Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition
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 th...
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| Published in | PLoS genetics Vol. 7; no. 3; p. e1002014 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.03.2011
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| 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. |
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| AbstractList | 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.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. 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. Epigenetic regulation of gene expression through modifications of histone tails is fundamental for growth and development of multicellular organisms. The trimethylation of lysine 27 of histone 3 (H3K27me3) is the landmark of Polycomb Repressive Complex2 (PRC2) function and is associated with gene repression. Here we present the development of a genetic system to generate homozygous null mutants of Arabidopsis PRC2. A first major finding is that H3K27me3 is globally lost in these mutants. Surprisingly, we found that initial body plant organization and embryo development is largely independent of PRC2 action, which is in sharp contrast to embryonic lethality of PRC2 mutants in animals. However, we show here that PRC2 is required to switch from embryonic to seedling phase, and mutant seeds showed enhanced dormancy and germination defects. Indeed, many genes controlling seed maturation and dormancy are marked by H3K27me3 and are upregulated upon loss of PRC2. The invention of seed dormancy of land plants is regarded as one of the major reasons for the evolutionary success of flowering plants, and the here-discovered key role of PRC2 during the developmental phase transition from embryo to seedling growth reveals the adaptation of conserved molecular mechanisms to carry out new functions. 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. 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. 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. Epigenetic regulation of gene expression through modifications of histone tails is fundamental for growth and development of multicellular organisms. The trimethylation of lysine 27 of histone 3 (H3K27me3) is the landmark of Polycomb Repressive Complex2 (PRC2) function and is associated with gene repression. Here we present the development of a genetic system to generate homozygous null mutants of Arabidopsis PRC2. A first major finding is that H3K27me3 is globally lost in these mutants. Surprisingly, we found that initial body plant organization and embryo development is largely independent of PRC2 action, which is in sharp contrast to embryonic lethality of PRC2 mutants in animals. However, we show here that PRC2 is required to switch from embryonic to seedling phase, and mutant seeds showed enhanced dormancy and germination defects. Indeed, many genes controlling seed maturation and dormancy are marked by H3K27me3 and are upregulated upon loss of PRC2. The invention of seed dormancy of land plants is regarded as one of the major reasons for the evolutionary success of flowering plants, and the here-discovered key role of PRC2 during the developmental phase transition from embryo to seedling growth reveals the adaptation of conserved molecular mechanisms to carry out new functions. |
| Audience | Academic |
| Author | Andersen, Ellen D. Gey, Delphine Colot, Vincent Grini, Paul E. Renou, Jean-Pierre Bouyer, Daniel Roudier, Francois Nowack, Moritz K. Goodrich, Justin Schnittger, Arp Heese, Maren |
| AuthorAffiliation | 2 Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR 8197–INSERM U 1024, Paris, France 5 Department of Plant Systems Biology, VIB, Gent, Belgium The University of North Carolina at Chapel Hill, United States of America 7 Institute of Molecular Plant Science, University of Edinburgh, Edinburgh, United Kingdom 1 Department of Molecular Mechanisms of Phenotypic Plasticity, Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France 3 Department of Molecular Biosciences, University of Oslo, Oslo, Norway 4 Department of Plant Genomics Research, CNRS/INRA, Evry, France 6 Department of Plant Biotechnology and Genetics, Ghent University, Gent, Belgium |
| AuthorAffiliation_xml | – name: 1 Department of Molecular Mechanisms of Phenotypic Plasticity, Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France – name: 4 Department of Plant Genomics Research, CNRS/INRA, Evry, France – name: 6 Department of Plant Biotechnology and Genetics, Ghent University, Gent, Belgium – name: 7 Institute of Molecular Plant Science, University of Edinburgh, Edinburgh, United Kingdom – name: 2 Institut de Biologie de l'Ecole Normale Supérieure, CNRS UMR 8197–INSERM U 1024, Paris, France – name: The University of North Carolina at Chapel Hill, United States of America – name: 3 Department of Molecular Biosciences, University of Oslo, Oslo, Norway – name: 5 Department of Plant Systems Biology, VIB, Gent, Belgium |
| Author_xml | – sequence: 1 givenname: Daniel surname: Bouyer fullname: Bouyer, Daniel – sequence: 2 givenname: Francois surname: Roudier fullname: Roudier, Francois – sequence: 3 givenname: Maren surname: Heese fullname: Heese, Maren – sequence: 4 givenname: Ellen D. surname: Andersen fullname: Andersen, Ellen D. – sequence: 5 givenname: Delphine surname: Gey fullname: Gey, Delphine – sequence: 6 givenname: Moritz K. surname: Nowack fullname: Nowack, Moritz K. – sequence: 7 givenname: Justin surname: Goodrich fullname: Goodrich, Justin – sequence: 8 givenname: Jean-Pierre surname: Renou fullname: Renou, Jean-Pierre – sequence: 9 givenname: Paul E. surname: Grini fullname: Grini, Paul E. – sequence: 10 givenname: Vincent surname: Colot fullname: Colot, Vincent – sequence: 11 givenname: Arp surname: Schnittger fullname: Schnittger, Arp |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21423668$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-02647278$$DView record in HAL |
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| Copyright | COPYRIGHT 2011 Public Library of Science Distributed under a Creative Commons Attribution 4.0 International License Bouyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 2011 2011 Bouyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, et al. (2011) Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition. PLoS Genet 7(3): e1002014. doi:10.1371/journal.pgen.1002014 |
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| Title | Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition |
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