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

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:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [2]; ORCiD logo [2];  [2];  [2]; ORCiD logo [4];  [3];  [3];  [3]; ORCiD logo [3];  [3]; ORCiD logo [3];  [2]; ORCiD logo [2]; ORCiD logo [2];  [5]; ORCiD logo [1]
  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
  2. Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
  3. Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States
  4. Department of Biology, University of Pennsylvania, Philadelphia, United States
  5. 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:
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. https://doi.org/10.7554/eLife.47835.
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
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.
@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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.7554/eLife.47835

Save / Share:

Works referenced in this record:

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

  • 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


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


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


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

  • 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


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


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


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


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

  • 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


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

  • 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


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

  • 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 SCFEBF1/EBF2-Dependent Proteolysis of EIN3 Transcription Factor
journal, December 2003


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


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


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

  • 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


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


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


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


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

  • 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


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

  • 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


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