DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: INDETERMINATE1 -mediated expression of FT family genes is required for proper timing of flowering in Brachypodium distachyon

Abstract

The transition to flowering is a major developmental switch in plants. In many temperate grasses, perception of indicators of seasonal change, such as changing day-length and temperature, leads to expression of FLOWERING LOCUS T1 ( FT1 ) and FT-Like ( FTL ) genes that are essential for promoting the transition to flowering. However, little is known about the upstream regulators of FT1 and FTL genes in temperate grasses. Here, we characterize the monocot-specific gene INDETERMINATE1 ( BdID1 ) in Brachypodium distachyon and demonstrate that BdID1 is a regulator of FT family genes. Mutations in ID1 impact the ability of the short-day (SD) vernalization, cold vernalization, and long-day (LD) photoperiod pathways to induce certain FTL genes. BdID1 is required for upregulation of FTL9 ( FT-LIKE9 ) expression by the SD vernalization pathway, and overexpression of FTL9 in an id1 background can partially restore the delayed flowering phenotype of id1 . We show that BdID1 binds in vitro to the promoter region of FTL genes suggesting that ID1 directly activates FTL expression. Transcriptome analysis shows that BdID1 is required for FT1 , FT2 , FTL12 , and FTL13 expression under inductive LD photoperiods, indicating that BdID1 is a regulator of the FTmore » gene family. Moreover, overexpression of FT1 in the id1 background results in rapid flowering similar to overexpressing FT1 in the wild type, demonstrating that BdID1 is upstream of FT family genes. Interestingly, ID1 negatively regulates a previously uncharacterized FTL gene, FTL4, and we show that FTL4 is a repressor of flowering. Thus, BdID1 is critical for proper timing of flowering in temperate grasses.« less

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [1]
  1. Department of Biochemistry, University of Wisconsin, Madison, WI 53706, Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, WI 53706
  2. Department of Biochemistry, University of Wisconsin, Madison, WI 53706, Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, WI 53706, Laboratory of Genetics, University of Wisconsin, Madison, WI 53706
  3. Department of Biochemistry, University of Wisconsin, Madison, WI 53706
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
2204900
Grant/Contract Number:  
SC0018409
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 Volume: 120 Journal Issue: 46; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Liu, Bing, Woods, Daniel P., Li, Weiya, and Amasino, Richard M. INDETERMINATE1 -mediated expression of FT family genes is required for proper timing of flowering in Brachypodium distachyon. United States: N. p., 2023. Web. doi:10.1073/pnas.2312052120.
Liu, Bing, Woods, Daniel P., Li, Weiya, & Amasino, Richard M. INDETERMINATE1 -mediated expression of FT family genes is required for proper timing of flowering in Brachypodium distachyon. United States. https://doi.org/10.1073/pnas.2312052120
Liu, Bing, Woods, Daniel P., Li, Weiya, and Amasino, Richard M. Tue . "INDETERMINATE1 -mediated expression of FT family genes is required for proper timing of flowering in Brachypodium distachyon". United States. https://doi.org/10.1073/pnas.2312052120.
@article{osti_2204900,
title = {INDETERMINATE1 -mediated expression of FT family genes is required for proper timing of flowering in Brachypodium distachyon},
author = {Liu, Bing and Woods, Daniel P. and Li, Weiya and Amasino, Richard M.},
abstractNote = {The transition to flowering is a major developmental switch in plants. In many temperate grasses, perception of indicators of seasonal change, such as changing day-length and temperature, leads to expression of FLOWERING LOCUS T1 ( FT1 ) and FT-Like ( FTL ) genes that are essential for promoting the transition to flowering. However, little is known about the upstream regulators of FT1 and FTL genes in temperate grasses. Here, we characterize the monocot-specific gene INDETERMINATE1 ( BdID1 ) in Brachypodium distachyon and demonstrate that BdID1 is a regulator of FT family genes. Mutations in ID1 impact the ability of the short-day (SD) vernalization, cold vernalization, and long-day (LD) photoperiod pathways to induce certain FTL genes. BdID1 is required for upregulation of FTL9 ( FT-LIKE9 ) expression by the SD vernalization pathway, and overexpression of FTL9 in an id1 background can partially restore the delayed flowering phenotype of id1 . We show that BdID1 binds in vitro to the promoter region of FTL genes suggesting that ID1 directly activates FTL expression. Transcriptome analysis shows that BdID1 is required for FT1 , FT2 , FTL12 , and FTL13 expression under inductive LD photoperiods, indicating that BdID1 is a regulator of the FT gene family. Moreover, overexpression of FT1 in the id1 background results in rapid flowering similar to overexpressing FT1 in the wild type, demonstrating that BdID1 is upstream of FT family genes. Interestingly, ID1 negatively regulates a previously uncharacterized FTL gene, FTL4, and we show that FTL4 is a repressor of flowering. Thus, BdID1 is critical for proper timing of flowering in temperate grasses.},
doi = {10.1073/pnas.2312052120},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 46,
volume = 120,
place = {United States},
year = {Tue Nov 07 00:00:00 EST 2023},
month = {Tue Nov 07 00:00:00 EST 2023}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.2312052120

Save / Share:

Works referenced in this record:

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, May 2016


Vernalization and epigenetics: how plants remember winter
journal, February 2004


Coordination of the Vernalization Response through a VIN3 and FLC Gene Family Regulatory Network in Arabidopsis    
journal, February 2013


PHYTOCHROME C regulation of photoperiodic flowering via PHOTOPERIOD1 is mediated by EARLY FLOWERING 3 in Brachypodium distachyon
journal, May 2023


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
  • DOI: 10.1038/35056041

Genome-Wide Analysis of the MADS-Box Gene Family in Brachypodium distachyon
journal, January 2014


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


The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update
journal, May 2018

  • Afgan, Enis; Baker, Dannon; Batut, Bérénice
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky379

A florigen paralog is required for short-day vernalization in a pooid grass
journal, January 2019


Ehd2 , a Rice Ortholog of the Maize INDETERMINATE1 Gene, Promotes Flowering by Up-Regulating Ehd1    
journal, September 2008

  • Matsubara, Kazuki; Yamanouchi, Utako; Wang, Zi-Xuan
  • Plant Physiology, Vol. 148, Issue 3
  • DOI: 10.1104/pp.108.125542

CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994

  • Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
  • Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
  • DOI: 10.1093/nar/22.22.4673

Regulation of flowering in temperate cereals
journal, April 2009


MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
journal, April 2007

  • Tamura, K.; Dudley, J.; Nei, M.
  • Molecular Biology and Evolution, Vol. 24, Issue 8
  • DOI: 10.1093/molbev/msm092

Florigen-Encoding Genes of Day-Neutral and Photoperiod-Sensitive Maize Are Regulated by Different Chromatin Modifications at the Floral Transition
journal, June 2015

  • Mascheretti, Iride; Turner, Katie; Brivio, Roberta S.
  • Plant Physiology, Vol. 168, Issue 4
  • DOI: 10.1104/pp.15.00535

Wheat VRN1, FUL2 and FUL3 play critical and redundant roles in spikelet development and spike determinacy
journal, July 2019

  • Li, Chengxia; Lin, Huiqiong; Chen, Andrew
  • Development, Vol. 146, Issue 14
  • DOI: 10.1242/dev.175398

A TILLING Platform for Functional Genomics in Brachypodium distachyon
journal, June 2013


Suppressor of rid1 (SID1) shares common targets with RID1 on florigen genes to initiate floral transition in rice
journal, February 2017


DELLA protein functions as a transcriptional activator through the DNA binding of the INDETERMINATE DOMAIN family proteins
journal, May 2014

  • Yoshida, Hideki; Hirano, Ko; Sato, Tomomi
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 21
  • DOI: 10.1073/pnas.1321669111

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

Epistatic interactions between PHOTOPERIOD1, CONSTANS1 and CONSTANS2 modulate the photoperiodic response in wheat
journal, July 2020


DELLAs Function as Coactivators of GAI-ASSOCIATED FACTOR1 in Regulation of Gibberellin Homeostasis and Signaling in Arabidopsis    
journal, July 2014

  • Fukazawa, Jutarou; Teramura, Hiroshi; Murakoshi, Satoru
  • The Plant Cell, Vol. 26, Issue 7
  • DOI: 10.1105/tpc.114.125690

Gene Ontology: tool for the unification of biology
journal, May 2000

  • Ashburner, Michael; Ball, Catherine A.; Blake, Judith A.
  • Nature Genetics, Vol. 25, Issue 1
  • DOI: 10.1038/75556

Florigen Coming of Age after 70 Years
journal, August 2006


Role of the INDETERMINATE DOMAIN Genes in Plants
journal, May 2019

  • Kumar, Manu; Le, Dung Thi; Hwang, Seongbin
  • International Journal of Molecular Sciences, Vol. 20, Issue 9
  • DOI: 10.3390/ijms20092286

Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome
journal, July 2004

  • Englbrecht, Claudia C.; Schoof, Heiko; Böhm, Siegfried
  • BMC Genomics, Vol. 5, Issue 1
  • DOI: 10.1186/1471-2164-5-39

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


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
  • DOI: 10.1105/tpc.110.081406

Maize floral regulator protein INDETERMINATE1 is localized to developing leaves and is not altered by light or the sink/source transition
journal, December 2006

  • Wong, A. Y. M.; Colasanti, J.
  • Journal of Experimental Botany, Vol. 58, Issue 3
  • DOI: 10.1093/jxb/erl206

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


The Gene Ontology resource: enriching a GOld mine
journal, December 2020

  • Carbon, Seth; Douglass, Eric; Good, Benjamin M.
  • Nucleic Acids Research, Vol. 49, Issue D1
  • DOI: 10.1093/nar/gkaa1113

Fast and accurate long-read alignment with Burrows–Wheeler transform
journal, January 2010


FLOWERING LOCUS T4delays flowering and decreases floret fertility in barley
journal, October 2020

  • Pieper, Rebecca; Tomé, Filipa; Pankin, Artem
  • Journal of Experimental Botany, Vol. 72, Issue 1
  • DOI: 10.1093/jxb/eraa466

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
  • DOI: 10.1186/1471-2229-11-164

Molecular and Phylogenetic Analyses of the Complete MADS-Box Transcription Factor Family in Arabidopsis: New Openings to the MADS World
journal, June 2003

  • Par̆enicová, Lucie; de Folter, Stefan; Kieffer, Martin
  • The Plant Cell, Vol. 15, Issue 7
  • DOI: 10.1105/tpc.011544

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

The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties
journal, March 2004


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


Distinct gene networks modulate floral induction of autonomous maize and photoperiod-dependent teosinte
journal, April 2018

  • Minow, Mark A. A.; Ávila, Luis M.; Turner, Katie
  • Journal of Experimental Botany, Vol. 69, Issue 12
  • DOI: 10.1093/jxb/ery110

Inheritance of Indeterminate Growth in Maize
journal, February 1946


Control of flowering and reproduction in temperate grasses
journal, October 1994


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

Floral Induction and Florigen
journal, May 1998


Divergent roles of FT-like 9 in flowering transition under different day lengths in Brachypodium distachyon
journal, February 2019


The genetic basis of flowering responses to seasonal cues
journal, August 2012

  • Andrés, Fernando; Coupland, George
  • Nature Reviews Genetics, Vol. 13, Issue 9
  • DOI: 10.1038/nrg3291

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

FLOWERING LOCUS T2 regulates spike development and fertility in temperate cereals
journal, October 2018

  • Shaw, Lindsay M.; Lyu, Bo; Turner, Rebecca
  • Journal of Experimental Botany, Vol. 70, Issue 1
  • DOI: 10.1093/jxb/ery350

Bulked-Segregant Analysis Coupled to Whole Genome Sequencing (BSA-Seq) for Rapid Gene Cloning in Maize
journal, September 2018

  • Klein, Harry; Xiao, Yuguo; Conklin, Phillip A.
  • G3: Genes|Genomes|Genetics, Vol. 8, Issue 11
  • DOI: 10.1534/g3.118.200499

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
  • DOI: 10.1038/s41467-017-02292-8

Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod
journal, December 2008


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

RID1 sets rice heading date by balancing its binding with SLR1 and SDG722
journal, January 2022

  • Zhang, Shuo; Deng, Li; Cheng, Rui
  • Journal of Integrative Plant Biology, Vol. 64, Issue 1
  • DOI: 10.1111/jipb.13196

Vernalization, Competence, and the Epigenetic Memory of Winter
journal, October 2004


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
  • DOI: 10.1073/pnas.1700536114

Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis
journal, July 2006

  • Cheng, Youfa; Dai, Xinhua; Zhao, Yunde
  • Genes & Development, Vol. 20, Issue 13
  • DOI: 10.1101/gad.1415106

Step by step evolution of Indeterminate Domain (IDD) transcriptional regulators: from algae to angiosperms
journal, March 2020

  • Prochetto, Santiago; Reinheimer, Renata
  • Annals of Botany, Vol. 126, Issue 1
  • DOI: 10.1093/aob/mcaa052

The florigen interactor BdES43 represses flowering in the model temperate grass Brachypodium distachyon
journal, January 2020

  • Cao, Shuanghe; Luo, Xumei; Xie, Li
  • The Plant Journal, Vol. 102, Issue 2
  • DOI: 10.1111/tpj.14622

PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools
journal, November 2018

  • Mi, Huaiyu; Muruganujan, Anushya; Ebert, Dustin
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1038

Overexpression of OsFTL10 induces early flowering and improves drought tolerance in Oryza sativa L.
journal, February 2019


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
  • DOI: 10.1104/pp.16.01161

A Chimeric IDD4 Repressor Constitutively Induces Immunity in Arabidopsis via the Modulation of Salicylic Acid and Jasmonic Acid Homeostasis
journal, April 2019

  • V�lz, Ronny; Kim, Soon-Kap; Mi, Jianing
  • Plant and Cell Physiology, Vol. 60, Issue 7
  • DOI: 10.1093/pcp/pcz057

OsFTL4, an FT-like Gene, Regulates Flowering Time and Drought Tolerance in Rice (Oryza sativa L.)
journal, September 2022


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


Global Analysis of DELLA Direct Targets in Early Gibberellin Signaling in Arabidopsis
journal, October 2007

  • Zentella, Rodolfo; Zhang, Zhong-Lin; Park, Mehea
  • The Plant Cell, Vol. 19, Issue 10
  • DOI: 10.1105/tpc.107.054999

The Sequence Alignment/Map format and SAMtools
journal, June 2009


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

RID1 , encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice
journal, September 2008

  • Wu, Changyin; You, Changjun; Li, Caishun
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 35
  • DOI: 10.1073/pnas.0806019105

High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3
journal, November 2007


Functional conservation and diversification of APETALA1/FRUITFULL genes in Brachypodium distachyon
journal, March 2016

  • Li, Qi; Wang, Ye; Wang, Fuxiang
  • Physiologia Plantarum, Vol. 157, Issue 4
  • DOI: 10.1111/ppl.12427

Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3
journal, January 2004


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


HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

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


Hd3a and RFT1 are essential for flowering in rice
journal, February 2008

  • Komiya, R.; Ikegami, A.; Tamaki, S.
  • Development, Vol. 135, Issue 4
  • DOI: 10.1242/dev.008631

H3K36 methyltransferase SDG708 enhances drought tolerance by promoting abscisic acid biosynthesis in rice
journal, March 2021

  • Chen, Kai; Du, Kangxi; Shi, Yichen
  • New Phytologist, Vol. 230, Issue 5
  • DOI: 10.1111/nph.17290