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Title: Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1

Abstract

A requirement for vernalization, the process by which prolonged cold exposure provides competence to flower, is an important adaptation to temperate climates that ensures flowering does not occur before the onset of winter. In temperate grasses, vernalization results in the up-regulation of VERNALIZATION1 (VRN1) to establish competence to flower; however, little is known about the mechanism underlying repression of VRN1 in the fall season, which is necessary to establish a vernalization requirement. In this paper, we report that a plant-specific gene containing a bromo-adjacent homology and transcriptional elongation factor S-II domain, which we named REPRESSOR OF VERNALIZATION1 (RVR1), represses VRN1 before vernalization in Brachypodium distachyon. That RVR1 is upstream of VRN1 is supported by the observations that VRN1 is precociously elevated in an rvr1 mutant, resulting in rapid flowering without cold exposure, and the rapid-flowering rvr1 phenotype is dependent on VRN1. The precocious VRN1 expression in rvr1 is associated with reduced levels of the repressive chromatin modification H3K27me3 at VRN1, which is similar to the reduced VRN1 H3K27me3 in vernalized plants. Furthermore, the transcriptome of vernalized wild-type plants overlaps with that of nonvernalized rvr1 plants, indicating loss of rvr1 is similar to the vernalized state at a molecular level. However,more » loss of rvr1 results in more differentially expressed genes than does vernalization, indicating that RVR1 may be involved in processes other than vernalization despite a lack of any obvious pleiotropy in the rvr1 mutant. This study provides an example of a role for this class of plant-specific genes.« less

Authors:
ORCiD logo; ; ORCiD logo; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1361438
Alternate Identifier(s):
OSTI ID: 1532918
Grant/Contract Number:  
FCO2-07ER64494; FC02-07ER64494
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; science & technology; vernalization; Brachypodium; flowering; VRN1; RVR1

Citation Formats

Woods, Daniel P., Ream, Thomas S., Bouché, Frédéric, Lee, Joohyun, Thrower, Nicholas, Wilkerson, Curtis, and Amasino, Richard M. Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1. United States: N. p., 2017. Web. doi:10.1073/pnas.1700536114.
Woods, Daniel P., Ream, Thomas S., Bouché, Frédéric, Lee, Joohyun, Thrower, Nicholas, Wilkerson, Curtis, & Amasino, Richard M. Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1. United States. https://doi.org/10.1073/pnas.1700536114
Woods, Daniel P., Ream, Thomas S., Bouché, Frédéric, Lee, Joohyun, Thrower, Nicholas, Wilkerson, Curtis, and Amasino, Richard M. Mon . "Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1". United States. https://doi.org/10.1073/pnas.1700536114.
@article{osti_1361438,
title = {Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1},
author = {Woods, Daniel P. and Ream, Thomas S. and Bouché, Frédéric and Lee, Joohyun and Thrower, Nicholas and Wilkerson, Curtis and Amasino, Richard M.},
abstractNote = {A requirement for vernalization, the process by which prolonged cold exposure provides competence to flower, is an important adaptation to temperate climates that ensures flowering does not occur before the onset of winter. In temperate grasses, vernalization results in the up-regulation of VERNALIZATION1 (VRN1) to establish competence to flower; however, little is known about the mechanism underlying repression of VRN1 in the fall season, which is necessary to establish a vernalization requirement. In this paper, we report that a plant-specific gene containing a bromo-adjacent homology and transcriptional elongation factor S-II domain, which we named REPRESSOR OF VERNALIZATION1 (RVR1), represses VRN1 before vernalization in Brachypodium distachyon. That RVR1 is upstream of VRN1 is supported by the observations that VRN1 is precociously elevated in an rvr1 mutant, resulting in rapid flowering without cold exposure, and the rapid-flowering rvr1 phenotype is dependent on VRN1. The precocious VRN1 expression in rvr1 is associated with reduced levels of the repressive chromatin modification H3K27me3 at VRN1, which is similar to the reduced VRN1 H3K27me3 in vernalized plants. Furthermore, the transcriptome of vernalized wild-type plants overlaps with that of nonvernalized rvr1 plants, indicating loss of rvr1 is similar to the vernalized state at a molecular level. However, loss of rvr1 results in more differentially expressed genes than does vernalization, indicating that RVR1 may be involved in processes other than vernalization despite a lack of any obvious pleiotropy in the rvr1 mutant. This study provides an example of a role for this class of plant-specific genes.},
doi = {10.1073/pnas.1700536114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = ,
volume = ,
place = {United States},
year = {Mon Jun 05 00:00:00 EDT 2017},
month = {Mon Jun 05 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1073/pnas.1700536114

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Cited by: 27 works
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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
  • DOI: 10.1038/ncomms3280

Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization
journal, January 2007


The Molecular Basis of Vernalization in Different Plant Groups
journal, January 2012

  • Ream, T. S.; Woods, D. P.; Amasino, R. M.
  • Cold Spring Harbor Symposia on Quantitative Biology, Vol. 77, Issue 0
  • DOI: 10.1101/sqb.2013.77.014449

Effect of Photoperiod on the Regulation of Wheat Vernalization Genes VRN1 and VRN2
journal, March 2006


The role of seasonal flowering responses in adaptation of grasses to temperate climates
journal, August 2014


The Flowering Integrator FT Regulates SEPALLATA3 and FRUITFULL Accumulation in Arabidopsis Leaves
journal, September 2005


CloudMap: A Cloud-Based Pipeline for Analysis of Mutant Genome Sequences
journal, October 2012


Regulation of flowering in temperate cereals
journal, April 2009


The Evolution of CONSTANS -Like Gene Families in Barley, Rice, and Arabidopsis
journal, March 2003

  • Griffiths, Simon; Dunford, Roy P.; Coupland, George
  • Plant Physiology, Vol. 131, Issue 4
  • DOI: 10.1104/pp.102.016188

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
  • DOI: 10.1104/pp.15.01279

The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation
journal, March 1999


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
  • DOI: 10.1104/pp.108.116418

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
  • DOI: 10.1104/pp.16.00813

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
  • DOI: 10.1073/pnas.0606385103

Characterization of the maintained vegetative phase deletions from diploid wheat and their effect on VRN2 and FT transcript levels
journal, January 2010


Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses
journal, April 2010


Phylogenomic Analyses of the BARREN STALK1/LAX PANICLE1 (BA1/LAX1) Genes and Evidence for Their Roles During Axillary Meristem Development
journal, February 2011

  • Woods, Daniel P.; Hope, Chelsea L.; Malcomber, Simon T.
  • Molecular Biology and Evolution, Vol. 28, Issue 7
  • DOI: 10.1093/molbev/msr036

Leaf-produced floral signals
journal, October 2008


SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building
journal, October 2009

  • Gouy, M.; Guindon, S.; Gascuel, O.
  • Molecular Biology and Evolution, Vol. 27, Issue 2
  • DOI: 10.1093/molbev/msp259

Seasonal and developmental timing of flowering
journal, March 2010


Genetic and Molecular Characterization of the VRN2 Loci in Tetraploid Wheat
journal, November 2008

  • Distelfeld, Assaf; Tranquilli, Gabriela; Li, Chengxia
  • Plant Physiology, Vol. 149, Issue 1
  • DOI: 10.1104/pp.108.129353

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
  • DOI: 10.1093/jxb/erp098

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
  • DOI: 10.1073/pnas.0607142103

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
  • DOI: 10.1104/pp.113.232678

Vernalization and its Relations to Dormancy
journal, June 1960


The transcription elongation factor TFIIS is a component of RNA polymerase II preinitiation complexes
journal, October 2007

  • Kim, B.; Nesvizhskii, A. I.; Rani, P. G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 41
  • DOI: 10.1073/pnas.0704573104

The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization
journal, March 2004


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
  • DOI: 10.1073/pnas.0808687105

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
  • DOI: 10.3389/fpls.2014.00099

Direct links between the vernalization response and other key traits of cereal crops
journal, January 2015

  • Deng, Weiwei; Casao, M. Cristina; Wang, Penghao
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms6882

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
  • DOI: 10.1104/pp.16.01178

Structure and function of the BAH domain in chromatin biology
journal, November 2012


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
  • DOI: 10.1073/pnas.0903566106

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
  • DOI: 10.1073/pnas.0937399100

FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis
journal, May 2007


Reading the Combinatorial Histone Language
journal, December 2015


Reconstructing the Evolutionary History of Paralogous APETALA1/FRUITFULL -Like Genes in Grasses (Poaceae)
journal, July 2006


The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals
journal, March 2009

  • Greenup, Aaron; Peacock, W. James; Dennis, Elizabeth S.
  • Annals of Botany, Vol. 103, Issue 8
  • DOI: 10.1093/aob/mcp063

PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon
journal, July 2014


Brachypodium distachyon and Setaria viridis : Model Genetic Systems for the Grasses
journal, April 2015


Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals
journal, March 2014

  • Shrestha, Roshi; Gómez-Ariza, Jorge; Brambilla, Vittoria
  • Annals of Botany, Vol. 114, Issue 7
  • DOI: 10.1093/aob/mcu032

Winter Memory throughout the Plant Kingdom: Different Paths to Flowering
journal, October 2016

  • Bouché, Frédéric; Woods, Daniel P.; Amasino, Richard M.
  • Plant Physiology, Vol. 173, Issue 1
  • DOI: 10.1104/pp.16.01322

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
  • DOI: 10.1105/tpc.11.5.949

Characterization of FLOWERING LOCUS T1 (FT1) Gene in Brachypodium and Wheat
journal, April 2014


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014