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Title: Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation?

Abstract

Similarities have long been recognized between vernalization, the prolonged exposure to cold temperatures that promotes the floral transition in many plants, and the chilling requirement to release bud dormancy in woody plants of temperate climates. In both cases the extended chilling period occurring during winter is used to coordinate developmental events to the appropriate seasonal time. However, whether or not these processes share common regulatory components and molecular mechanisms remain largely unknown. Both gene function and association genetics studies in Populus are beginning to answer this question. In Populus, studies have revealed that orthologs of the antagonistic flowering time genes FT and CEN/TFL1 might have central roles in both processes. We review Populus seasonal shoot development related to dormancy release and the floral transition and evidence for FT/TFL1 mediated regulation of these processes to consider the question of regulatory overlap. In addition, we discuss the potential for and challenges to integrating functional and population genomics studies to uncover the regulatory mechanisms underpinning these processes in woody plant systems.

Authors:
 [1];  [2];  [3];  [1]
  1. Virginia Polytechnic Institute and State University, Blacksburg, Virginia (United States). Department of Forest Resources and Environmental Conservation
  2. West Virginia Univ., Morgantown, WV (United States). Dept. of Biology
  3. Mississippi State Univ., Mississippi State, MS (United States). Institute for Genomics, Biocomputing and Biotechnology
Publication Date:
Research Org.:
Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1628269
Grant/Contract Number:  
SC0012574
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
Plant Sciences

Citation Formats

Brunner, Amy M., Evans, Luke M., Hsu, Chuan-Yu, and Sheng, Xiaoyan. Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation?. United States: N. p., 2014. Web. doi:10.3389/fpls.2014.00732.
Brunner, Amy M., Evans, Luke M., Hsu, Chuan-Yu, & Sheng, Xiaoyan. Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation?. United States. https://doi.org/10.3389/fpls.2014.00732
Brunner, Amy M., Evans, Luke M., Hsu, Chuan-Yu, and Sheng, Xiaoyan. Wed . "Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation?". United States. https://doi.org/10.3389/fpls.2014.00732. https://www.osti.gov/servlets/purl/1628269.
@article{osti_1628269,
title = {Vernalization and the chilling requirement to exit bud dormancy: shared or separate regulation?},
author = {Brunner, Amy M. and Evans, Luke M. and Hsu, Chuan-Yu and Sheng, Xiaoyan},
abstractNote = {Similarities have long been recognized between vernalization, the prolonged exposure to cold temperatures that promotes the floral transition in many plants, and the chilling requirement to release bud dormancy in woody plants of temperate climates. In both cases the extended chilling period occurring during winter is used to coordinate developmental events to the appropriate seasonal time. However, whether or not these processes share common regulatory components and molecular mechanisms remain largely unknown. Both gene function and association genetics studies in Populus are beginning to answer this question. In Populus, studies have revealed that orthologs of the antagonistic flowering time genes FT and CEN/TFL1 might have central roles in both processes. We review Populus seasonal shoot development related to dormancy release and the floral transition and evidence for FT/TFL1 mediated regulation of these processes to consider the question of regulatory overlap. In addition, we discuss the potential for and challenges to integrating functional and population genomics studies to uncover the regulatory mechanisms underpinning these processes in woody plant systems.},
doi = {10.3389/fpls.2014.00732},
journal = {Frontiers in Plant Science},
number = ,
volume = 5,
place = {United States},
year = {Wed Dec 17 00:00:00 EST 2014},
month = {Wed Dec 17 00:00:00 EST 2014}
}

Works referenced in this record:

Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar-dependent manner
journal, September 2011


FT Protein Acts as a Long-Range Signal in Arabidopsis
journal, June 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

Reproductive Development in Populus
book, December 2009


TERMINAL FLOWER1 Is a Mobile Signal Controlling Arabidopsis Architecture
journal, March 2007


Vernalization-Induced Trimethylation of Histone H3 Lysine 27 at FLC Is Not Maintained in Mitotically Quiescent Cells
journal, November 2007


Gated communities: apoplastic and symplastic signals converge at plasmodesmata to control cell fates
journal, August 2013

  • Stahl, Yvonne; Simon, Rüdiger
  • Journal of Experimental Botany, Vol. 64, Issue 17
  • DOI: 10.1093/jxb/ert245

Flowering responses to seasonal cues: what's new?
journal, October 2014

  • Romera-Branchat, Maida; Andrés, Fernando; Coupland, George
  • Current Opinion in Plant Biology, Vol. 21
  • DOI: 10.1016/j.pbi.2014.07.006

Control of inflorescence architecture in Antirrhinum
journal, February 1996

  • Bradley, Desmond; Carpenter, Rosemary; Copsey, Lucy
  • Nature, Vol. 379, Issue 6568
  • DOI: 10.1038/379791a0

Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014

  • Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
  • Nature Genetics, Vol. 46, Issue 10
  • DOI: 10.1038/ng.3075

Poplar FT2 Shortens the Juvenile Phase and Promotes Seasonal Flowering
journal, July 2006


Vernalization and its Relations to Dormancy
journal, June 1960


Shoot morphogenesis associated with flowering in Populus deltoides (Salicaceae)
journal, February 2003

  • Yuceer, C.; Land, S. B.; Kubiske, M. E.
  • American Journal of Botany, Vol. 90, Issue 2
  • DOI: 10.3732/ajb.90.2.196

Regulation of potato tuber sprouting
journal, October 2013


A Pair of Related Genes with Antagonistic Roles in Mediating Flowering Signals
journal, December 1999


Interlocking Feedback Loops Govern the Dynamic Behavior of the Floral Transition in Arabidopsis
journal, March 2013


Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate
journal, February 2010

  • Jiménez, S.; Reighard, G. L.; Bielenberg, D. G.
  • Plant Molecular Biology, Vol. 73, Issue 1-2
  • DOI: 10.1007/s11103-010-9608-5

Seasonal and developmental timing of flowering
journal, March 2010


Activation Tagging of the Floral Inducer FT
journal, December 1999


The FLOWERING LOCUS T/TERMINAL FLOWER 1 Family in Lombardy Poplar
journal, March 2008

  • Igasaki, Tomohiro; Watanabe, Yumiko; Nishiguchi, Mitsuru
  • Plant and Cell Physiology, Vol. 49, Issue 3
  • DOI: 10.1093/pcp/pcn010

PEP1 regulates perennial flowering in Arabis alpina
journal, April 2009

  • Wang, Renhou; Farrona, Sara; Vincent, Coral
  • Nature, Vol. 459, Issue 7245
  • DOI: 10.1038/nature07988

Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar
journal, November 2007

  • Rohde, Antje; Ruttink, Tom; Hostyn, Vanessa
  • Journal of Experimental Botany, Vol. 58, Issue 15-16
  • DOI: 10.1093/jxb/erm261

Plant dormancy in the perennial context
journal, May 2007


Floral Phenology and Morphology of Black Cottonwood, Populus trichocarpa (Salicaceae)
journal, May 1994

  • Boes, Teresa K.; Strauss, Steven H.
  • American Journal of Botany, Vol. 81, Issue 5
  • DOI: 10.2307/2445730

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

Control of inflorescence architecture in Antirrhinum
journal, February 1996

  • Bradley, Desmond; Carpenter, Rosemary; Copsey, Lucy
  • Nature, Vol. 379, Issue 6568
  • DOI: 10.1038/379791a0

FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar
journal, June 2011

  • Hsu, C. -Y.; Adams, J. P.; Kim, H.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 26
  • DOI: 10.1073/pnas.1104713108

Poplar FT2 Shortens the Juvenile Phase and Promotes Seasonal Flowering
journal, July 2006


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


The flowering hormone florigen functions as a general systemic regulator of growth and termination
journal, May 2009

  • Shalit, A.; Rozman, A.; Goldshmidt, A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 20
  • DOI: 10.1073/pnas.0810810106

Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge
journal, January 2010


Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses
journal, September 2014

  • Sager, R.; Lee, J. -Y.
  • Journal of Experimental Botany, Vol. 65, Issue 22
  • DOI: 10.1093/jxb/eru365

Molecular mechanisms of seed dormancy: Molecular mechanisms of seed dormancy
journal, June 2012


Leaf Dimorphism in Populus Trichocarpa
journal, October 1960


FT Protein Acts as a Long-Range Signal in Arabidopsis
journal, June 2007


TERMINAL FLOWER1 Is a Mobile Signal Controlling Arabidopsis Architecture
journal, March 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

High-density linkage mapping and evolution of paralogs and orthologs in Salix and Populus
journal, January 2010


Shoot morphogenesis associated with flowering in Populus deltoides (Salicaceae)
journal, February 2003

  • Yuceer, C.; Land, S. B.; Kubiske, M. E.
  • American Journal of Botany, Vol. 90, Issue 2
  • DOI: 10.3732/ajb.90.2.196

Common mechanisms regulate flowering and dormancy
journal, December 2009


The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy: Chilled AM restores its symplasmic network
journal, May 2001


Regulation of potato tuber sprouting
journal, October 2013


Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014

  • Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
  • Nature Genetics, Vol. 46, Issue 10
  • DOI: 10.1038/ng.3075

From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees
journal, December 2003

  • Howe, Glenn T.; Aitken, Sally N.; Neale, David B.
  • Canadian Journal of Botany, Vol. 81, Issue 12
  • DOI: 10.1139/b03-141

Gated communities: apoplastic and symplastic signals converge at plasmodesmata to control cell fates
journal, August 2013

  • Stahl, Yvonne; Simon, Rüdiger
  • Journal of Experimental Botany, Vol. 64, Issue 17
  • DOI: 10.1093/jxb/ert245

Plasmodesmata dynamics are coordinated by intracellular signaling pathways
journal, October 2013

  • Brunkard, Jacob O.; Runkel, Anne M.; Zambryski, Patricia C.
  • Current Opinion in Plant Biology, Vol. 16, Issue 5
  • DOI: 10.1016/j.pbi.2013.07.007

The flowering hormone florigen functions as a general systemic regulator of growth and termination
journal, May 2009

  • Shalit, A.; Rozman, A.; Goldshmidt, A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 20
  • DOI: 10.1073/pnas.0810810106

Reproductive Development in Populus
book, December 2009


Shoot meristems of deciduous woody perennials: self-organization and morphogenetic transitions
journal, February 2014

  • Paul, Laju K.; Rinne, Päivi LH; van der Schoot, Christiaan
  • Current Opinion in Plant Biology, Vol. 17
  • DOI: 10.1016/j.pbi.2013.11.009

Epigenetic regulation of bud dormancy events in perennial plants
journal, June 2014


FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar
journal, June 2011

  • Hsu, C. -Y.; Adams, J. P.; Kim, H.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 26
  • DOI: 10.1073/pnas.1104713108

Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar
journal, November 2007

  • Rohde, Antje; Ruttink, Tom; Hostyn, Vanessa
  • Journal of Experimental Botany, Vol. 58, Issue 15-16
  • DOI: 10.1093/jxb/erm261

PEP1 regulates perennial flowering in Arabis alpina
journal, April 2009

  • Wang, Renhou; Farrona, Sara; Vincent, Coral
  • Nature, Vol. 459, Issue 7245
  • DOI: 10.1038/nature07988

The FLOWERING LOCUS T/TERMINAL FLOWER 1 Family in Lombardy Poplar
journal, March 2008

  • Igasaki, Tomohiro; Watanabe, Yumiko; Nishiguchi, Mitsuru
  • Plant and Cell Physiology, Vol. 49, Issue 3
  • DOI: 10.1093/pcp/pcn010

The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Vernalization and its Relations to Dormancy
journal, June 1960


Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge
journal, January 2010


From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees
journal, December 2003

  • Howe, Glenn T.; Aitken, Sally N.; Neale, David B.
  • Canadian Journal of Botany, Vol. 81, Issue 12
  • DOI: 10.1139/b03-141

Activation Tagging of the Floral Inducer FT
journal, December 1999


Interlocking Feedback Loops Govern the Dynamic Behavior of the Floral Transition in Arabidopsis
journal, March 2013


Epigenetic regulation of bud dormancy events in perennial plants
journal, June 2014


The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms: Bud dormancy in trees
journal, July 2012


Vernalization-Induced Trimethylation of Histone H3 Lysine 27 at FLC Is Not Maintained in Mitotically Quiescent Cells
journal, November 2007


A Pair of Related Genes with Antagonistic Roles in Mediating Flowering Signals
journal, December 1999


Leaf Dimorphism in Populus Trichocarpa
journal, October 1960

  • Critchfield, William B.
  • American Journal of Botany, Vol. 47, Issue 8
  • DOI: 10.2307/2439521

Shoot meristems of deciduous woody perennials: self-organization and morphogenetic transitions
journal, February 2014

  • Paul, Laju K.; Rinne, Päivi LH; van der Schoot, Christiaan
  • Current Opinion in Plant Biology, Vol. 17
  • DOI: 10.1016/j.pbi.2013.11.009

Plasmodesmata dynamics are coordinated by intracellular signaling pathways
journal, October 2013

  • Brunkard, Jacob O.; Runkel, Anne M.; Zambryski, Patricia C.
  • Current Opinion in Plant Biology, Vol. 16, Issue 5
  • DOI: 10.1016/j.pbi.2013.07.007

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


Functional and Expressional Analyses of PmDAM Genes Associated with Endodormancy in Japanese Apricot
journal, July 2011

  • Sasaki, Ryuta; Yamane, Hisayo; Ooka, Tomomi
  • Plant Physiology, Vol. 157, Issue 1
  • DOI: 10.1104/pp.111.181982

Plant dormancy in the perennial context
journal, May 2007


Common mechanisms regulate flowering and dormancy
journal, December 2009


A common mechanism controls the life cycle and architecture of plants
journal, May 1998

  • Ratcliffe, Oliver J.; Amaya, Iraida; Vincent, Coral A.
  • Development, Vol. 125, Issue 9
  • DOI: 10.1242/dev.125.9.1609

Flowering responses to seasonal cues: what's new?
journal, October 2014

  • Romera-Branchat, Maida; Andrés, Fernando; Coupland, George
  • Current Opinion in Plant Biology, Vol. 21
  • DOI: 10.1016/j.pbi.2014.07.006

High-density linkage mapping and evolution of paralogs and orthologs in Salix and Populus
journal, January 2010


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

A common mechanism controls the life cycle and architecture of plants
journal, May 1998

  • Ratcliffe, Oliver J.; Amaya, Iraida; Vincent, Coral A.
  • Development, Vol. 125, Issue 9
  • DOI: 10.1242/dev.125.9.1609

Works referencing / citing this record:

Seasonal induction of alternative principal pathway for rose flower scent
journal, February 2016

  • Hirata, Hiroshi; Ohnishi, Toshiyuki; Tomida, Kensuke
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep20234

Chemical control of flowering time
journal, December 2016

  • Ionescu, Irina Alexandra; Møller, Birger Lindberg; Sánchez-Pérez, Raquel
  • Journal of Experimental Botany
  • DOI: 10.1093/jxb/erw427

Decoupling photo- and thermoperiod by projected climate change perturbs bud development, dormancy establishment and vernalization in the model tree Populus
journal, October 2018

  • Rinne, Päivi L. H.; Paul, Laju K.; van der Schoot, Christiaan
  • BMC Plant Biology, Vol. 18, Issue 1
  • DOI: 10.1186/s12870-018-1432-0

Evolution of Catkins: Inflorescence Morphology of Selected Salicaceae in an Evolutionary and Developmental Context
journal, December 2015

  • Cronk, Quentin C. B.; Needham, Isabelle; Rudall, Paula J.
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.01030

Beyond rest and quiescence (endodormancy and ecodormancy): A novel model for quantifying plant–environment interaction in bud dormancy release
journal, August 2019

  • Lundell, Robin; Hänninen, Heikki; Saarinen, Timo
  • Plant, Cell & Environment, Vol. 43, Issue 1
  • DOI: 10.1111/pce.13650

Energy and lipid metabolism during direct and diapause development in a pierid butterfly
journal, July 2016

  • Lehmann, Philipp; Pruisscher, Peter; Posledovich, Diana
  • The Journal of Experimental Biology, Vol. 219, Issue 19
  • DOI: 10.1242/jeb.142687

How fall dormancy benefits alfalfa winter-survival? Physiologic and transcriptomic analyses of dormancy process
journal, May 2019


Agronomic performance of Populus deltoides trees engineered for biofuel production
journal, November 2017

  • Macaya-Sanz, David; Chen, Jin‐Gui; Kalluri, Udaya C.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0934-6

Decoupling photo- and thermoperiod by projected climate change perturbs bud development, dormancy establishment and vernalization in the model tree Populus
journal, October 2018

  • Rinne, Päivi L. H.; Paul, Laju K.; van der Schoot, Christiaan
  • BMC Plant Biology, Vol. 18, Issue 1
  • DOI: 10.1186/s12870-018-1432-0

Agronomic performance of Populus deltoides trees engineered for biofuel production
journal, November 2017

  • Macaya-Sanz, David; Chen, Jin‐Gui; Kalluri, Udaya C.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0934-6

Herbivory and inbreeding affect growth, reproduction, and resistance in the rhizomatous offshoots of Solanum carolinense (Solanaceae)
journal, June 2019

  • Nihranz, Chad T.; Kolstrom, Rebecca L.; Kariyat, Rupesh R.
  • Evolutionary Ecology, Vol. 33, Issue 4
  • DOI: 10.1007/s10682-019-09997-w

Axillary buds are dwarfed shoots that tightly regulate GA pathway and GA-inducible 1,3-β-glucanase genes during branching in hybrid aspen
journal, October 2016

  • Rinne, Päivi L. H.; Paul, Laju K.; Vahala, Jorma
  • Journal of Experimental Botany, Vol. 67, Issue 21
  • DOI: 10.1093/jxb/erw352

Adaptive introgression and maintenance of a trispecies hybrid complex in range-edge populations of Populus
journal, September 2018

  • Chhatre, Vikram E.; Evans, Luke M.; DiFazio, Stephen P.
  • Molecular Ecology, Vol. 27, Issue 23
  • DOI: 10.1111/mec.14820

How fall dormancy benefits alfalfa winter-survival? Physiologic and transcriptomic analyses of dormancy process
journal, May 2019


Modulation of Dormancy and Growth Responses in Reproductive Buds of Temperate Trees
journal, September 2018

  • Lloret, Alba; Badenes, María Luisa; Ríos, Gabino
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01368