An ortholog of CURLY LEAF / ENHANCER OF ZESTE like‐1 is required for proper flowering in Brachypodium distachyon
Abstract
Summary Many plants require prolonged exposure to cold to acquire the competence to flower. The process by which cold exposure results in competence is known as vernalization. In Arabidopsis thaliana , vernalization leads to the stable repression of the floral repressor FLOWERING LOCUS C via chromatin modification, including an increase of trimethylation on lysine 27 of histone H3 (H3K27me3) by Polycomb Repressive Complex 2 ( PRC 2). Vernalization in pooids is associated with the stable induction of a floral promoter, VERNALIZATION 1 ( VRN1 ). From a screen for mutants with a reduced vernalization requirement in the model grass Brachypodium distachyon , we identified two recessive alleles of ENHANCER OF ZESTE ‐ LIKE 1 ( EZL 1 ). EZL 1 is orthologous to A. thaliana CURLY LEAF 1 , a gene that encodes the catalytic subunit of PRC 2. B. distachyon ezl1 mutants flower rapidly without vernalization in long‐day ( LD ) photoperiods; thus, EZL 1 is required for the proper maintenance of the vegetative state prior to vernalization. Transcriptomic studies in ezl1 revealed mis‐regulation of thousands of genes, including ectopic expression of several floral homeotic genes in leaves. Loss of EZL 1 results in the global reduction of H3K27me3 andmore »
- Authors:
-
[1];
[2];
[4];
[6];
[2]
- Laboratory of Genetics University of Wisconsin 425‐G Henry Mall Madison WI 53706 USA, Department of Biochemistry University of Wisconsin 433 Babcock Dr. Madison WI 53706 USA
- Laboratory of Genetics University of Wisconsin 425‐G Henry Mall Madison WI 53706 USA, Department of Biochemistry University of Wisconsin 433 Babcock Dr. Madison WI 53706 USA, DOE Great Lakes Bioenergy Research Center University of Wisconsin‐Madison Madison WI 53706 USA
- Department of Biochemistry University of Wisconsin 433 Babcock Dr. Madison WI 53706 USA
- Department of Biochemistry University of Wisconsin 433 Babcock Dr. Madison WI 53706 USA, DOE Great Lakes Bioenergy Research Center University of Wisconsin‐Madison Madison WI 53706 USA
- Donald Danforth Plant Science Center St. Louis MO 63132 USA
- Laboratory of Genetics University of Wisconsin 425‐G Henry Mall Madison WI 53706 USA, Wisconsin Institute for Discovery University of Wisconsin, Madison Madison WI 53705 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1419893
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Name: The Plant Journal Journal Volume: 93 Journal Issue: 5; Journal ID: ISSN 0960-7412
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Lomax, Aaron, Woods, Daniel P., Dong, Yinxin, Bouché, Frédéric, Rong, Ying, Mayer, Kevin S., Zhong, Xuehua, and Amasino, Richard M. An ortholog of CURLY LEAF / ENHANCER OF ZESTE like‐1 is required for proper flowering in Brachypodium distachyon. United Kingdom: N. p., 2018.
Web. doi:10.1111/tpj.13815.
Lomax, Aaron, Woods, Daniel P., Dong, Yinxin, Bouché, Frédéric, Rong, Ying, Mayer, Kevin S., Zhong, Xuehua, & Amasino, Richard M. An ortholog of CURLY LEAF / ENHANCER OF ZESTE like‐1 is required for proper flowering in Brachypodium distachyon. United Kingdom. https://doi.org/10.1111/tpj.13815
Lomax, Aaron, Woods, Daniel P., Dong, Yinxin, Bouché, Frédéric, Rong, Ying, Mayer, Kevin S., Zhong, Xuehua, and Amasino, Richard M. Wed .
"An ortholog of CURLY LEAF / ENHANCER OF ZESTE like‐1 is required for proper flowering in Brachypodium distachyon". United Kingdom. https://doi.org/10.1111/tpj.13815.
@article{osti_1419893,
title = {An ortholog of CURLY LEAF / ENHANCER OF ZESTE like‐1 is required for proper flowering in Brachypodium distachyon},
author = {Lomax, Aaron and Woods, Daniel P. and Dong, Yinxin and Bouché, Frédéric and Rong, Ying and Mayer, Kevin S. and Zhong, Xuehua and Amasino, Richard M.},
abstractNote = {Summary Many plants require prolonged exposure to cold to acquire the competence to flower. The process by which cold exposure results in competence is known as vernalization. In Arabidopsis thaliana , vernalization leads to the stable repression of the floral repressor FLOWERING LOCUS C via chromatin modification, including an increase of trimethylation on lysine 27 of histone H3 (H3K27me3) by Polycomb Repressive Complex 2 ( PRC 2). Vernalization in pooids is associated with the stable induction of a floral promoter, VERNALIZATION 1 ( VRN1 ). From a screen for mutants with a reduced vernalization requirement in the model grass Brachypodium distachyon , we identified two recessive alleles of ENHANCER OF ZESTE ‐ LIKE 1 ( EZL 1 ). EZL 1 is orthologous to A. thaliana CURLY LEAF 1 , a gene that encodes the catalytic subunit of PRC 2. B. distachyon ezl1 mutants flower rapidly without vernalization in long‐day ( LD ) photoperiods; thus, EZL 1 is required for the proper maintenance of the vegetative state prior to vernalization. Transcriptomic studies in ezl1 revealed mis‐regulation of thousands of genes, including ectopic expression of several floral homeotic genes in leaves. Loss of EZL 1 results in the global reduction of H3K27me3 and H3K27me2, consistent with this gene making a major contribution to PRC 2 activity in B. distachyon . Furthermore, in ezl1 mutants, the flowering genes VRN 1 and AGAMOUS ( AG ) are ectopically expressed and have reduced H3K27me3. Artificial micro RNA knock‐down of either VRN 1 or AG in ezl1‐1 mutants partially restores wild‐type flowering behavior in non‐vernalized plants, suggesting that ectopic expression in ezl1 mutants may contribute to the rapid‐flowering phenotype.},
doi = {10.1111/tpj.13815},
journal = {The Plant Journal},
number = 5,
volume = 93,
place = {United Kingdom},
year = {Wed Feb 07 00:00:00 EST 2018},
month = {Wed Feb 07 00:00:00 EST 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/tpj.13815
https://doi.org/10.1111/tpj.13815
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 18 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes
journal, August 2013
- Ruelens, Philip; de Maagd, Ruud A.; Proost, Sebastian
- Nature Communications, Vol. 4, Issue 1
Function and evolution of the plant MADS-box gene family
journal, March 2001
- Ng, Medard; Yanofsky, Martin F.
- Nature Reviews Genetics, Vol. 2, Issue 3
Distinct Roles of CONSTANS Target Genes in Reproductive Development of Arabidopsis
journal, June 2000
- Samach, A.
- Science, Vol. 288, Issue 5471
Polycomb-group proteins repressthe floral activator AGL19 in the FLC-independent vernalization pathway
journal, June 2006
- Schonrock, N.
- Genes & Development, Vol. 20, Issue 12
A Polycomb-group gene regulates homeotic gene expression in Arabidopsis
journal, March 1997
- Goodrich, Justin; Puangsomlee, Preeya; Martin, Marta
- Nature, Vol. 386, Issue 6620
OsVIL2 functions with PRC2 to induce flowering by repressing O s LFL 1 in rice
journal, December 2012
- Yang, Jungil; Lee, Shinyong; Hang, Runlai
- The Plant Journal, Vol. 73, Issue 4
The rice enhancer of zeste [E(z)] genes SDG711 and SDG718 are respectively involved in long day and short day signaling to mediate the accurate photoperiod control of flowering time
journal, October 2014
- Liu, Xiaoyun; Zhou, Chao; Zhao, Yu
- Frontiers in Plant Science, Vol. 5
Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity
journal, October 1992
- Mizukami, Yukiko; Ma, Hong
- Cell, Vol. 71, Issue 1
Interaction of Polycomb-group proteins controlling flowering in Arabidopsis
journal, November 2004
- Chanvivattana, Y.
- Development, Vol. 131, Issue 21
Polycomb-Dependent H3K27me1 and H3K27me2 Regulate Active Transcription and Enhancer Fidelity
journal, January 2014
- Ferrari, Karin J.; Scelfo, Andrea; Jammula, SriGanesh
- Molecular Cell, Vol. 53, Issue 1
REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms
journal, July 2011
- Supek, Fran; Bošnjak, Matko; Škunca, Nives
- PLoS ONE, Vol. 6, Issue 7
Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds
journal, August 2000
- Luo, M.; Bilodeau, P.; Dennis, E. S.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 19
The FLF MADS Box Gene: A Repressor of Flowering in Arabidopsis Regulated by Vernalization and Methylation
journal, March 1999
- Sheldon, Candice C.; Burn, Joanne E.; Perez, Pascual P.
- The Plant Cell, Vol. 11, Issue 3
A genetic network of flowering-time genes in wheat leaves, in which an APETALA1 / FRUITFULL -like gene, VRN1 , is upstream of FLOWERING LOCUS T
journal, May 2009
- Shimada, Sanae; Ogawa, Taiichi; Kitagawa, Satoshi
- The Plant Journal, Vol. 58, Issue 4
Quantitative Mass Spectrometry of Histones H3.2 and H3.3 in Suz12 -deficient Mouse Embryonic Stem Cells Reveals Distinct, Dynamic Post-translational Modifications at Lys-27 and Lys-36
journal, February 2010
- Jung, Hye Ryung; Pasini, Diego; Helin, Kristian
- Molecular & Cellular Proteomics, Vol. 9, Issue 5
The molecular basis of vernalization-induced flowering in cereals
journal, August 2007
- Trevaskis, Ben; Hemming, Megan N.; Dennis, Elizabeth S.
- Trends in Plant Science, Vol. 12, Issue 8
Wheat TILLING Mutants Show That the Vernalization Gene VRN1 Down-Regulates the Flowering Repressor VRN2 in Leaves but Is Not Essential for Flowering
journal, December 2012
- Chen, Andrew; Dubcovsky, Jorge
- PLoS Genetics, Vol. 8, Issue 12
Evolution of VRN2/Ghd7- Like Genes in Vernalization-Mediated Repression of Grass Flowering
journal, February 2016
- Woods, Daniel P.; McKeown, Meghan A.; Dong, Yinxin
- Plant Physiology, Vol. 170, Issue 4
Low-Temperature and Daylength Cues Are Integrated to Regulate FLOWERING LOCUS T in Barley
journal, March 2008
- Hemming, Megan N.; Peacock, W. James; Dennis, Elizabeth S.
- Plant Physiology, Vol. 147, Issue 1
Natural Variation in Brachypodium Links Vernalization and Flowering Time Loci as Major Flowering Determinants
journal, September 2016
- Bettgenhaeuser, Jan; Corke, Fiona M. K.; Opanowicz, Magdalena
- Plant Physiology, Vol. 173, Issue 1
EMBRYONIC FLOWER2, a Novel Polycomb Group Protein Homolog, Mediates Shoot Development and Flowering in Arabidopsis
journal, November 2001
- Yoshida, Nobumasa; Yanai, Yukihiro; Chen, Lingjing
- The Plant Cell, Vol. 13, Issue 11
Keeping the gate closed: functions of the polycomb repressive complex PRC2 in development
journal, April 2015
- Mozgova, Iva; Köhler, Claudia; Hennig, Lars
- The Plant Journal, Vol. 83, Issue 1
The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3
journal, September 2006
- Wood, C. C.; Robertson, M.; Tanner, G.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 39
Expression, Imprinting, and Evolution of Rice Homologs of the Polycomb Group Genes
journal, July 2009
- Luo, Ming; Platten, Damien; Chaudhury, Abed
- Molecular Plant, Vol. 2, Issue 4
Rice leaf inclination2, a VIN3-like protein, regulates leaf angle through modulating cell division of the collar
journal, July 2010
- Zhao, Shu-Qing; Hu, Jiang; Guo, Long-Biao
- Cell Research, Vol. 20, Issue 8
Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27
journal, September 2006
- Schubert, Daniel; Primavesi, Lucia; Bishopp, Anthony
- The EMBO Journal, Vol. 25, Issue 19
Environmental perception and epigenetic memory: mechanistic insight through FLC
journal, May 2015
- Berry, Scott; Dean, Caroline
- The Plant Journal, Vol. 83, Issue 1
Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs: Imprinting of Mez1 in the maize endosperm
journal, December 2006
- Haun, William J.; Laoueillé-Duprat, Sylvia; O'Connell, Mary J.
- The Plant Journal, Vol. 49, Issue 2
Seasonal and developmental timing of flowering
journal, March 2010
- Amasino, Richard
- The Plant Journal, Vol. 61, Issue 6
Polycomb Group Gene OsFIE2 Regulates Rice (Oryza sativa) Seed Development and Grain Filling via a Mechanism Distinct from Arabidopsis
journal, March 2013
- Nallamilli, Babi Ramesh Reddy; Zhang, Jian; Mujahid, Hana
- PLoS Genetics, Vol. 9, Issue 3
The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare).
journal, April 2009
- Sasani, Shahryar; Hemming, Megan N.; Oliver, Sandra N.
- Journal of Experimental Botany, Vol. 60, Issue 7
MADS box genes control vernalization-induced flowering in cereals
journal, October 2003
- Trevaskis, B.; Bagnall, D. J.; Ellis, M. H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 22
Control of reproduction by Polycomb Group complexes in animals and plants
journal, January 2005
- Guitton, Anne-Elisabeth; Berger, Frederic
- The International Journal of Developmental Biology, Vol. 49, Issue 5-6
The wheat and barley vernalization gene VRN3 is an orthologue of FT
journal, December 2006
- Yan, L.; Fu, D.; Li, C.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 51
LC2 and OsVIL2 Promote Rice Flowering by Photoperoid-Induced Epigenetic Silencing of OsLF
journal, March 2013
- Wang, Jun; Hu, Jiang; Qian, Qian
- Molecular Plant, Vol. 6, Issue 2
TaVRT-1, a Putative Transcription Factor Associated with Vegetative to Reproductive Transition in Cereals
journal, July 2003
- Danyluk, Jean; Kane, Ndjido A.; Breton, Ghislain
- Plant Physiology, Vol. 132, Issue 4
Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon
journal, December 2013
- Ream, Thomas S.; Woods, Daniel P.; Schwartz, Christopher J.
- Plant Physiology, Vol. 164, Issue 2
From flour to flower: how Polycomb group proteins influence multiple aspects of plant development
journal, September 2003
- Hsieh, T.
- Trends in Plant Science, Vol. 8, Issue 9
Vernalization and its Relations to Dormancy
journal, June 1960
- Chouard, P.
- Annual Review of Plant Physiology, Vol. 11, Issue 1
Imprinted gene OsFIE1 modulates rice seed development by influencing nutrient metabolism and modifying genome H3K27me3
journal, July 2016
- Huang, Xiaolong; Lu, Zhanhua; Wang, Xin
- The Plant Journal, Vol. 87, Issue 3
PlantTFcat: an online plant transcription factor and transcriptional regulator categorization and analysis tool
journal, January 2013
- Dai, Xinbin; Sinharoy, Senjuti; Udvardi, Michael
- BMC Bioinformatics, Vol. 14, Issue 1
A PHD-Polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization
journal, October 2008
- De Lucia, F.; Crevillen, P.; Jones, A. M. E.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 44
The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization
journal, March 2004
- Yan, L.
- Science, Vol. 303, Issue 5664
Memory of the vernalized state in plants including the model grass Brachypodium distachyon
journal, March 2014
- Woods, Daniel P.; Ream, Thomas S.; Amasino, Richard M.
- Frontiers in Plant Science, Vol. 5
Genetic Architecture of Flowering-Time Variation in Brachypodium distachyon
journal, October 2016
- Woods, Daniel P.; Bednarek, Ryland; Bouché, Frédéric
- Plant Physiology, Vol. 173, Issue 1
FD, a bZIP Protein Mediating Signals from the Floral Pathway Integrator FT at the Shoot Apex
journal, August 2005
- Abe, M.
- Science, Vol. 309, Issue 5737
Genome-wide activities of Polycomb complexes control pervasive transcription
journal, May 2015
- Lee, Hun-Goo; Kahn, Tatyana G.; Simcox, Amanda
- Genome Research, Vol. 25, Issue 8
WAP1, a Wheat APETALA1 Homolog, Plays a Central Role in the Phase Transition from Vegetative to Reproductive Growth
journal, December 2003
- Murai, Koji; Miyamae, Mamiko; Kato, Hiromi
- Plant and Cell Physiology, Vol. 44, Issue 12
Integration of Spatial and Temporal Information During Floral Induction in Arabidopsis
journal, August 2005
- Wigge, P. A.
- Science, Vol. 309, Issue 5737
The VERNALIZATION 2 Gene Mediates the Epigenetic Regulation of Vernalization in Arabidopsis
journal, November 2001
- Gendall, Anthony R.; Levy, Yaron Y.; Wilson, Allison
- Cell, Vol. 107, Issue 4
Vernalization requires epigenetic silencing of FLC by histone methylation
journal, January 2004
- Bastow, Ruth; Mylne, Joshua S.; Lister, Clare
- Nature, Vol. 427, Issue 6970
Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene
journal, May 2009
- Oliver, S. N.; Finnegan, E. J.; Dennis, E. S.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 20
The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene
journal, January 2007
- Shitsukawa, Naoki; Ikari, Chihiro; Shimada, Sanae
- Genes & Genetic Systems, Vol. 82, Issue 2
Positional cloning of the wheat vernalization gene VRN1
journal, May 2003
- Yan, L.; Loukoianov, A.; Tranquilli, G.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 10
Vernalization, Competence, and the Epigenetic Memory of Winter
journal, October 2004
- Amasino, Richard
- The Plant Cell, Vol. 16, Issue 10
Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1
journal, June 2017
- Woods, Daniel P.; Ream, Thomas S.; Bouché, Frédéric
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 25
Vernalization: Winter and the Timing of Flowering in Plants
journal, November 2009
- Kim, Dong-Hwan; Doyle, Mark R.; Sung, Sibum
- Annual Review of Cell and Developmental Biology, Vol. 25, Issue 1
Mutagenesis of Plants Overexpressing CONSTANS Demonstrates Novel Interactions among Arabidopsis Flowering-Time Genes
journal, June 2000
- Onouchi, Hitoshi; Igeño, M. Isabel; Périlleux, Claire
- The Plant Cell, Vol. 12, Issue 6
Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb Repressive Complex 2 Components
journal, October 2008
- Jiang, Danhua; Wang, Yuqi; Wang, Yizhong
- PLoS ONE, Vol. 3, Issue 10
Antagonistic Roles of SEPALLATA3, FT and FLC Genes as Targets of the Polycomb Group Gene CURLY LEAF
journal, February 2012
- Lopez-Vernaza, Manuel; Yang, Suxin; Müller, Ralf
- PLoS ONE, Vol. 7, Issue 2
Reconstructing the Evolutionary History of Paralogous APETALA1/FRUITFULL -Like Genes in Grasses (Poaceae)
journal, July 2006
- Preston, Jill C.; Kellogg, Elizabeth A.
- Genetics, Vol. 174, Issue 1
The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis
journal, September 2000
- Lee, H.
- Genes & Development, Vol. 14, Issue 18
A Flowering Locus C Homolog Is a Vernalization-Regulated Repressor in Brachypodium and Is Cold Regulated in Wheat
journal, December 2016
- Sharma, Neha; Ruelens, Philip; D'hauw, Mariëlla
- Plant Physiology, Vol. 173, Issue 2
The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis
journal, March 2006
- Searle, I.
- Genes & Development, Vol. 20, Issue 7
PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon
journal, July 2014
- Woods, Daniel P.; Ream, Thomas S.; Minevich, Gregory
- Genetics, Vol. 198, Issue 1
High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3
journal, November 2007
- Vogel, John; Hill, Theresa
- Plant Cell Reports, Vol. 27, Issue 3
FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering
journal, May 1999
- Michaels, Scott D.; Amasino, Richard M.
- The Plant Cell, Vol. 11, Issue 5
Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3
journal, January 2004
- Sung, Sibum; Amasino, Richard M.
- Nature, Vol. 427, Issue 6970
The polycomb group gene EMF2B is essential for maintenance of floral meristem determinacy in rice
journal, November 2014
- Conrad, Liza J.; Khanday, Imtiyaz; Johnson, Cameron
- The Plant Journal, Vol. 80, Issue 5