A florigen paralog is required for short-day vernalization in a pooid grass
Abstract
Perception of seasonal cues is critical for reproductive success in many plants. Exposure to winter cold is a cue that can confer competence to flower in the spring via a process known as vernalization. In certain grasses, exposure to short days is another winter cue that can lead to a vernalized state. In Brachypodium distachyon, we find that natural variation for the ability of short days to confer competence to flower is due to allelic variation of the FLOWERING LOCUS T (FT1) paralog FT-like9 (FTL9). An active FTL9 allele is required for the acquisition of floral competence, demonstrating a novel role for a member of the FT family of genes. Loss of the short-day vernalization response appears to have arisen once in B. distachyon and spread through diverse lineages indicating that this loss has adaptive value, perhaps by delaying spring flowering until the danger of cold damage to flowers has subsided.
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States); Univ. of California, Davis, CA (United States)
- Univ. of Wisconsin, Madison, WI (United States); Northwest A&F Univ., Yangling (China); Chinese Academy of Sciences (CAS), Kunming (China)
- Univ. of Wisconsin, Madison, WI (United States); Univ. of Liege (Belgium)
- Univ. of Wisconsin, Madison, WI (United States); Cornell Univ., Ithaca, NY (United States)
- Univ. of Wisconsin, Madison, WI (United States)
- Univ. of Wisconsin, Madison, WI (United States); Monsanto Company, Chesterfield, MO (United States)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foudnation (NSF); National Institutes of Health (NIH)
- OSTI Identifier:
- 1601237
- Grant/Contract Number:
- SC0018409; FC02-07ER6449; IOS-1258126
- Resource Type:
- Accepted Manuscript
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Woods, Daniel, Dong, Yinxin, Bouche, Frederic, Bednarek, Ryland, Rowe, Mark, Ream, Thomas, and Amasino, Richard. A florigen paralog is required for short-day vernalization in a pooid grass. United States: N. p., 2019.
Web. doi:10.7554/eLife.42153.
Woods, Daniel, Dong, Yinxin, Bouche, Frederic, Bednarek, Ryland, Rowe, Mark, Ream, Thomas, & Amasino, Richard. A florigen paralog is required for short-day vernalization in a pooid grass. United States. https://doi.org/10.7554/eLife.42153
Woods, Daniel, Dong, Yinxin, Bouche, Frederic, Bednarek, Ryland, Rowe, Mark, Ream, Thomas, and Amasino, Richard. Tue .
"A florigen paralog is required for short-day vernalization in a pooid grass". United States. https://doi.org/10.7554/eLife.42153. https://www.osti.gov/servlets/purl/1601237.
@article{osti_1601237,
title = {A florigen paralog is required for short-day vernalization in a pooid grass},
author = {Woods, Daniel and Dong, Yinxin and Bouche, Frederic and Bednarek, Ryland and Rowe, Mark and Ream, Thomas and Amasino, Richard},
abstractNote = {Perception of seasonal cues is critical for reproductive success in many plants. Exposure to winter cold is a cue that can confer competence to flower in the spring via a process known as vernalization. In certain grasses, exposure to short days is another winter cue that can lead to a vernalized state. In Brachypodium distachyon, we find that natural variation for the ability of short days to confer competence to flower is due to allelic variation of the FLOWERING LOCUS T (FT1) paralog FT-like9 (FTL9). An active FTL9 allele is required for the acquisition of floral competence, demonstrating a novel role for a member of the FT family of genes. Loss of the short-day vernalization response appears to have arisen once in B. distachyon and spread through diverse lineages indicating that this loss has adaptive value, perhaps by delaying spring flowering until the danger of cold damage to flowers has subsided.},
doi = {10.7554/eLife.42153},
journal = {eLife},
number = ,
volume = 8,
place = {United States},
year = {Tue Jan 08 00:00:00 EST 2019},
month = {Tue Jan 08 00:00:00 EST 2019}
}
Web of Science
Works referenced in this record:
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
TASSEL: software for association mapping of complex traits in diverse samples
journal, June 2007
- Bradbury, P. J.; Zhang, Z.; Kroon, D. E.
- Bioinformatics, Vol. 23, Issue 19
Adaptation of barley to mild winters: A role for PPDH2
journal, January 2011
- Casao, M. Cristina; Karsai, Ildiko; Igartua, Ernesto
- BMC Plant Biology, Vol. 11, Issue 1
Expression analysis of vernalization and day-length response genes in barley (Hordeum vulgare L.) indicates that VRNH2 is a repressor of PPDH2 (HvFT3) under long days
journal, December 2010
- Casao, M. Cristina; Igartua, Ernesto; Karsai, Ildiko
- Journal of Experimental Botany, Vol. 62, Issue 6
Vernalization and its Relations to Dormancy
journal, June 1960
- Chouard, P.
- Annual Review of Plant Physiology, Vol. 11, Issue 1
FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis
journal, May 2007
- Corbesier, L.; Vincent, C.; Jang, S.
- Science, Vol. 316, Issue 5827
Effect of Photoperiod on the Regulation of Wheat Vernalization Genes VRN1 and VRN2
journal, March 2006
- Dubcovsky, Jorge; Loukoianov, Artem; Fu, Daolin
- Plant Molecular Biology, Vol. 60, Issue 4
Short Day Induction of Inflorescence Initiation in Some Winter Wheat Varieties
journal, January 1987
- Evans, Lt
- Functional Plant Biology, Vol. 14, Issue 3
The FLOWERING LOCUS T -Like Gene Family in Barley ( Hordeum vulgare )
journal, March 2007
- Faure, Sébastien; Higgins, Janet; Turner, Adrian
- Genetics, Vol. 176, Issue 1
The role of seasonal flowering responses in adaptation of grasses to temperate climates
journal, August 2014
- Fjellheim, Siri; Boden, Scott; Trevaskis, Ben
- Frontiers in Plant Science, Vol. 5
Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure
journal, December 2017
- Gordon, Sean P.; Contreras-Moreira, Bruno; Woods, Daniel P.
- Nature Communications, Vol. 8, Issue 1
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
Systematic Investigation of FLOWERING LOCUS T-Like Poaceae Gene Families Identifies the Short-Day Expressed Flowering Pathway Gene, TaFT3 in Wheat (Triticum aestivum L.)
journal, June 2016
- Halliwell, Joanna; Borrill, Philippa; Gordon, Anna
- Frontiers in Plant Science, Vol. 7
Control of flowering and reproduction in temperate grasses
journal, October 1994
- Heide, O. M.
- New Phytologist, Vol. 128, Issue 2
Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses
journal, April 2010
- Higgins, Janet A.; Bailey, Paul C.; Laurie, David A.
- PLoS ONE, Vol. 5, Issue 4
Molecular and Functional Characterization of PEBP Genes in Barley Reveal the Diversification of Their Roles in Flowering
journal, January 2009
- Kikuchi, Rie; Kawahigashi, Hiroyuki; Ando, Tsuyu
- Plant Physiology, Vol. 149, Issue 3
RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter × spring barley ( Hordeum vulgare L.) cross
journal, June 1995
- Laurie, D. A.; Pratchett, N.; Snape, J. W.
- Genome, Vol. 38, Issue 3
ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize
journal, July 2011
- Lazakis, Chloë M.; Coneva, Viktoriya; Colasanti, Joseph
- Journal of Experimental Botany, Vol. 62, Issue 14
DNA Polymorphism at the FRIGIDA Gene in Arabidopsis thaliana: Extensive Nonsynonymous Variation Is Consistent with Local Selection for Flowering Time
journal, August 2002
- Le Corre, Valérie; Roux, Fabrice; Reboud, Xavier
- Molecular Biology and Evolution, Vol. 19, Issue 8
An ortholog of CURLY LEAF / ENHANCER OF ZESTE like‐1 is required for proper flowering in Brachypodium distachyon
journal, February 2018
- Lomax, Aaron; Woods, Daniel P.; Dong, Yinxin
- The Plant Journal, Vol. 93, Issue 5
Characterization of FLOWERING LOCUS T1 (FT1) Gene in Brachypodium and Wheat
journal, April 2014
- Lv, Bo; Nitcher, Rebecca; Han, Xiuli
- PLoS ONE, Vol. 9, Issue 4
How to usefully compare homologous plant genes and chromosomes as DNA sequences: How to usefully compare plant genomes
journal, February 2008
- Lyons, Eric; Freeling, Michael
- The Plant Journal, Vol. 53, Issue 4
Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species: Gateway-compatible vectors for monocot transformation
journal, September 2011
- Mann, David G. J.; LaFayette, Peter R.; Abercrombie, Laura L.
- Plant Biotechnology Journal, Vol. 10, Issue 2
The FT -Like ZCN8 Gene Functions as a Floral Activator and Is Involved in Photoperiod Sensitivity in Maize
journal, March 2011
- Meng, Xin; Muszynski, Michael G.; Danilevskaya, Olga N.
- The Plant Cell, Vol. 23, Issue 3
Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum
journal, September 2011
- Murphy, R. L.; Klein, R. R.; Morishige, D. T.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 39, p. 16469-16474
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
An Antagonistic Pair of FT Homologs Mediates the Control of Flowering Time in Sugar Beet
journal, December 2010
- Pin, P. A.; Benlloch, R.; Bonnet, D.
- Science, Vol. 330, Issue 6009
Discrete Developmental Roles for Temperate Cereal Grass VERNALIZATION1 / FRUITFULL -Like Genes in Flowering Competency and the Transition to Flowering
journal, November 2007
- Preston, Jill C.; Kellogg, Elizabeth A.
- Plant Physiology, Vol. 146, Issue 1
Studies in Vernalisation of Cereals: I. A Comparative Study of Vernalisation of Winter Rye by Low Temperature and by Short Days
journal, October 1937
- Purvis, O. N.; Gregory, F. G.
- Annals of Botany, Vol. 1, Issue 4
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
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
INFLUENCE OF PHOTOPERIOD, SHORT-DAY VERNALIZATION, AND COLD VERNALIZATION ON DAYS TO HEADING IN AVENA SPECIES AND CULTIVARS
journal, July 1972
- Sampson, D. R.; Burrows, V. D.
- Canadian Journal of Plant Science, Vol. 52, Issue 4
Comparative plastome genomics and phylogenomics of Brachypodium : flowering time signatures, introgression and recombination in recently diverged ecotypes
journal, December 2017
- Sancho, Rubén; Cantalapiedra, Carlos P.; López-Alvarez, Diana
- New Phytologist, Vol. 218, Issue 4
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
Hd3a Protein Is a Mobile Flowering Signal in Rice
journal, May 2007
- Tamaki, S.; Matsuo, S.; Wong, H. L.
- Science, Vol. 316, Issue 5827
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
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
The FLC Locus: A Platform for Discoveries in Epigenetics and Adaptation
journal, October 2017
- Whittaker, Charles; Dean, Caroline
- Annual Review of Cell and Developmental Biology, Vol. 33, Issue 1
Three FLOWERING LOCUS T -like genes function as potential florigens and mediate photoperiod response in sorghum
journal, January 2016
- Wolabu, Tezera W.; Zhang, Fei; Niu, Lifang
- New Phytologist, Vol. 210, Issue 3
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
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
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
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
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
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
Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice
journal, May 2008
- Xue, Weiya; Xing, Yongzhong; Weng, Xiaoyu
- Nature Genetics, Vol. 40, Issue 6
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
The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization
journal, March 2004
- Yan, L.
- Science, Vol. 303, Issue 5664
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
Transcriptomic and genome-wide association study reveal long noncoding RNAs responding to nitrogen deficiency in maize
journal, February 2021
- Ma, Peng; Zhang, Xiao; Luo, Bowen
- BMC Plant Biology, Vol. 21, Issue 1
Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure
text, January 2017
- Gordon, Sean P.; Contreras-Moreira, Bruno; Woods, Daniel P.
- Nature Publishing Group
Works referencing / citing this record:
Evolutionary processes from the perspective of flowering time diversity
journal, October 2019
- Gaudinier, Allison; Blackman, Benjamin K.
- New Phytologist, Vol. 225, Issue 5
Fine-tuning of the flowering time control in winter barley: the importance of HvOS2 and HvVRN2 in non-inductive conditions
journal, March 2019
- Monteagudo, Arantxa; Igartua, Ernesto; Contreras-Moreira, Bruno
- BMC Plant Biology, Vol. 19, Issue 1
Effect of phyB and phyC loss-of-function mutations on the wheat transcriptome under short and long day photoperiods
journal, June 2020
- Kippes, Nestor; VanGessel, Carl; Hamilton, James
- BMC Plant Biology, Vol. 20, Issue 1
In Vitro Tissue Culture in Brachypodium: Applications and Challenges
journal, February 2020
- Betekhtin, Alexander; Hus, Karolina; Rojek-Jelonek, Magdalena
- International Journal of Molecular Sciences, Vol. 21, Issue 3