Skip to main content
Log in

Co-ordinated responses to endogenous and environmental triggers allow a well-timed floral transition in plants

  • Review
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

The initiation of flowering is a crucial event in the life cycle of plants. Flowering marks the transition of the plant from its vegetative to reproductive state. Flowers are shoot modifications derived from flower primordia, as a means of reproduction and securing seed production adopted by plants to transmit their genomic information across generations for the survival of the species. Floral transition is a consequence of the interplay between endogenous factors such as plant genetic structure, and exogenous factors such as photoperiod, temperature, and nutrients. The generic mechanism of flowering initiation is evolutionarily conserved across plant families. In addition, it is highly dependent on the genetic and physiological characteristics of individual species, in coordination with the surrounding environmental factors. Therefore, flowering control is extremely adaptable to seasonal changes, ensuring the reproductive success of the plant species. The genes involved in flowering control maintain a delicate balance orchestrated by different signalling mechanisms in response to the environmental cues. In this study, various mechanisms related to flowering are collectively demonstrated in terms of endogenous genetic cues responding to natural exogenous triggers and artificial inducers, including environmental factors and phytohormones, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AP1,2:

APATELLA 1,2

PI:

Pistillata

AG:

Agamous

TF1:

Terminal flower 1

LFY:

Leafy gene

CAL:

Cauliflower

FUL:

Fruitful

UFO:

Unusual floral organs

EF1:

Elongation factor 1

FT:

Flowering locus T

CO:

Constans

TSF1:

Twin sister of FT

F-BOX1:

F-box transcription factor

FKF1:

Flavin-binding Kelch repeat, F-box1

LOV:

Light, oxygen, voltage

GI:

Gigantea

CDF1:

Cyclin DOF factor 1

COP1:

Constitutive photomorphogenic 1

PRC 1&2:

Polycomb repressive complexes 1,2

NF-Y:

Nuclear factor Y

SAM:

Shoot apical meristem

FD:

Flowering locus D

FDP:

FD paralog

FLC:

Flowering locus D

MADS:

Initial letter if MCM1 agamous, deficiens

SOC1:

Suppressor of overexpression of CO1

COI1:

Coronatine insensitive 1

SPL15:

Squamosa promoter-binding-like protein 15

FCA:

Flowering control locus A

FY:

Flowering time control protein Y

FLK:

Flowering locus KH domain

LD:

Long day

FLD:

Flowering locus D

SD:

Short day

ZTL:

Zeitlupe

LKP2:

LOV Kelch protein 2

CCA1:

Circadian clock associated 1

LHY:

Late elongated hypocotyl

TOC1:

Timing of CAB expression 1

LUX:

Lux Arrythmo

ELF4:

Early flowering 4

EC:

Evening complex

PIF:

Phytochrome interacting factor

SVP:

Short vegetative phase, HOS1, high expression of osmotically responsive genes 1

ABA:

Abscisic acid

ABRE:

ABA-responsive element binding protein

ABFs:

ABRE-binding factors

FMT:

Friendly mitochondria

TFL1:

Terminal flower1

ABI3:

Abscisic acid insensitive 3

GAI:

GA insensitive;

RGA:

Repressor of GA1-3

RGL1:

RGA-like 1

NTL8:

Transmembrane motif 1- like 8

BFT:

Brother of FT

CRY1:

Cryptochrome 1

JA:

Jasmonic acid

ET:

Ethylene

RGL123:

RGA-like 1,2,3

SOC1:

MADS-box gene SOC1

MYB33:

Myeloblastosis 33

PIN1:

Peptidylproyl cis/trans isomerase NIMA interacting 1

PAT:

Phosphinothricin acetyl transferase

AIL:

Aintegumenta-like

PLT:

Plethora

ERF:

Ethylene-responsive factor

PYR:

Pyrabactin resistance

RCAR:

Regulatory components of ABA receptors

PP2Cs:

Type 2 C protein phosphatases

SnRK:

Snf1- related protein kinase

bZIP:

Basic leucine zipper

ABI:

Abscisic acid insensitive

AAC:

1-Aminocyclopropane-1-carboxylic acid

ACS:

AAC synthase

EIN3:

Ethylene sensitive 3

EIL:

EIN3- like

ATR1:

Altered tryptophan regulator 1

CTR1:

Coronatine insensitive 1

EBF 12:

EIN3-binding f box protein 1

SCFcoi1 E3:

SKP/Cullin1/F-box protein COI1 E3-ubiquitin-ligase complex

JAZ:

JASMONATE ZIM domain

bHLH-MYCs:

Basic helix–loop–helix-myelocytomatosis oncogenes

References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science(new York, NY) 311:91

    Article  CAS  Google Scholar 

  • Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alejandra Mandel M, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  Google Scholar 

  • Álvarez-Aragón R, Haro R, Benito B, Rodríguez-Navarro A (2016) Salt intolerance in Arabidopsis: shoot and root sodium toxicity, and inhibition by sodium-plus-potassium overaccumulation. Planta 243:97–114

    Article  PubMed  Google Scholar 

  • Amano T, Smithers RJ, Sparks TH, Sutherland WJ (2010) A 250-year index of first flowering dates and its response to temperature changes. Proc R Soc B 277:2451–2457

    Article  PubMed  PubMed Central  Google Scholar 

  • An H, Roussot C, Suárez-López P, Corbesier L, Vincent C, Piñeiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004a) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615

    Article  CAS  PubMed  Google Scholar 

  • An H, Roussot C, Suárez-López P, Corbesier L, Vincent C, Piñeiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004b) Constans acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development (cambridge, England) 131:3615–3626

    Article  CAS  Google Scholar 

  • Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2:e106

    Article  PubMed  PubMed Central  Google Scholar 

  • Bäurle I, Dean C (2008) Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE 3:e2733

    Article  PubMed  PubMed Central  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  Google Scholar 

  • Chandler JW (2009) Local auxin production: a small contribution to a big field. BioEssays 31:60–70

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Cho HJ, Kim JJ, Lee JH, Kim W, Jung JH, Park CM, Ahn JH (2012) Short vegetative phase (SVP) protein negatively regulates miR172 transcription via direct binding to the pri-miR172a promoter in Arabidopsis. FEBS Lett 586:2332–2337

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Hyun Y, Kang MJ, In Yun H, Yun JY, Lister C, Dean C, Amasino RM, Noh B, Noh YS, Choi Y (2009) Resetting and regulation of flowering locus C expression during Arabidopsis reproductive development. Plant J 57:918–931

    Article  CAS  PubMed  Google Scholar 

  • Chuang T-H, Li K-H, Li P-F, Yang C-H (2018) Functional analysis of an APETALA1-like MADS box gene from Eustoma grandiflorum in regulating floral transition and formation. Plant Biotechnol Rep 12:115–125

    Article  Google Scholar 

  • Chung KS, Yoo SY, Yoo SJ, Lee JS, Ahn JH (2010) Brother of FT and TFL1 (BFT), a member of the FT/TFL1 family, shows distinct pattern of expression during the vegetative growth of Arabidopsis. Plant Signal Behav 5:1102–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  CAS  PubMed  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science (new York, NY) 316:1030–1033

    Article  CAS  Google Scholar 

  • Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:e222

    Article  PubMed  PubMed Central  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • de Folter S, Immink RG, Kieffer M, Parenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17:1424–1433

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES (2011) Flowering locus C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA 108:6680–6685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dill A, Sun T-P (2001a) Synergistic derepression of Gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dill A, Sun T-P (2001b) Synergistic derepression of Gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2006) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA 103:236–241

    Article  CAS  PubMed  Google Scholar 

  • Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72:673–689

    Article  CAS  PubMed  Google Scholar 

  • Fernández V, Takahashi Y, Le Gourrierec J, Coupland G (2016) Photoperiodic and thermosensory pathways interact through Constans to promote flowering at high temperature under short days. Plant J 86:426–440

    Article  PubMed  Google Scholar 

  • Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000a) Redundant regulation of meristem identity and plant architecture by Fruitfull, Apetala1 and Cauliflower. Development 127:725

    Article  CAS  PubMed  Google Scholar 

  • Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000b) Redundant regulation of meristem identity and plant architecture by Fruitfull, Apetala1 and Cauliflower. Development 127:725–734

    Article  CAS  PubMed  Google Scholar 

  • Galvão VC, Collani S, Horrer D, Schmid M (2015) Gibberellic acid signaling is required for ambient temperature-mediated induction of flowering in Arabidopsis thaliana. Plant J 84:949–962

    Article  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science (new York, NY) 282:2226

    Article  Google Scholar 

  • Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-P, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 Gibberellin receptors in Arabidopsis. Plant Cell 18:3399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu X, Le C, Wang Y, Li Z, Jiang D, Wang Y, He Y (2013) Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat Commun 4:1947

    Article  PubMed  Google Scholar 

  • Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677

    Article  CAS  PubMed  Google Scholar 

  • Gusmaroli G, Tonelli C, Mantovani R (2001) Regulation of the CCAAT-Binding NF-Y subunits in Arabidopsis thaliana. Gene 264:173–185

    Article  CAS  PubMed  Google Scholar 

  • He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science (new York, NY) 302:1751–1754

    Article  CAS  Google Scholar 

  • Henderson IR, Liu F, Drea S, Simpson GG, Dean C (2005) An allelic series reveals essential roles for FY in plant development in addition to flowering-time control. Development (cambridge, England) 132:3597–3607

    Article  CAS  Google Scholar 

  • Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science (new York, NY) 331:76

    Article  CAS  Google Scholar 

  • Hornyik C, Terzi LC, Simpson GG (2010) The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18:203–213

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Nusinow DA (2016) Into the evening: complex interactions in the Arabidopsis circadian clock. Trends Genet 32:674–686

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Pérez-García P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science (new York, NY) 336:75–79

    Article  CAS  Google Scholar 

  • Hwang K, Susila H, Nasim Z, Jung J-Y, Ahn JH (2019) Arabidopsis ABF3 and ABF4 transcription factors act with the NF-YC complex to regulate SOC1 expression and mediate drought-accelerated flowering. Mol Plant 12:489–505

    Article  CAS  PubMed  Google Scholar 

  • Jagadish SV, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PV, Craufurd PQ (2016) Implications of high temperature and elevated CO2 on flowering time in plants. Front Plant Sci 7:913

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Wang Y, Wang Y, He Y (2008) Repression of Flowering Locus C and Flowering Locus T by the Arabidopsis polycomb repressive complex 2 components. PLoS ONE 3:e3404

    Article  PubMed  PubMed Central  Google Scholar 

  • Jung JH, Seo PJ, Park CM (2012) The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. J Biol Chem 287:43277–43287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7:e1002021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khanale V, Bhattacharya A, Satpute R, Char B (2021) Brief bioinformatics identification of cotton bZIP transcription factors family from Gossypium hirsutum, Gossypium arboreum and Gossypium raimondii. Plant Biotechnol Rep 15:493–511

    Article  Google Scholar 

  • Kim SG, Park CM (2007) Membrane-mediated salt stress signaling in flowering time control. Plant Signal Behav 2:517–518

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim S, Choi K, Park C, Hwang H-J, Lee I (2006) Suppressor of FRIGIDA4, encoding a C2H2-Type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis Flowering Locus C. Plant Cell 18:2985–2998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J-S, Seo S-G, Jun B-K, Lee Y, Jeon SB, Choe J, Kim J-B, Kim ST, Kim S-H (2011) An IbEF1 from sweet potato promotes flowering in transgenic tobacco. Genes Genom 33:335–341

    Article  CAS  Google Scholar 

  • Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microRNA156-squamosa promoter binding protein-LIKE3 module regulates ambient temperature-responsive flowering via Flowering Locus T in Arabidopsis. Plant Physiol 159:461–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wiśniewska J, Paciorek T, Benková E, Friml J (2008) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Peeters AJ (1998) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148:885–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krizek B (2009) Aintegumenta and Aintegumenta-Like6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150:1916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147

    Article  CAS  PubMed  Google Scholar 

  • Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, Hempel FD, Ratcliffe OJ (2008) 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. Planta 228:709–723

    Article  CAS  PubMed  Google Scholar 

  • la Rosa NM-d, Sotillo B, Miskolczi P, Gibbs DJ, Vicente J, Carbonero P, Oñate-Sánchez L, Holdsworth MJ, Bhalerao R, Alabadí D, Blázquez MA (2014) Large-scale identification of Gibberellin-related transcription factors defines group VII Ethylene Response Factors as functional DELLA partners. Plant Physiol 166:1022–1032

    Article  PubMed Central  Google Scholar 

  • Langridge J (1957) Effect of day-length and Gibberellic acid on the flowering of Arabidopsis. Nature 180:36–37

    Article  CAS  Google Scholar 

  • Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994) Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Plant Cell 6:75–83

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38:3081–3093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JH, Ryu H-S, Chung KS, Posé D, Kim S, Schmid M, Ahn JH (2013) Regulation of temperature-responsive flowering by MADS-Box transcription factor repressors. Science 342:628–632

    Article  CAS  PubMed  Google Scholar 

  • Li K, Wang Y, Han C, Zhang W, Jia H, Li X (2007) GA signaling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana. Plant Growth Regul 53:195–206

    Article  CAS  Google Scholar 

  • Liu H, Stone SL (2010a) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22:2630–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Stone SL (2010b) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22:2630–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28:398–407

    Article  PubMed  Google Scholar 

  • Liu T, Li Y, Ren J, Qian Y, Yang X, Duan W, Hou X (2013) Nitrate or NaCl regulates floral induction in Arabidopsis thaliana. Biologia 68:215–222

    Article  CAS  Google Scholar 

  • Lutz U, Posé D, Pfeifer M, Gundlach H, Hagmann J, Wang C, Weigel D, Mayer KF, Schmid M, Schwechheimer C (2015) Modulation of ambient temperature-dependent flowering in Arabidopsis thaliana by natural variation of Flowering Locus M. PLoS Genet 11:e1005588

    Article  PubMed  PubMed Central  Google Scholar 

  • Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89:737–745

    Article  CAS  PubMed  Google Scholar 

  • Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524

    Article  CAS  PubMed  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  CAS  PubMed  Google Scholar 

  • Mockler TC, Yu X, Shalitin D, Parikh D, Michael TP, Liou J, Huang J, Smith Z, Alonso JM, Ecker JR, Chory J, Lin C (2004) Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc Natl Acad Sci USA 101:12759–12764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon J, Suh S-S, Lee H, Choi K-R, Hong CB, Paek N-C, Kim S-G, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623

    Article  CAS  PubMed  Google Scholar 

  • Nole-Wilson S, Tranby TL, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57:613–628

    Article  CAS  PubMed  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paltiel J, Amin R, Gover A, Ori N, Samach A (2006) Novel roles for GIGANTEA revealed under environmental conditions that modify its expression in Arabidopsis and Medicago truncatula. Planta 224:1255–1268

    Article  CAS  PubMed  Google Scholar 

  • Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566

    Article  CAS  PubMed  Google Scholar 

  • Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the Jasmonate signaling cascade. Plant Cell 23:3089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  CAS  PubMed  Google Scholar 

  • Posé D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC, Immink RG, Schmid M (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503:414–417

    Article  PubMed  Google Scholar 

  • Riboni M, Galbiati M, Tonelli C, Conti L (2013) GIGANTEA enables drought escape response via abscisic acid-dependent activation of the Florigens and Suppressor of Overexpression of Constans. Plant Physiol 162:1706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riboni M, Robustelli Test A, Galbiati M, Tonelli C, Conti L (2016) ABA-dependent control of GIGANTEA signalling enables drought escape via up-regulation of Flowering Locus T in Arabidopsis thaliana. J Exp Bot 67:6309–6322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Cazorla E, Ripoll JJ, Andújar A, Bailey LJ, Martínez-Laborda A, Yanofsky MF, Vera A (2015) K-homology nuclear ribonucleoproteins regulate floral organ identity and determinacy in Arabidopsis. PLoS Genet 11:e1004983

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryu JY, Park C-M, Seo PJ (2011) The floral repressor Brother of FT and TFL1 (BFT) modulates flowering initiation under high salinity in Arabidopsis. Mol Cells 32:295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salisbury FB, Marinos NG (1985) The ecological role of plant growth substances. In: Pharis RP, Reid DM (eds) Hormonal regulation of development III: role of environmental factors. Springer, Berlin Heidelberg, pp 707–766

    Chapter  Google Scholar 

  • Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229

    Article  CAS  PubMed  Google Scholar 

  • Schomburg FM, Patton DA, Meinke DW, Amasino RM (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13:1427–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin JM, Seo S-G, Kim J-S, Jang H, Shin M-R, Lee C, Kim S-H (2015) Ectopic expression of NtEF1 and NtEF2 promotes flowering and alters floral organ identity in Nicotiana tabacum. Plant Biotechnol Rep 9:11–26

    Article  Google Scholar 

  • Shu K, Chen Q, Wu Y, Liu R, Zhang H, Wang S, Tang S, Yang W, Xie Q (2016) Abscisic acid-insensitive 4 negatively regulates flowering through directly promoting Arabidopsis Flowering Locus C transcription. J Exp Bot 67:195–205

    Article  CAS  PubMed  Google Scholar 

  • Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C (2003) FY is an RNA 3’ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113:777–787

    Article  CAS  PubMed  Google Scholar 

  • Siriwardana NS, Lamb RS (2012) The poetry of reproduction: the role of LEAFY in Arabidopsis thaliana flower formation. Int J Dev Biol 56:207–221

    Article  CAS  PubMed  Google Scholar 

  • Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for Constans stabilization in photoperiodic flowering. Science (new York, NY) 336:1045–1049

    Article  CAS  Google Scholar 

  • Song J, Irwin J, Dean C (2013) Remembering the prolonged cold of winter. Curr Biol 23:R807–R811

    Article  CAS  PubMed  Google Scholar 

  • Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) Constans mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  PubMed  Google Scholar 

  • Talbert PB, Henikoff S (2014) Environmental responses mediated by histone variants. Trends Cell Biol 24:642–650

    Article  CAS  PubMed  Google Scholar 

  • Tejos R, Rodriguez-Furlán C, Adamowski M, Sauer M, Norambuena L, Friml J (2018) PATELLINS are regulators of auxin-mediated PIN1 relocation and plant development in Arabidopsis thaliana. J Cell Sci 131(2)

  • Tiwari SB, Shen Y, Chang HC, Hou Y, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C, Belachew A, Repetti PP, Reuber TL, Ratcliffe OJ (2010) The flowering time regulator Constans is recruited to the Flowering Locus T promoter via a unique cis-element. New Phytol 187:57–66

    Article  CAS  PubMed  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8

  • Wada KC, Takeno K (2010) Stress-induced flowering. Plant Signal Behav 5:944–947

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner D, Sablowski RWM, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by Leafy. Science (new York, NY) 285:582

    Article  CAS  Google Scholar 

  • Wang ZY, Tobin EM (1998) Constitutive expression of the Circadian clock associated 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–1217

    Article  CAS  PubMed  Google Scholar 

  • Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li L, Ye T, Lu Y, Chen X, Wu Y (2013) The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J Exp Bot 64:675–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859

    Article  CAS  PubMed  Google Scholar 

  • Wigge PA (2013) Ambient temperature signalling in plants. Curr Opin Plant Biol 16:661–666

    Article  CAS  PubMed  Google Scholar 

  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos Transact R Soc B 365:2093–2106

    Article  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development (cambridge, England) 133:3539–3547

    Article  CAS  PubMed Central  Google Scholar 

  • Xi W, Liu C, Hou X, Yu H (2010) MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 22:1733–1748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2015) Omics approaches toward defining the comprehensive abscisic acid signaling network in plants. Plant Cell Physiol 56:1043–1052

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Xu Y, Tan EL, Kumar PP (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci 99:16336–16341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan S, Zhang Z-W, Zheng C, Zhao Z-Y, Wang Y, Feng L-Y, Niu G, Wang C-Q, Wang J-H, Feng H, Xu F, Bao F, Hu Y, Cao Y, Ma L, Wang H, Kong D-D, Xiao W, Lin H-H, He Y (2016) Arabidopsis cryptochrome 1 functions in nitrogen regulation of flowering. Proc Natl Acad Sci 113:7661–7666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai Q, Zhang X, Wu F, Feng H, Deng L, Xu L, Zhang M, Wang Q (2015) Transcriptional mechanism of Jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27:2814–2828

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Garreton V, Chua NH (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19:1532–1543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Jin Y, Hao H, Liang S, Ma X, Luan W (2020) Characterization and identification of OsFTL8 gene in rice. Plant Biotechnol Rep 14:683–694

    Article  Google Scholar 

Download references

Acknowledgements

This research was funded by the New Breeding Technologies Development Program (No. PJ01485802), Rural Development Administration, Republic of Korea. The permission to use Fig. 4 in this manuscript has been granted (Moon et al. 2003).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geung-Joo Lee.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaur, C., Lim, Y.P. & Lee, GJ. Co-ordinated responses to endogenous and environmental triggers allow a well-timed floral transition in plants. Plant Biotechnol Rep 16, 145–159 (2022). https://doi.org/10.1007/s11816-021-00731-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-021-00731-z

Keywords

Navigation