Flowering time regulation: photoperiod- and temperature-sensing in leaves.

Plants monitor changes in photoperiod and temperature to synchronize their flowering with seasonal changes to maximize fitness. In the Arabidopsis photoperiodic flowering pathway, the circadian clock-regulated components, such as FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 and CONSTANS, both of which have light-controlled functions, are crucial to induce the day-length specific expression of the FLOWERING LOCUS T (FT) gene in leaves. Recent advances indicate that FT transcriptional regulation is central for integrating the information derived from other important internal and external factors, such as developmental age, amount of gibberellic acid, and the ambient temperature. In this review, we describe how these factors interactively regulate the expression of FT, the main component of florigen, in leaves.

[1]  G. Coupland,et al.  Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. , 2009, Developmental cell.

[2]  Dmitri A. Nusinow,et al.  FKF1 and GIGANTEA Complex Formation Is Required for Day-Length Measurement in Arabidopsis , 2007, Science.

[3]  G. Coupland,et al.  Distinct Roles of GIGANTEA in Promoting Flowering and Regulating Circadian Rhythms in Arabidopsis , 2005, The Plant Cell Online.

[4]  A. Fitter,et al.  Rapid Changes in Flowering Time in British Plants , 2002, Science.

[5]  Young Hun Song,et al.  Isolation of CONSTANS as a TGA4/OBF4 interacting protein. , 2008, Molecules and cells.

[6]  C. Helliwell,et al.  Regulation of flowering time and floral patterning by miR172. , 2011, Journal of experimental botany.

[7]  T. Mockler,et al.  Regulation of photoperiodic flowering by Arabidopsis photoreceptors , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. van Zanten,et al.  High temperature acclimation through PIF4 signaling. , 2013, Trends in plant science.

[9]  Ji Hoon Ahn,et al.  Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis , 2010, Nucleic acids research.

[10]  Karine David,et al.  ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. , 2007, Nature.

[11]  S. Kay,et al.  FKF1 F-Box Protein Mediates Cyclic Degradation of a Repressor of CONSTANS in Arabidopsis , 2005, Science.

[12]  D. E. Somers,et al.  ELF4 regulates GIGANTEA chromatin access through subnuclear sequestration. , 2013, Cell reports.

[13]  W. Peng,et al.  The Effect of the Crosstalk between Photoperiod and Temperature on the Heading-Date in Rice , 2009, PloS one.

[14]  P. Huijser,et al.  The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 Module Regulates Ambient Temperature-Responsive Flowering via FLOWERING LOCUS T in Arabidopsis1[C][W][OA] , 2012, Plant Physiology.

[15]  Jae-Hoon Jung,et al.  SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the pri‐miR172a promoter in Arabidopsis , 2012, FEBS letters.

[16]  D. Weigel,et al.  Potent Induction of Arabidopsis thaliana Flowering by Elevated Growth Temperature , 2006, PLoS genetics.

[17]  J. Mathieu,et al.  Repression of Flowering by the miR172 Target SMZ , 2009, PLoS biology.

[18]  M. Mihara,et al.  Deciphering and Prediction of Transcriptome Dynamics under Fluctuating Field Conditions , 2012, Cell.

[19]  O. Nilsson,et al.  The multifaceted roles of FLOWERING LOCUS T in plant development. , 2012, Plant, cell & environment.

[20]  Jae-Hoon Jung,et al.  Arabidopsis RNA-binding Protein FCA Regulates MicroRNA172 Processing in Thermosensory Flowering* , 2012, The Journal of Biological Chemistry.

[21]  G. Coupland,et al.  Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. , 2002, The Plant journal : for cell and molecular biology.

[22]  Frank Küttner,et al.  Spatial control of flowering by DELLA proteins in Arabidopsis thaliana , 2012, Development.

[23]  T. Chiou,et al.  The role of the miR399-PHO2 module in the regulation of flowering time in response to different ambient temperatures in Arabidopsis thaliana , 2011, Molecules and cells.

[24]  Mariano J. Alvarez,et al.  A complementary role for ELF3 and TFL1 in the regulation of flowering time by ambient temperature. , 2009, The Plant journal : for cell and molecular biology.

[25]  Shinjiro Yamaguchi,et al.  Gibberellin metabolism and its regulation. , 2008, Annual review of plant biology.

[26]  Patrick Achard,et al.  Gibberellin signaling in plants , 2013, Development.

[27]  Yuanli Song,et al.  Interaction between temperature and photoperiod in regulation of flowering time in rice , 2012, Science China Life Sciences.

[28]  Fabio Fornara,et al.  FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis , 2007, Science.

[29]  Young Hun Song,et al.  CONSTANS and ASYMMETRIC LEAVES 1 complex is involved in the induction of FLOWERING LOCUS T in photoperiodic flowering in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[30]  Detlef Weigel,et al.  miR156-Regulated SPL Transcription Factors Define an Endogenous Flowering Pathway in Arabidopsis thaliana , 2009, Cell.

[31]  C. Pittendrigh,et al.  The Entrainment of Circadian Oscillations by Light and Their Role as Photoperiodic Clocks , 1964, The American Naturalist.

[32]  Yuehui He,et al.  Chromatin regulation of flowering. , 2012, Trends in plant science.

[33]  A. Califano,et al.  PFT1, the MED25 subunit of the plant Mediator complex, promotes flowering through CONSTANS dependent and independent mechanisms in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[34]  M. Schmid,et al.  Gibberellin Regulates the Arabidopsis Floral Transition through miR156-Targeted SQUAMOSA PROMOTER BINDING–LIKE Transcription Factors[W] , 2012, Plant Cell.

[35]  G. Coupland,et al.  Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods , 2012, Development.

[36]  Maitreya J. Dunham,et al.  Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis , 2000, Nature.

[37]  J. A. Jarillo,et al.  The Arabidopsis E3 Ubiquitin Ligase HOS1 Negatively Regulates CONSTANS Abundance in the Photoperiodic Control of Flowering[W] , 2012, Plant Cell.

[38]  Young Hun Song,et al.  FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis , 2012, Proceedings of the National Academy of Sciences.

[39]  Cristina Castillejo,et al.  The Balance between CONSTANS and TEMPRANILLO Activities Determines FT Expression to Trigger Flowering , 2008, Current Biology.

[40]  X. Deng,et al.  Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response , 2008, The EMBO journal.

[41]  Jianhua Zhu,et al.  Cold stress regulation of gene expression in plants. , 2007, Trends in plant science.

[42]  Mariko Sawa,et al.  GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana , 2011, Proceedings of the National Academy of Sciences.

[43]  M. Schmid,et al.  Regulation of flowering time: all roads lead to Rome , 2011, Cellular and Molecular Life Sciences.

[44]  Y. Sang,et al.  COP1-Mediated Ubiquitination of CONSTANS Is Implicated in Cryptochrome Regulation of Flowering in Arabidopsis[W] , 2008, The Plant Cell Online.

[45]  Gang Wu,et al.  Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3 , 2006, Development.

[46]  C. Fankhauser.  Faculty Opinions recommendation of Transcription factor PIF4 controls the thermosensory activation of flowering. , 2012 .

[47]  M. Schmid,et al.  The end of innocence: flowering networks explode in complexity. , 2012, Current opinion in plant biology.

[48]  C. Fankhauser,et al.  A molecular framework for light and gibberellin control of cell elongation , 2008, Nature.

[49]  Yan Zhang,et al.  NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. , 2010, The Plant journal : for cell and molecular biology.

[50]  C. Vincent,et al.  The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. , 2006, Genes & development.

[51]  K. Morris,et al.  DAY NEUTRAL FLOWERING Represses CONSTANS to Prevent Arabidopsis Flowering Early in Short Days[W][OA] , 2010, Plant Cell.

[52]  Y. Ogura,et al.  LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. , 2011, The Plant journal : for cell and molecular biology.

[53]  Jia Chen,et al.  AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress. , 2007, Journal of biochemistry and molecular biology.

[54]  Dong Chen,et al.  A Putative CCAAT-Binding Transcription Factor Is a Regulator of Flowering Timing in Arabidopsis1[C][W][OA] , 2007, Plant Physiology.

[55]  N. Chua,et al.  The GIGANTEA-Regulated MicroRNA172 Mediates Photoperiodic Flowering Independent of CONSTANS in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[56]  Daphne Vince-Prue,et al.  Photoperiodism in Plants , 1975 .

[57]  Cornelia Klose,et al.  EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana , 2011, Journal of experimental botany.

[58]  Jessika Adrian,et al.  Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability , 2006, Development.

[59]  R. Amasino,et al.  Vernalization: winter and the timing of flowering in plants. , 2009, Annual review of cell and developmental biology.

[60]  Yang Wu,et al.  A repressor complex governs the integration of flowering signals in Arabidopsis. , 2008, Developmental cell.

[61]  Young Hun Song,et al.  F-Box Proteins FKF1 and LKP2 Act in Concert with ZEITLUPE to Control Arabidopsis Clock Progression[C][W] , 2010, Plant Cell.

[62]  G. Coupland,et al.  The genetic basis of flowering responses to seasonal cues , 2012, Nature Reviews Genetics.

[63]  Jae-Hoon Jung,et al.  The E3 Ubiquitin Ligase HOS1 Regulates Arabidopsis Flowering by Mediating CONSTANS Degradation Under Cold Stress* , 2012, The Journal of Biological Chemistry.

[64]  Joonki Kim,et al.  The E3 ubiquitin ligase HOS1 regulates low ambient temperature-responsive flowering in Arabidopsis thaliana. , 2012, Plant & cell physiology.

[65]  M. Robertson,et al.  The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. , 2006, The Plant journal : for cell and molecular biology.

[66]  Andrew J. Millar,et al.  FKF1 Conveys Timing Information for CONSTANS Stabilization in Photoperiodic Flowering , 2012, Science.

[67]  Yan-chun Zhang,et al.  Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. , 2011, Genes & development.

[68]  S. Kay,et al.  FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis , 2003, Nature.

[69]  O. Ratcliffe,et al.  The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. , 2010, The New phytologist.

[70]  S. Park,et al.  Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. , 2007, Genes & development.

[71]  T. Kohchi,et al.  The Phytochrome-Interacting VASCULAR PLANT ONE–ZINC FINGER1 and VOZ2 Redundantly Regulate Flowering in Arabidopsis[C][W] , 2012, Plant Cell.

[72]  Chentao Lin,et al.  Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis , 2008, Science.

[73]  O. Ratcliffe,et al.  The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis , 2008, Planta.

[74]  T. Imaizumi,et al.  Arabidopsis circadian clock and photoperiodism: time to think about location. , 2010, Current opinion in plant biology.

[75]  B. Liu,et al.  Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. , 2011, Genes & development.

[76]  Michela Osnato,et al.  TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis , 2012, Nature Communications.

[77]  Ilha Lee,et al.  A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana , 2004, Nature Genetics.

[78]  G. Coupland,et al.  The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. , 2006, The Plant journal : for cell and molecular biology.

[79]  Xingliang Hou,et al.  FTIP1 Is an Essential Regulator Required for Florigen Transport , 2012, PLoS biology.

[80]  P. Wigge,et al.  H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis , 2010, Cell.

[81]  D. Weigel,et al.  A thermosensory pathway controlling flowering time in Arabidopsis thaliana , 2003, Nature Genetics.

[82]  Detlef Weigel,et al.  The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis , 2009, Cell.

[83]  Xuanming Liu,et al.  Blue Light-Dependent Interaction of CRY2 with SPA1 Regulates COP1 activity and Floral Initiation in Arabidopsis , 2011, Current Biology.

[84]  Christian Jung,et al.  Flowering time control and applications in plant breeding. , 2009, Trends in plant science.

[85]  F. Turck,et al.  CONSTANS and the CCAAT Box Binding Complex Share a Functionally Important Domain and Interact to Regulate Flowering of Arabidopsis[W][OA] , 2006, The Plant Cell Online.

[86]  D. Ravenscroft,et al.  Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering , 2004, Science.