vol. 110, Issue 51
DOI: 10.1073/pnas.1317092110

Natural variation of H3K27me3 distribution between two Arabidopsis accessions and its association with flanking transposable elements
journal, January 2012

Dong, Xue; Reimer, Julia; Göbel, Ulrike
Genome Biology, Vol. 13, Issue 12
DOI: 10.1186/gb-2012-13-12-r117

Multi-layered Regulation of SPL15 and Cooperation with SOC1 Integrate Endogenous Flowering Pathways at the Arabidopsis Shoot Meristem
journal, May 2016

Hyun, Youbong; Richter, René; Vincent, Coral
Developmental Cell, Vol. 37, Issue 3
DOI: 10.1016/j.devcel.2016.04.001

Deposition of Histone Variant H2A.Z within Gene Bodies Regulates Responsive Genes
journal, October 2012

Coleman-Derr, Devin; Zilberman, Daniel
PLoS Genetics, Vol. 8, Issue 10
DOI: 10.1371/journal.pgen.1002988

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010

Quinlan, Aaron R.; Hall, Ira M.
Bioinformatics, Vol. 26, Issue 6
DOI: 10.1093/bioinformatics/btq033

DTASelect and Contrast: Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics
journal, February 2002

Tabb, David L.; McDonald, W. Hayes; Yates, John R.
Journal of Proteome Research, Vol. 1, Issue 1, p. 21-26
DOI: 10.1021/pr015504q

A clustering approach for identification of enriched domains from histone modification ChIP-Seq data
journal, June 2009

Zang, Chongzhi; Schones, Dustin E.; Zeng, Chen
Bioinformatics, Vol. 25, Issue 15
DOI: 10.1093/bioinformatics/btp340

SHOREmap: simultaneous mapping and mutation identification by deep sequencing
journal, August 2009

Schneeberger, Korbinian; Ossowski, Stephan; Lanz, Christa
Nature Methods, Vol. 6, Issue 8
DOI: 10.1038/nmeth0809-550

CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis
journal, November 2012

Ju, C.; Yoon, G. M.; Shemansky, J. M.
Proceedings of the National Academy of Sciences, Vol. 109, Issue 47
DOI: 10.1073/pnas.1214848109

Gibberellin Regulates PIN-FORMED Abundance and Is Required for Auxin Transport–Dependent Growth and Development in Arabidopsis thaliana
journal, June 2011

Willige, Björn C.; Isono, Erika; Richter, René
The Plant Cell, Vol. 23, Issue 6
DOI: 10.1105/tpc.111.086355

High Resolution Genome Wide Binding Event Finding and Motif Discovery Reveals Transcription Factor Spatial Binding Constraints
journal, August 2012

Guo, Yuchun; Mahony, Shaun; Gifford, David K.
PLoS Computational Biology, Vol. 8, Issue 8
DOI: 10.1371/journal.pcbi.1002638

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998

Clough, Steven J.; Bent, Andrew F.
The Plant Journal, Vol. 16, Issue 6, p. 735-743
DOI: 10.1046/j.1365-313x.1998.00343.x

Extracting Accurate Precursor Information for Tandem Mass Spectra by RawConverter
journal, October 2015

He, Lin; Diedrich, Jolene; Chu, Yen-Yin
Analytical Chemistry, Vol. 87, Issue 22
DOI: 10.1021/acs.analchem.5b02721

INO80 Facilitates Pluripotency Gene Activation in Embryonic Stem Cell Self-Renewal, Reprogramming, and Blastocyst Development
journal, May 2014

Wang, Li; Du, Ying; Ward, James M.
Cell Stem Cell, Vol. 14, Issue 5
DOI: 10.1016/j.stem.2014.02.013

Dual Role of the Histone Variant H2A.Z in Transcriptional Regulation of Stress-Response Genes
journal, March 2017

Sura, Weronika; Kabza, Michał; Karlowski, Wojciech M.
The Plant Cell, Vol. 29, Issue 4
DOI: 10.1105/tpc.16.00573

CEAS: cis-regulatory element annotation system
journal, August 2009

Shin, Hyunjin; Liu, Tao; Manrai, Arjun K.
Bioinformatics, Vol. 25, Issue 19
DOI: 10.1093/bioinformatics/btp479

The Histone Chaperones FACT and Spt6 Restrict H2A.Z from Intragenic Locations
journal, June 2015

Jeronimo, Célia; Watanabe, Shinya; Kaplan, Craig D.
Molecular Cell, Vol. 58, Issue 6
DOI: 10.1016/j.molcel.2015.03.030

RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011

Li, Bo; Dewey, Colin N.
BMC Bioinformatics, Vol. 12, Issue 1
DOI: 10.1186/1471-2105-12-323

The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development
journal, May 2015

Zhang, Chi; Cao, Lin; Rong, Liang
The Plant Journal, Vol. 82, Issue 4
DOI: 10.1111/tpj.12840

Global Regulation of H2A.Z Localization by the INO80 Chromatin-Remodeling Enzyme Is Essential for Genome Integrity
journal, January 2011

Papamichos-Chronakis, Manolis; Watanabe, Shinya; Rando, Oliver J.
Cell, Vol. 144, Issue 2
DOI: 10.1016/j.cell.2010.12.021

Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis
journal, May 2008

Lister, Ryan; O'Malley, Ronan C.; Tonti-Filippini, Julian
Cell, Vol. 133, Issue 3
DOI: 10.1016/j.cell.2008.03.029

The Sequence Alignment/Map format and SAMtools
journal, June 2009

Li, H.; Handsaker, B.; Wysoker, A.
Bioinformatics, Vol. 25, Issue 16
DOI: 10.1093/bioinformatics/btp352

ProLuCID: An improved SEQUEST-like algorithm with enhanced sensitivity and specificity
journal, November 2015

Xu, T.; Park, S. K.; Venable, J. D.
Journal of Proteomics, Vol. 129
DOI: 10.1016/j.jprot.2015.07.001

ATX1/AtCOMPASS and the H3K4me3 marks: how do they activate Arabidopsis genes?
journal, October 2014

Fromm, Michael; Avramova, Zoya
Current Opinion in Plant Biology, Vol. 21
DOI: 10.1016/j.pbi.2014.07.004

The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana
journal, May 2017

Wollmann, Heike; Stroud, Hume; Yelagandula, Ramesh
Genome Biology, Vol. 18, Issue 1
DOI: 10.1186/s13059-017-1221-3

Evaluation of Multidimensional Chromatography Coupled with Tandem Mass Spectrometry (LC/LC−MS/MS) for Large-Scale Protein Analysis: The Yeast Proteome
journal, February 2003

Peng, Junmin; Elias, Joshua E.; Thoreen, Carson C.
Journal of Proteome Research, Vol. 2, Issue 1
DOI: 10.1021/pr025556v

A transcription factor hierarchy defines an environmental stress response network
journal, November 2016

Song, L.; Huang, S. -s. C.; Wise, A.
Science, Vol. 354, Issue 6312
DOI: 10.1126/science.aag1550

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, September 2016

O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang
Cell, Vol. 166, Issue 6
DOI: 10.1016/j.cell.2016.08.063

Similar Records in DOE PAGES and OSTI.GOV collections:

Epigenetic Regulation of Hormone-dependent Plant Growth Processes

Technical Report Ecker, Joseph Robert

Impact of EIN6, EEN and ethylene on the H3K27me3 dynamics in Arabidopsis: To assess the dynamic responsiveness of H3K27me3 levels to ethylene and how this might affect ethylene-induced gene expression, we plan to perform H3K27me3 ChIP-seq and RNA- seq experiments in parallel with etiolated seedlings in the absence and presence of ethylene. Further implementation of ein6, een and ein6een mutants will visualize how the H3K27me3 landscape (-/+ET) is altered when H3K27me3 demethylation and/or INO80-mediated chromatin remodeling is compromised. Additional ChIP-seq analyses with EIN6 will show if ethylene- induced H3K27me3 removal at certain genes is always accompanied by the presence ofmore » EIN6.« less
https://doi.org/10.2172/1332760

Full Text Available
Down-regulated lncRNA MEG3 promotes osteogenic differentiation of human dental follicle stem cells by epigenetically regulating Wnt pathway

Journal Article Deng, Lidi ; Hong, Hong ; Zhang, Xueqin ; ... - Biochemical and Biophysical Research Communications

Our previous long noncoding RNA (lncRNA) microarray results showed that lncRNA MEG3 (maternally expressed 3) was significantly downregulated in human dental follicle cells than human periodontal ligament cells. Latest studies show that MEG3 contributes to polycomb repressive complex 2 (PRC2) recruitment to silence gene expression. The enhancer of zeste homolog 2 (EZH2), a crucial catalytic subunit of PRC2, mediates gene silencing and participates in cell lineage determination via methyltransferase activity. In this study, we found that the expression of EZH2 and H3K27me3 (trimethylation on lysine 27 in histone H3) decreased during osteogenesis of human dental follicle stem cells (hDFSCs). Knockdownmore »« less
https://doi.org/10.1016/J.BBRC.2018.07.160
Astronauts Plasma-Derived Exosomes Induced Aberrant EZH2-Mediated H3K27me3 Epigenetic Regulation of the Vitamin D Receptor

Journal Article Bisserier, Malik ; Brojakowska, Agnieszka ; Saffran, Nathaniel ; ... - Frontiers in cardiovascular medicine

There are unique stressors in the spaceflight environment. Exposure to such stressors may be associated with adverse effects on astronauts' health, including increased cancer and cardiovascular disease risks. Small extracellular vesicles (sEVs, i.e., exosomes) play a vital role in intercellular communication and regulate various biological processes contributing to their role in disease pathogenesis. To assess whether spaceflight alters sEVs transcriptome profile, sEVs were isolated from the blood plasma of 3 astronauts at two different time points: 10 days before launch (L-10) and 3 days after return (R+3) from the Shuttle mission. AC16 cells (human cardiomyocyte cell line) were treated withmore »« less
https://doi.org/10.3389/fcvm.2022.855181

Full Text Available
Exposure to coplanar PCBs induces endothelial cell inflammation through epigenetic regulation of NF-κB subunit p65

Journal Article Liu, Dandan ; Perkins, Jordan T. ; Department of Animal and Food Sciences, College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY 40536 ; ... - Toxicology and Applied Pharmacology

Epigenetic modifications of DNA and histones alter cellular phenotypes without changing genetic codes. Alterations of epigenetic marks can be induced by exposure to environmental pollutants and may contribute to associated disease risks. Here we test the hypothesis that endothelial cell dysfunction induced by exposure to polychlorinated biphenyls (PCBs) is mediated in part though histone modifications. In this study, human vascular endothelial cells were exposed to physiologically relevant concentrations of several PCBs congeners (e.g., PCBs 77, 118, 126 and 153) followed by quantification of inflammatory gene expression and changes of histone methylation. Only exposure to coplanar PCBs 77 and 126 inducedmore »« less
https://doi.org/10.1016/J.TAAP.2015.10.015
Altered epigenetic regulation of homeobox genes in human oral squamous cell carcinoma cells

Journal Article Marcinkiewicz, Katarzyna M. ; Gudas, Lorraine J., E-mail: ljgudas@med.cornell.edu - Experimental Cell Research

To gain insight into oral squamous cell carcinogenesis, we performed deep sequencing (RNAseq) of non-tumorigenic human OKF6-TERT1R and tumorigenic SCC-9 cells. Numerous homeobox genes are differentially expressed between OKF6-TERT1R and SCC-9 cells. Data from Oncomine, a cancer microarray database, also show that homeobox (HOX) genes are dysregulated in oral SCC patients. The activity of Polycomb repressive complexes (PRC), which causes epigenetic modifications, and retinoic acid (RA) signaling can control HOX gene transcription. HOXB7, HOXC10, HOXC13, and HOXD8 transcripts are higher in SCC-9 than in OKF6-TERT1R cells; using ChIP (chromatin immunoprecipitation) we detected PRC2 protein SUZ12 and the epigenetic H3K27me3 markmore »« less
https://doi.org/10.1016/J.YEXCR.2013.09.011

Similar Records

Title: Epigenetic silencing of a multifunctional plant stress regulator

Abstract

Citation Formats

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape journal, May 2016

Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions journal, July 2016

THE ETHYLENE GAS SIGNAL TRANSDUCTION PATHWAY: A Molecular Perspective journal, December 1998

EIN3-Dependent Regulation of Plant Ethylene Hormone Signaling by Two Arabidopsis F Box Proteins journal, December 2003

Interactions between Abscisic Acid and Ethylene Signaling Cascades journal, July 2000

MEME-ChIP: motif analysis of large DNA datasets journal, April 2011

Histone modifications and mitosis: countermarks, landmarks, and bookmarks journal, April 2013

The complex architecture and epigenomic impact of plant T-DNA insertions journal, January 2019

Identification of Rice Ethylene-Response Mutants and Characterization of MHZ7/OsEIN2 in Distinct Ethylene Response and Yield Trait Regulation journal, November 2013

STAR: ultrafast universal RNA-seq aligner journal, October 2012

Clustal W and Clustal X version 2.0 journal, September 2007

Relaying the Ethylene Signal: New Roles for EIN2 journal, January 2016

Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus journal, October 2012

Removal of H2A.Z by INO 80 promotes homologous recombination journal, July 2015

Divergent Roles of a Pair of Homologous Jumonji/Zinc-Finger–Class Transcription Factor Proteins in the Regulation of Arabidopsis Flowering Time journal, September 2004

Aligning Short Sequencing Reads with Bowtie journal, December 2010

Processing and Subcellular Trafficking of ER-Tethered EIN2 Control Response to Ethylene Gas journal, August 2012

EIN2, a Bifunctional Transducer of Ethylene and Stress Responses in Arabidopsis journal, June 1999

A hydrophobic anchor mechanism defines a deacetylase family that suppresses host response against YopJ effectors journal, December 2017

Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells journal, February 2011

Tyrosine Phosphorylation Regulates the Activity of Phytochrome Photoreceptors journal, June 2013

Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development journal, January 2012

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression journal, July 2014

ANP32E is a histone chaperone that removes H2A.Z from chromatin journal, January 2014

Arabidopsis REF6 is a histone H3 lysine 27 demethylase journal, June 2011

Structural analyses of the chromatin remodelling enzymes INO80-C and SWR-C journal, May 2015

deepTools: a flexible platform for exploring deep-sequencing data journal, May 2014

Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis journal, April 2016

REF6 recognizes a specific DNA sequence to demethylate H3K27me3 and regulate organ boundary formation in Arabidopsis journal, April 2016

The INO80 Protein Controls Homologous Recombination in Arabidopsis thaliana journal, November 2004

PIE1 , an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis journal, June 2003

Human body epigenome maps reveal noncanonical DNA methylation variation journal, June 2015

H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis journal, January 2010

EIN2 mediates direct regulation of histone acetylation in the ethylene response journal, September 2017

Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis journal, June 2013

The Medicago truncatula ortholog of Arabidopsis EIN2, sickle , is a negative regulator of symbiotic and pathogenic microbial associations journal, August 2008

Structure and Subunit Topology of the INO80 Chromatin Remodeler and Its Nucleosome Complex journal, September 2013

Arabidopsis actin-related protein ARP5 in multicellular development and DNA repair journal, November 2009

The repressive role of Arabidopsis H2A.Z in transcriptional regulation depends on AtBMI1 activity journal, June 2019

Jmjd3 and UTX Play a Demethylase-Independent Role in Chromatin Remodeling to Regulate T-Box Family Member-Dependent Gene Expression journal, November 2010

Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. journal, June 1990

Structural basis for ATP-dependent chromatin remodelling by the INO80 complex journal, April 2018

The Pivotal Role of Ethylene in Plant Growth journal, April 2018

Conservation of ethylene as a plant hormone over 450 million years of evolution journal, January 2015

EIN2-Directed Translational Regulation of Ethylene Signaling in Arabidopsis journal, October 2015

Gene-Specific Translation Regulation Mediated by the Hormone-Signaling Molecule EIN2 journal, October 2015

Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP) journal, February 2010

Plant Responses to Ethylene Gas Are Mediated by SCFEBF1/EBF2-Dependent Proteolysis of EIN3 Transcription Factor journal, December 2003

The Human Genome Browser at UCSC journal, May 2002

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal, November 2009

The Chromatin Remodelers PKL and PIE1 Act in an Epigenetic Pathway That Determines H3K27me3 Homeostasis in Arabidopsis journal, May 2018

Multiple modes of regulation of the human Ino80 SNF2 ATPase by subunits of the INO80 chromatin-remodeling complex journal, December 2013

Natural variation of H3K27me3 distribution between two Arabidopsis accessions and its association with flanking transposable elements journal, January 2012

Multi-layered Regulation of SPL15 and Cooperation with SOC1 Integrate Endogenous Flowering Pathways at the Arabidopsis Shoot Meristem journal, May 2016

Deposition of Histone Variant H2A.Z within Gene Bodies Regulates Responsive Genes journal, October 2012

BEDTools: a flexible suite of utilities for comparing genomic features journal, January 2010

DTASelect and Contrast: Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics journal, February 2002

A clustering approach for identification of enriched domains from histone modification ChIP-Seq data journal, June 2009

SHOREmap: simultaneous mapping and mutation identification by deep sequencing journal, August 2009

CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis journal, November 2012

Gibberellin Regulates PIN-FORMED Abundance and Is Required for Auxin Transport–Dependent Growth and Development in Arabidopsis thaliana journal, June 2011

High Resolution Genome Wide Binding Event Finding and Motif Discovery Reveals Transcription Factor Spatial Binding Constraints journal, August 2012

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal, December 1998

Extracting Accurate Precursor Information for Tandem Mass Spectra by RawConverter journal, October 2015

INO80 Facilitates Pluripotency Gene Activation in Embryonic Stem Cell Self-Renewal, Reprogramming, and Blastocyst Development journal, May 2014

Dual Role of the Histone Variant H2A.Z in Transcriptional Regulation of Stress-Response Genes journal, March 2017

CEAS: cis-regulatory element annotation system journal, August 2009

The Histone Chaperones FACT and Spt6 Restrict H2A.Z from Intragenic Locations journal, June 2015

RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome journal, August 2011

The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development journal, May 2015

Global Regulation of H2A.Z Localization by the INO80 Chromatin-Remodeling Enzyme Is Essential for Genome Integrity journal, January 2011

Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis journal, May 2008

The Sequence Alignment/Map format and SAMtools journal, June 2009

ProLuCID: An improved SEQUEST-like algorithm with enhanced sensitivity and specificity journal, November 2015

ATX1/AtCOMPASS and the H3K4me3 marks: how do they activate Arabidopsis genes? journal, October 2014

The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana journal, May 2017

Evaluation of Multidimensional Chromatography Coupled with Tandem Mass Spectrometry (LC/LC−MS/MS) for Large-Scale Protein Analysis: The Yeast Proteome journal, February 2003

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, May 2016

Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions
journal, July 2016

THE ETHYLENE GAS SIGNAL TRANSDUCTION PATHWAY: A Molecular Perspective
journal, December 1998

EIN3-Dependent Regulation of Plant Ethylene Hormone Signaling by Two Arabidopsis F Box Proteins
journal, December 2003

Interactions between Abscisic Acid and Ethylene Signaling Cascades
journal, July 2000

MEME-ChIP: motif analysis of large DNA datasets
journal, April 2011

Histone modifications and mitosis: countermarks, landmarks, and bookmarks
journal, April 2013

The complex architecture and epigenomic impact of plant T-DNA insertions
journal, January 2019

Identification of Rice Ethylene-Response Mutants and Characterization of MHZ7/OsEIN2 in Distinct Ethylene Response and Yield Trait Regulation
journal, November 2013

STAR: ultrafast universal RNA-seq aligner
journal, October 2012

Clustal W and Clustal X version 2.0
journal, September 2007

Relaying the Ethylene Signal: New Roles for EIN2
journal, January 2016

Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus
journal, October 2012

Removal of H2A.Z by INO 80 promotes homologous recombination
journal, July 2015

Divergent Roles of a Pair of Homologous Jumonji/Zinc-Finger–Class Transcription Factor Proteins in the Regulation of Arabidopsis Flowering Time
journal, September 2004

Aligning Short Sequencing Reads with Bowtie
journal, December 2010

Processing and Subcellular Trafficking of ER-Tethered EIN2 Control Response to Ethylene Gas
journal, August 2012

EIN2, a Bifunctional Transducer of Ethylene and Stress Responses in Arabidopsis
journal, June 1999

A hydrophobic anchor mechanism defines a deacetylase family that suppresses host response against YopJ effectors
journal, December 2017

Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells
journal, February 2011

Tyrosine Phosphorylation Regulates the Activity of Phytochrome Photoreceptors
journal, June 2013

Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development
journal, January 2012

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression
journal, July 2014

ANP32E is a histone chaperone that removes H2A.Z from chromatin
journal, January 2014

Arabidopsis REF6 is a histone H3 lysine 27 demethylase
journal, June 2011

Structural analyses of the chromatin remodelling enzymes INO80-C and SWR-C
journal, May 2015

deepTools: a flexible platform for exploring deep-sequencing data
journal, May 2014

Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis
journal, April 2016

REF6 recognizes a specific DNA sequence to demethylate H3K27me3 and regulate organ boundary formation in Arabidopsis
journal, April 2016

The INO80 Protein Controls Homologous Recombination in Arabidopsis thaliana
journal, November 2004

PIE1 , an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis
journal, June 2003

Human body epigenome maps reveal noncanonical DNA methylation variation
journal, June 2015

H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis
journal, January 2010

EIN2 mediates direct regulation of histone acetylation in the ethylene response
journal, September 2017

Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis
journal, June 2013

The Medicago truncatula ortholog of Arabidopsis EIN2, sickle , is a negative regulator of symbiotic and pathogenic microbial associations
journal, August 2008

Structure and Subunit Topology of the INO80 Chromatin Remodeler and Its Nucleosome Complex
journal, September 2013

Arabidopsis actin-related protein ARP5 in multicellular development and DNA repair
journal, November 2009

The repressive role of Arabidopsis H2A.Z in transcriptional regulation depends on AtBMI1 activity
journal, June 2019

Jmjd3 and UTX Play a Demethylase-Independent Role in Chromatin Remodeling to Regulate T-Box Family Member-Dependent Gene Expression
journal, November 2010

Exploiting the triple response of Arabidopsis to identify ethylene-related mutants.
journal, June 1990

Structural basis for ATP-dependent chromatin remodelling by the INO80 complex
journal, April 2018

The Pivotal Role of Ethylene in Plant Growth
journal, April 2018

Conservation of ethylene as a plant hormone over 450 million years of evolution
journal, January 2015

EIN2-Directed Translational Regulation of Ethylene Signaling in Arabidopsis
journal, October 2015

Gene-Specific Translation Regulation Mediated by the Hormone-Signaling Molecule EIN2
journal, October 2015

Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP)
journal, February 2010

Plant Responses to Ethylene Gas Are Mediated by SCF^EBF1/EBF2-Dependent Proteolysis of EIN3 Transcription Factor
journal, December 2003

The Human Genome Browser at UCSC
journal, May 2002

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009

The Chromatin Remodelers PKL and PIE1 Act in an Epigenetic Pathway That Determines H3K27me3 Homeostasis in Arabidopsis
journal, May 2018

Multiple modes of regulation of the human Ino80 SNF2 ATPase by subunits of the INO80 chromatin-remodeling complex
journal, December 2013

Natural variation of H3K27me3 distribution between two Arabidopsis accessions and its association with flanking transposable elements
journal, January 2012

Multi-layered Regulation of SPL15 and Cooperation with SOC1 Integrate Endogenous Flowering Pathways at the Arabidopsis Shoot Meristem
journal, May 2016

Deposition of Histone Variant H2A.Z within Gene Bodies Regulates Responsive Genes
journal, October 2012

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010

DTASelect and Contrast: Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics
journal, February 2002

A clustering approach for identification of enriched domains from histone modification ChIP-Seq data
journal, June 2009

SHOREmap: simultaneous mapping and mutation identification by deep sequencing
journal, August 2009

CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis
journal, November 2012

Gibberellin Regulates PIN-FORMED Abundance and Is Required for Auxin Transport–Dependent Growth and Development in Arabidopsis thaliana
journal, June 2011

High Resolution Genome Wide Binding Event Finding and Motif Discovery Reveals Transcription Factor Spatial Binding Constraints
journal, August 2012

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998

Extracting Accurate Precursor Information for Tandem Mass Spectra by RawConverter
journal, October 2015

INO80 Facilitates Pluripotency Gene Activation in Embryonic Stem Cell Self-Renewal, Reprogramming, and Blastocyst Development
journal, May 2014

Dual Role of the Histone Variant H2A.Z in Transcriptional Regulation of Stress-Response Genes
journal, March 2017

CEAS: cis-regulatory element annotation system
journal, August 2009

The Histone Chaperones FACT and Spt6 Restrict H2A.Z from Intragenic Locations
journal, June 2015

RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011

The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development
journal, May 2015

Global Regulation of H2A.Z Localization by the INO80 Chromatin-Remodeling Enzyme Is Essential for Genome Integrity
journal, January 2011

Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis
journal, May 2008

The Sequence Alignment/Map format and SAMtools
journal, June 2009

ProLuCID: An improved SEQUEST-like algorithm with enhanced sensitivity and specificity
journal, November 2015

ATX1/AtCOMPASS and the H3K4me3 marks: how do they activate Arabidopsis genes?
journal, October 2014

The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana
journal, May 2017

Evaluation of Multidimensional Chromatography Coupled with Tandem Mass Spectrometry (LC/LC−MS/MS) for Large-Scale Protein Analysis: The Yeast Proteome
journal, February 2003

A transcription factor hierarchy defines an environmental stress response network
journal, November 2016

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, September 2016