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Polycomb repressive complex 2 controls the embryo-to-seedling phase transition

Daniel Bouyer, Francois Roudier, Maren Heese, Ellen D Andersen, Delphine Gey, Moritz Nowack UGent, Justin Goodrich, Jean-Pierre Renou, Paul E Grini, Vincent Colot, et al. (2011) PLOS GENETICS. 7(3). p.1-19
abstract
Polycomb repressive complex 2 (PRC2) is a key regulator of epigenetic states catalyzing histone H3 lysine 27 trimethylation (H3K27me3), a repressive chromatin mark. PRC2 composition is conserved from humans to plants, but the function of PRC2 during the early stage of plant life is unclear beyond the fact that it is required for the development of endosperm, a nutritive tissue that supports embryo growth. Circumventing the requirement of PRC2 in endosperm allowed us to generate viable homozygous null mutants for FERTILIZATION INDEPENDENT ENDOSPERM (FIE), which is the single Arabidopsis homolog of Extra Sex Combs, an indispensable component of Drosophila and mammalian PRC2. Here we show that H3K27me3 deposition is abolished genome-wide in fie mutants demonstrating the essential function of PRC2 in placing this mark in plants as in animals. In contrast to animals, we find that PRC2 function is not required for initial body plan formation in Arabidopsis. Rather, our results show that fie mutant seeds exhibit enhanced dormancy and germination defects, indicating a deficiency in terminating the embryonic phase. After germination, fie mutant seedlings switch to generative development that is not sustained, giving rise to neoplastic, callus-like structures. Further genome-wide studies showed that only a fraction of PRC2 targets are transcriptionally activated in fie seedlings and that this activation is accompanied in only a few cases with deposition of H3K4me3, a mark associated with gene activity and considered to act antagonistically to H3K27me3. Up-regulated PRC2 target genes were found to act at different hierarchical levels from transcriptional master regulators to a wide range of downstream targets. Collectively, our findings demonstrate that PRC2-mediated regulation represents a robust system controlling developmental phase transitions, not only from vegetative phase to flowering but also especially from embryonic phase to the seedling stage.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
TRITHORAX, FIE, DORMANCY, STEM-CELLS, GENE-EXPRESSION, ENDOSPERM DEVELOPMENT, ARABIDOPSIS-THALIANA, GROUP PROTEINS, LAND PLANT EVOLUTION, FLOWERING-LOCUS-C
journal title
PLOS GENETICS
PLoS Genet.
volume
7
issue
3
article number
e1002014
pages
1 - 19
Web of Science type
Article
Web of Science id
000288996600046
JCR category
GENETICS & HEREDITY
JCR impact factor
8.694 (2011)
JCR rank
11/155 (2011)
JCR quartile
1 (2011)
ISSN
1553-7390
DOI
10.1371/journal.pgen.1002014
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1249315
handle
http://hdl.handle.net/1854/LU-1249315
date created
2011-05-31 14:33:59
date last changed
2016-12-21 15:42:01
@article{1249315,
  abstract     = {Polycomb repressive complex 2 (PRC2) is a key regulator of epigenetic states catalyzing histone H3 lysine 27 trimethylation (H3K27me3), a repressive chromatin mark. PRC2 composition is conserved from humans to plants, but the function of PRC2 during the early stage of plant life is unclear beyond the fact that it is required for the development of endosperm, a nutritive tissue that supports embryo growth. Circumventing the requirement of PRC2 in endosperm allowed us to generate viable homozygous null mutants for FERTILIZATION INDEPENDENT ENDOSPERM (FIE), which is the single Arabidopsis homolog of Extra Sex Combs, an indispensable component of Drosophila and mammalian PRC2. Here we show that H3K27me3 deposition is abolished genome-wide in fie mutants demonstrating the essential function of PRC2 in placing this mark in plants as in animals. In contrast to animals, we find that PRC2 function is not required for initial body plan formation in Arabidopsis. Rather, our results show that fie mutant seeds exhibit enhanced dormancy and germination defects, indicating a deficiency in terminating the embryonic phase. After germination, fie mutant seedlings switch to generative development that is not sustained, giving rise to neoplastic, callus-like structures. Further genome-wide studies showed that only a fraction of PRC2 targets are transcriptionally activated in fie seedlings and that this activation is accompanied in only a few cases with deposition of H3K4me3, a mark associated with gene activity and considered to act antagonistically to H3K27me3. Up-regulated PRC2 target genes were found to act at different hierarchical levels from transcriptional master regulators to a wide range of downstream targets. Collectively, our findings demonstrate that PRC2-mediated regulation represents a robust system controlling developmental phase transitions, not only from vegetative phase to flowering but also especially from embryonic phase to the seedling stage.},
  articleno    = {e1002014},
  author       = {Bouyer, Daniel and Roudier, Francois and Heese, Maren and Andersen, Ellen D and Gey, Delphine and Nowack, Moritz and Goodrich, Justin and Renou, Jean-Pierre and Grini, Paul E and Colot, Vincent and Schnittger, Arp},
  issn         = {1553-7390},
  journal      = {PLOS GENETICS},
  keyword      = {TRITHORAX,FIE,DORMANCY,STEM-CELLS,GENE-EXPRESSION,ENDOSPERM DEVELOPMENT,ARABIDOPSIS-THALIANA,GROUP PROTEINS,LAND PLANT EVOLUTION,FLOWERING-LOCUS-C},
  language     = {eng},
  number       = {3},
  pages        = {e1002014:1--e1002014:19},
  title        = {Polycomb repressive complex 2 controls the embryo-to-seedling phase transition},
  url          = {http://dx.doi.org/10.1371/journal.pgen.1002014},
  volume       = {7},
  year         = {2011},
}

Chicago
Bouyer, Daniel, Francois Roudier, Maren Heese, Ellen D Andersen, Delphine Gey, Moritz Nowack, Justin Goodrich, et al. 2011. “Polycomb Repressive Complex 2 Controls the Embryo-to-seedling Phase Transition.” Plos Genetics 7 (3): 1–19.
APA
Bouyer, D., Roudier, F., Heese, M., Andersen, E. D., Gey, D., Nowack, M., Goodrich, J., et al. (2011). Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLOS GENETICS, 7(3), 1–19.
Vancouver
1.
Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack M, et al. Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLOS GENETICS. 2011;7(3):1–19.
MLA
Bouyer, Daniel, Francois Roudier, Maren Heese, et al. “Polycomb Repressive Complex 2 Controls the Embryo-to-seedling Phase Transition.” PLOS GENETICS 7.3 (2011): 1–19. Print.