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Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation

Hilde Nelissen UGent, Steven De Groeve UGent, Delphine Fleury, Pia Neyt UGent, Leonardo Bruno, Maria Beatrice Bitonti, Filip Vandenbussche UGent, Dominique Van Der Straeten UGent, Takahiro Yamaguchi and Hirokazu Tsukaya, et al. (2010) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 107(4). p.1678-1683
abstract
In eukaryotes, transcription of protein-encoding genes is strongly regulated by posttranslational modifications of histones that affect the accessibility of the DNA by RNA polymerase II (RNAPII). The Elongator complex was originally identified in yeast as a histone acetyltransferase (HAT) complex that activates RNAPII-mediated transcription. In Arabidopsis thaliana, the Elongator mutants elo1, elo2, and elo3 with decreased leaf and primary root growth due to reduced cell proliferation identified homologs of components of the yeast Elongator complex, Elp4, Elp1, and Elp3, respectively. Here we show that the Elongator complex was purified from plant cell cultures as a six-component complex. The role of plant Elongator in transcription elongation was supported by colocalization of the HAT enzyme, ELO3, with euchromatin and the phosphorylated form of RNAPII, and reduced histone H3 lysine 14 acetylation at the coding region of the SHORT HYPOCOTYL 2 auxin repressor and the LAX2 auxin influx carrier gene with reduced expression levels in the elo3 mutant. Additional auxin-related genes were down-regulated in the transcriptome of elo mutants but not targeted by the Elongator HAT activity showing specificity in target gene selection. Biological relevance was apparent by auxin-related phenotypes and marker gene analysis. Ethylene and jasmonic acid signaling and abiotic stress responses were up-regulated in the elo transcriptome and might contribute to the pleiotropic elo phenotype. Thus, although the structure of Elongator and its substrate are conserved, target gene selection has diverged, showing that auxin signaling and influx are under chromatin control.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
BOX PROTEIN TIR1, CELLS, TANDEM AFFINITY PURIFICATION, HOLO-ELONGATOR, ORGAN GROWTH, ABSCISIC-ACID, ARABIDOPSIS-THALIANA, COMPLEX, TRANSPORT, EXPRESSION
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. U. S. A.
volume
107
issue
4
pages
6 pages
publisher
NATL ACAD SCIENCES
place of publication
WASHINGTON
Web of Science type
Article
Web of Science id
000273974600080
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
9.771 (2010)
JCR rank
3/56 (2010)
JCR quartile
1 (2010)
ISSN
0027-8424
DOI
10.1073/pnas.0913559107
language
English
UGent publication?
yes
classification
A1
copyright statement
I don't know the status of the copyright for this publication
id
878821
handle
http://hdl.handle.net/1854/LU-878821
date created
2010-02-24 11:41:39
date last changed
2012-09-19 14:03:55
@article{878821,
  abstract     = {In eukaryotes, transcription of protein-encoding genes is strongly regulated by posttranslational modifications of histones that affect the accessibility of the DNA by RNA polymerase II (RNAPII). The Elongator complex was originally identified in yeast as a histone acetyltransferase (HAT) complex that activates RNAPII-mediated transcription. In Arabidopsis thaliana, the Elongator mutants elo1, elo2, and elo3 with decreased leaf and primary root growth due to reduced cell proliferation identified homologs of components of the yeast Elongator complex, Elp4, Elp1, and Elp3, respectively. Here we show that the Elongator complex was purified from plant cell cultures as a six-component complex. The role of plant Elongator in transcription elongation was supported by colocalization of the HAT enzyme, ELO3, with euchromatin and the phosphorylated form of RNAPII, and reduced histone H3 lysine 14 acetylation at the coding region of the SHORT HYPOCOTYL 2 auxin repressor and the LAX2 auxin influx carrier gene with reduced expression levels in the elo3 mutant. Additional auxin-related genes were down-regulated in the transcriptome of elo mutants but not targeted by the Elongator HAT activity showing specificity in target gene selection. Biological relevance was apparent by auxin-related phenotypes and marker gene analysis. Ethylene and jasmonic acid signaling and abiotic stress responses were up-regulated in the elo transcriptome and might contribute to the pleiotropic elo phenotype. Thus, although the structure of Elongator and its substrate are conserved, target gene selection has diverged, showing that auxin signaling and influx are under chromatin control.},
  author       = {Nelissen, Hilde and De Groeve, Steven and Fleury, Delphine and Neyt, Pia and Bruno, Leonardo and Bitonti, Maria Beatrice and Vandenbussche, Filip and Van Der Straeten, Dominique and Yamaguchi, Takahiro and Tsukaya, Hirokazu and Witters, Erwin and De Jaeger, Geert and Houben, Andreas and Van Lijsebettens, Maria},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {BOX PROTEIN TIR1,CELLS,TANDEM AFFINITY PURIFICATION,HOLO-ELONGATOR,ORGAN GROWTH,ABSCISIC-ACID,ARABIDOPSIS-THALIANA,COMPLEX,TRANSPORT,EXPRESSION},
  language     = {eng},
  number       = {4},
  pages        = {1678--1683},
  publisher    = {NATL ACAD SCIENCES},
  title        = {Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation},
  url          = {http://dx.doi.org/10.1073/pnas.0913559107},
  volume       = {107},
  year         = {2010},
}

Chicago
Nelissen, Hilde, Steven De Groeve, Delphine Fleury, Pia Neyt, Leonardo Bruno, Maria Beatrice Bitonti, Filip Vandenbussche, et al. 2010. “Plant Elongator Regulates Auxin-related Genes During RNA Polymerase II Transcription Elongation.” Proceedings of the National Academy of Sciences of the United States of America 107 (4): 1678–1683.
APA
Nelissen, H., De Groeve, S., Fleury, D., Neyt, P., Bruno, L., Bitonti, M. B., Vandenbussche, F., et al. (2010). Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 107(4), 1678–1683.
Vancouver
1.
Nelissen H, De Groeve S, Fleury D, Neyt P, Bruno L, Bitonti MB, et al. Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. WASHINGTON: NATL ACAD SCIENCES; 2010;107(4):1678–83.
MLA
Nelissen, Hilde, Steven De Groeve, Delphine Fleury, et al. “Plant Elongator Regulates Auxin-related Genes During RNA Polymerase II Transcription Elongation.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 107.4 (2010): 1678–1683. Print.