Skip to main content
SpringerLink
Log in

A survey of flowering genes reveals the role of gibberellins in floral control in rose

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Exhaustive studies on flowering control in annual plants have provided a framework for exploring this process in other plant species, especially in perennials for which little molecular data are currently available. Rose is a woody perennial plant with a particular flowering strategy—recurrent blooming, which is controlled by a recessive locus (RB). Gibberellins (GA) inhibit flowering only in non-recurrent roses. Moreover, the GA content varies during the flowering process and between recurrent and non-recurrent rose. Only a few rose genes potentially involved in flowering have been described, i.e. homologues of ABC model genes and floral genes from EST screening. In this study, we gained new information on the molecular basis of rose flowering: date of flowering and recurrent blooming. Based on a candidate gene strategy, we isolated genes that have similarities with genes known to be involved in floral control in Arabidopsis (GA pathway, floral repressors and integrators). Candidate genes were mapped on a segregating population, gene expression was studied in different organs and transcript abundance was monitored in growing shoot apices. Twenty-five genes were studied. RoFT, RoAP1 and RoLFY are proposed to be good floral markers. RoSPY and RB co-localized in our segregating population. GA metabolism genes were found to be regulated during floral transition. Furthermore, GA signalling genes were differentially regulated between a non-recurrent rose and its recurrent mutant. We propose that flowering gene networks are conserved between Arabidopsis and rose. The GA pathway appears to be a key regulator of flowering in rose. We postulate that GA metabolism is involved in floral initiation and GA signalling might be responsible for the recurrent flowering character.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    PubMed  CAS  Google Scholar 

  • Al-Humaid AI (2003) Effects of benzyladenine on the growth and the flowering of Sntrix rose. Egyp J Hortic 30:151–161

    Google Scholar 

  • Araki T (2001) Transition from vegetative to reproductive phase. Curr Opin Plant Biol 4:63–68

    PubMed  CAS  Google Scholar 

  • Aubert D, Chen L, Moon YH, Martin D, Castle LA, Yang CH, Sung ZR (2001) EMF1, a novel protein involved in the control of shoot architecture and flowering in Arabidopsis. Plant Cell 13:1865–1875

    PubMed  CAS  Google Scholar 

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    PubMed  CAS  Google Scholar 

  • Battey NH, Miere Pl, Tehranifar A, Cekic C, Taylor S, Shrives KJ, Hadley P, Greenland AJ, Darby J, Wilkinson MJ (1998) Genetic and environmental control of flowering in strawberry. In: Cockshull KE, Gray D, Seymour GB, Thomas B (ed) Genetic and environmental manipulation of horticultural crops, CAB international, Wallingford, UK, pp 111–131

  • Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    PubMed  CAS  Google Scholar 

  • Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    PubMed  CAS  Google Scholar 

  • Blazquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404:889–892

    PubMed  CAS  Google Scholar 

  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850

    PubMed  CAS  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31

    PubMed  CAS  Google Scholar 

  • Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83

    PubMed  CAS  Google Scholar 

  • Cao D, Cheng H, Wu W, Soo HM, Peng J (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142:509–525

    PubMed  CAS  Google Scholar 

  • Carmona MJ, Cubas P, Calonje M, Martinez-Zapater JM (2007) Flowering transition in grapevine (Vitis vinifera L.). Can J Bot 85:701–711

    CAS  Google Scholar 

  • Chakradhar M, Khiratkar SD (2004) Growth and flowering responses of rose cv. Gladiator to certain growth regulant sprays. Orissa J Hortic 32:112–115

    Google Scholar 

  • Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064

    PubMed  CAS  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 316:1030–1033

    PubMed  CAS  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890

    PubMed  CAS  Google Scholar 

  • Crespel L, Chirollet M, Durel CE, Zhang D, Meynet J, Gudin S (2002) Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theor Appl Genet 105:1207–1214

    PubMed  CAS  Google Scholar 

  • Creste S, Neto A, Figueira A (2001) Detection of single sequence repeat polymorphism in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep 19:299–306

    CAS  Google Scholar 

  • Diaz-Riquelme J, Lijavetzky D, Martinez-Zapater JM, Carmona MJ (2009) Genome-wide analysis of MIKCC-Type MADS box genes in grapevine. Plant Physiol 149:354–369

    PubMed  CAS  Google Scholar 

  • Eriksson S, Bohlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18:2172–2181

    PubMed  CAS  Google Scholar 

  • Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85

    PubMed  CAS  Google Scholar 

  • Foster T, Kirk C, Jones W, Allan A, Espley R, Karunairetnam S, Rakonjac J (2007) Characterisation of the DELLA subfamily in apple (Malus x domestica Borkh.). Tree Genet Genomes 3:187–197

    Google Scholar 

  • Foucher F, Chevalier M, Corre C, Soufflet-Freslon V, Legeai F, Hibrand-Saint Oyant L (2008) New resources for studying the rose flowering process. Genome 51:827–837

    PubMed  CAS  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    PubMed  CAS  Google Scholar 

  • Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, Lefebvre D, Grandjean O (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128:4847–4858

    PubMed  CAS  Google Scholar 

  • Gendall AR, Levy YY, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535

    PubMed  CAS  Google Scholar 

  • Gutierrez L, Mauriat M, Pelloux J, Bellini C, Van Wuytswinkel O (2008) Towards a systematic validation of references in real-time RT-PCR. Plant Cell 20:1734–1735

    PubMed  CAS  Google Scholar 

  • Hamès C, Ptchelkine D, Grimm D, Thevenon E, Moyroud E, Gérard F, Martiel JL, Benlloch R, Parcy F, Müller CW (2008) Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. EMBO J 27:2628–2637

    PubMed  Google Scholar 

  • Havely AH (1972) Phytohormones in flowering regulation of self-inductive plants. In: Gauthier-Villars (ed) Proceeding of the 18th international horticultural congress, Paris, pp 178–198

  • Hecht V, Foucher F, Ferrandiz C, Macknight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltran JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420–1434

    PubMed  CAS  Google Scholar 

  • Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530

    PubMed  CAS  Google Scholar 

  • Hibino Y, Kitahara K, Hirai S, Matsumoto S (2006) Structural and functional analysis of rose class B MADS-box genes MASAKO BP, euB3 and B3: paleo-type AP3 homologue MASAKO B3 association with petal development. Plant Sci 170:778–785

    CAS  Google Scholar 

  • Hibrand-Saint Oyant L, Crespel L, Rajapakse S, Zhang L, Foucher F (2008) Genetic linkage maps of rose constructed with new microsatellite markers and locating QTL controlling flowering traits. Tree Genet Genomes 4:11–23

    Google Scholar 

  • Horridge JS, Cockshull KE (1974) Flower initiation and development in the glasshouse rose. Scienta Horticulturae 2:274–284

    Google Scholar 

  • Hsu C-Y, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861

    PubMed  CAS  Google Scholar 

  • Igasaki T, Watanabe Y, Nishiguchi M, Kotoda N (2008) The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar. Plant Cell Physiol 49:291–300

    PubMed  CAS  Google Scholar 

  • Ikeda A, Yamamuro C, Yamaguchi J (2003) Gibberellin signaling factors; all about DELLA family. Regul Plant Growth Dev 38:36–47

    CAS  Google Scholar 

  • Izawa T (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58:3091–3097

    PubMed  CAS  Google Scholar 

  • Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120

    PubMed  CAS  Google Scholar 

  • Jack T (2001) Relearning our ABCs: new twists on an old model. Trends Plant Sci 6:310–316

    PubMed  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    PubMed  CAS  Google Scholar 

  • Jain R, Gomer RH, Murtagh JJ Jr (1992) Increasing specificity from the PCR-RACE technique. Biotechniques 12:58–59

    PubMed  CAS  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    PubMed  CAS  Google Scholar 

  • King RW, Evans LT, Mander LN, Moritz T, Pharis RP, Twitchin B (2003) Synthesis of gibberellin GA6 and its role in flowering of Lolium temulentum. Phytochemistry 62:77–82

    PubMed  CAS  Google Scholar 

  • King RW, Moritz T, Evans LT, Martin J, Andersen CH, Blundell C, Kardailsky I, Chandler PM (2006) Regulation of flowering in the long-day grass Lolium temulentum by gibberellins and the FLOWERING LOCUS T gene. Plant Physiol 141:498–507

    PubMed  CAS  Google Scholar 

  • Kitahara K, Matsumoto S (2000) Rose MADS-box genes ‘MASAKO C1 and D1’ homologous to class C floral identity genes. Plant Sci 151:121–134

    PubMed  CAS  Google Scholar 

  • Kitahara K, Hirai S, Fukui H, Matsumoto S (2001) Rose MADS-box genes ‘MASAKO BP and B3’ homologous to class B floral identity genes. Plant Sci 161:549–557

    CAS  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    PubMed  CAS  Google Scholar 

  • Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66

    PubMed  CAS  Google Scholar 

  • Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Gene Dev 16:646–658

    PubMed  CAS  Google Scholar 

  • Lee JH, Hong SM, Yoo SJ, Park OK, Lee JS, Ahn JH (2006) Integration of floral inductive signals by flowering locus T and suppressor of overexpression of CONSTANS 1. Physiol Plant 126:475–483

    CAS  Google Scholar 

  • Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243–246

    PubMed  CAS  Google Scholar 

  • Lewis R (1994) Investigation of mutants of Rosa that affect growth before flowering. Dissertation, University of East London

  • Lifschitz E, Eshed Y (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. J Exp Bot 57:3405–3414

    PubMed  CAS  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    PubMed  CAS  Google Scholar 

  • McDaniel CN, Hartnett LK (1996) Flowering as metamorphosis: two sequential signals regulate floral initiation in Lolium temulentum. Development 122:3661–3668

    PubMed  CAS  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130

    PubMed  CAS  Google Scholar 

  • McMillan CP, Blundell CA, King RW (2005) Flowering of the grass Lolium perenne. Effects of vernalization and long days on gibberellin biosynthesis and signaling. Plant Physiol 138:1794–1806

    Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    PubMed  CAS  Google Scholar 

  • Mimida N, Goto K, Kobayashi Y, Araki T, Ahn JH, Weigel D, Murata M, Motoyoshi F, Sakamoto W (2001) Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells 6:327–336

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Moon Y-H, Chen L, Pan RL, Chang H-S, Zhu T, Maffeo DM, Sung ZR (2003b) EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell 15:681–693

    PubMed  CAS  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:s111–s130

    PubMed  CAS  Google Scholar 

  • Nakajima M, Shimada A, Takashi Y, Kim Y-C, Park S-H, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M, Maeda T, Matsuoka M, Yamaguchi I (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889

    PubMed  CAS  Google Scholar 

  • Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    PubMed  CAS  Google Scholar 

  • Oh E, Yamaguchi S, Kamiya Y, Bae G, Chung WI, Choi G (2006) Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J 47:124–139

    PubMed  CAS  Google Scholar 

  • Okazaki K, Sakamoto K, Kikuchi R, Saito A, Togashi E, Kuginuki Y, Matsumoto S, Hirai M (2007) Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea. Theor Appl Genet 114:595–608

    PubMed  CAS  Google Scholar 

  • Onouchi H, Igeno MI, Perilleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12:885–900

    PubMed  CAS  Google Scholar 

  • Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551

    PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45

    PubMed  CAS  Google Scholar 

  • Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989

    PubMed  CAS  Google Scholar 

  • Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93

    PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615

    PubMed  CAS  Google Scholar 

  • Reeves PA, He Y, Schmitz RJ, Amasino RM, Panella LW, Richards CM (2007) Evolutionary conservation of the FLOWERING LOCUS C-mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176:295–307

    PubMed  CAS  Google Scholar 

  • Roberts AV, Blake PS, Lewis R, Taylor JM, Dunstan DI (1999) The effect of gibberellins on flowering in roses. J Plant Growth Regul 18:113–119

    PubMed  CAS  Google Scholar 

  • Rose T, Henikoff J, Henikoff S (2003) CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. Nucleic Acids Res 31:3763–3766

    PubMed  CAS  Google Scholar 

  • Rouse DT, Sheldon CC, Bagnall DJ, Peacock WJ, Dennis ES (2002) FLC, a repressor of flowering, is regulated by genes in different inductive pathways. Plant J 29:183–191

    PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653

    PubMed  CAS  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616

    PubMed  CAS  Google Scholar 

  • Semeniuk P (1971) Inheritance of recurrent blooming in Rosa wichuraiana. J Hered 62:203–204

    Google Scholar 

  • Sheldon CC, Finnegan EJ, Rouse DT, Tadege M, Bagnall DJ, Helliwell CA, Peacock WJ, Dennis ES (2000a) The control of flowering by vernalization. Curr Opin Plant Biol 3:418–422

    PubMed  CAS  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000b) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758

    PubMed  CAS  Google Scholar 

  • Sheldon CC, Finnegan EJ, Dennis ES, Peacock WJ (2006) Quantitative effects of vernalization on FLC and SOC1 expression. Plant J 45:871–883

    PubMed  CAS  Google Scholar 

  • Silverstone AL, Tseng T-S, Swain SM, Dill A, Jeong SY, Olszewski NE, Sun T-p (2007) Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis. Plant Physiol 143:987–1000

    PubMed  CAS  Google Scholar 

  • Simpson GG (2004) The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr Opin Plant Biol 7:570–574

    PubMed  CAS  Google Scholar 

  • Simpson GG, Dean C (2002) Flowering—Arabidopsis, the rosetta stone of flowering time? Science 296:285–289

    PubMed  CAS  Google Scholar 

  • Suarez-Lopez 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

    PubMed  CAS  Google Scholar 

  • Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164

    PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa. Science 313:1596–1604

    PubMed  CAS  Google Scholar 

  • Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun T-p (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019

    PubMed  CAS  Google Scholar 

  • Udvardi MK, Czechowski T, Scheible W-R (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20:1736–1737

    PubMed  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    PubMed  CAS  Google Scholar 

  • Wigge PA, Kim M, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Yamaguchi S, Smith MW, Brown RG, Kamiya Y, Sun T (1998) Phytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10:2115–2126

    PubMed  CAS  Google Scholar 

  • Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189

    PubMed  CAS  Google Scholar 

  • Yoo SY, Kardailsky I, Lee JS, Weigel D, Ahn JH (2004) Acceleration of flowering by overexpression of MFT (MOTHER OF FT AND TFL1). Mol Cells 17:95–101

    PubMed  CAS  Google Scholar 

  • Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T, Sung ZR, Takahashi S (2001) EMBRYONIC FLOWER2, a novel Polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13:2471–2481

    PubMed  CAS  Google Scholar 

  • Yu H, Ito T, Zhao YX, Peng JR, Kumar PP, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 101:7827–7832

    PubMed  CAS  Google Scholar 

  • Zeevaart JAD (1983) Gibberellins and flowering. Praeger Publishers, East Sussex edn

    Google Scholar 

  • Zeevaart JA (2008) Leaf-produced floral signals. Curr Opin Plant Biol 11:541–547

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ouest-Genopole® for the sequencing and genotyping work. The authors gratefully acknowledge M. Tellier and Dr M. Chevalier for the histological studies, J. Chameau for growing the plants, Dr M. Bendhammane for information on RoTCTP and N. Mansion for technical advice about figure layout. We also thank Prof. S. Sakr for the critical reading of the manuscript. A. Remay was supported by a joint grant from Région Pays de la Loire and the French Institut National de la Recherche Agronomique.

Author information

Authors and Affiliations

  1. INRA d’Angers Nantes, IFR 149 Quasav, UMR 1259 GenHort, BP60057, 49071, Beaucouzé cedex, France

    Arnaud Remay, David Lalanne, Tatiana Thouroude, Fabien Le Couviour, Laurence Hibrand-Saint Oyant & Fabrice Foucher

Authors
  1. Arnaud Remay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Lalanne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiana Thouroude
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabien Le Couviour
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laurence Hibrand-Saint Oyant
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabrice Foucher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabrice Foucher.

Additional information

Communicated by H. Nybom.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 108 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Remay, A., Lalanne, D., Thouroude, T. et al. A survey of flowering genes reveals the role of gibberellins in floral control in rose. Theor Appl Genet 119, 767–781 (2009). https://doi.org/10.1007/s00122-009-1087-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1087-1

Keywords

Search

Navigation