Skip to main content
Log in

The LEAFY Floral Regulators in Angiosperms: Conserved Proteins with Diverse Roles

  • REVIEW
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Genetic analyses in model angiosperms have shown that the LEAFY/FLORICAULA transcription factor plays a central role in flower development. In Arabidopsis, LEAFY (LFY) triggers the development of floral meristems and controls their patterning through the activation of floral organ identity genes. Several recent reports enlighten the structure and function of this conserved protein but also illustrate the variety of roles it plays in different angiosperms.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aagaard JE, Willis JH, Phillips PC (2006) Relaxed selection among duplicate floral regulatory genes in Lamiales. J Mol Evol 63:493–503

    Article  PubMed  CAS  Google Scholar 

  • Ahearn KP, Johnson HA, Weigel D, Wagner DR (2001) NFL1, a Nicotiana tabacum LEAFY-like gene, controls meristem initiation and floral structure. Plant Cell Physiol 42:1130–1139

    Article  PubMed  CAS  Google Scholar 

  • Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM (2005) The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29:231–262

    Article  PubMed  CAS  Google Scholar 

  • Archambault A, Bruneau A (2004) Phylogenetic utility of the LEAFY/FLORICAULA gene in the Caesalpinioideae (Leguminosae): gene duplication and a novel insertion. Syst Bot 29:609–626

    Article  Google Scholar 

  • Baum DA, Yoon HS, Oldham RL (2005) Molecular evolution of the transcription factor LEAFY in Brassicaceae. Mol Phylogenet Evol 37:1–14

    Article  PubMed  CAS  Google Scholar 

  • Benlloch R, Berbel A, Serrano-Mislata A, Madueno F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot (Lond) 100:659–676

    Article  Google Scholar 

  • Bharathan G, Janssen BJ, Kellogg EA, Sinha N (1999) Phylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins. Mol Biol Evol 16:553–563

    PubMed  CAS  Google Scholar 

  • Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844

    PubMed  CAS  Google Scholar 

  • Blazquez MA, Ferrandiz C, Madueno F, Parcy F (2006) How floral meristems are built. Plant Mol Biol 60:855–870

    Article  PubMed  CAS  Google Scholar 

  • Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322:1835–1839

    Article  PubMed  CAS  Google Scholar 

  • Bomblies K, Doebley JF (2005) Molecular evolution of FLORICAULA/LEAFY orthologs in the Andropogoneae (Poaceae). Mol Biol Evol 22:1082–1094

    Article  PubMed  CAS  Google Scholar 

  • Bomblies K, Doebley JF (2006) Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics 172:519–531

    Article  PubMed  CAS  Google Scholar 

  • Bomblies K, Wang RL, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–2395

    Article  PubMed  CAS  Google Scholar 

  • Breitling R, Gerber JK (2000) Origin of the paired domain. Dev Genes Evol 210:644–650

    Article  PubMed  CAS  Google Scholar 

  • Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14:867–876

    Article  PubMed  CAS  Google Scholar 

  • Busch A, Gleissberg S (2003) EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta 217:841–848

    Article  PubMed  CAS  Google Scholar 

  • Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587

    Article  PubMed  CAS  Google Scholar 

  • Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493

    Article  PubMed  CAS  Google Scholar 

  • Carpenter R, Coen ES (1995) Transposon induced chimeras show that floricaula, a meristem identity gene, acts non-autonomously between cell layers. Development 121:19–26

    PubMed  CAS  Google Scholar 

  • Chae E, Tan QK, Hill TA, Irish VF (2008) An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135:1235–1245

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Cheng JC, Castle L, Sung ZR (1997) EMF genes regulate Arabidopsis inflorescence development. Plant Cell 9:2011–2024

    Article  PubMed  CAS  Google Scholar 

  • Chou ML, Haung MD, Yang CH (2001) EMF genes interact with late-flowering genes in regulating floral initiation genes during shoot development in Arabidopsis thaliana. Plant Cell Physiol 42:499–507

    Article  PubMed  CAS  Google Scholar 

  • Chujo A, Zhang Z, Kishino H, Shimamoto K, Kyozuka J (2003) Partial conservation of LFY function between rice and Arabidopsis. Plant Cell Physiol 44:1311–1319

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Romero JM, Doyle S, Elliott R, Murphy G, Carpenter R (1990) floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322

    Article  PubMed  CAS  Google Scholar 

  • Conaway RC, Brower CS, Conaway JW (2002) Emerging roles of ubiquitin in transcription regulation. Science 296:1254–1258

    Article  PubMed  CAS  Google Scholar 

  • Cronk QC (2001) Plant evolution and development in a post-genomic context. Nat Rev Genet 2:607–619

    Article  PubMed  CAS  Google Scholar 

  • Dong ZC, Zhao Z, Liu CW, Luo JH, Yang J, Huang WH, Hu XH, Wang TL, Luo D (2005) Floral patterning in Lotus japonicus. Plant Physiol 137:1272–1282

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405

    Article  PubMed  CAS  Google Scholar 

  • Frohlich MW, Chase MW (2007) After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450:1184–1189

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hantke SS, Carpenter R, Coen ES (1995) Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems. Development 121:27–35

    PubMed  CAS  Google Scholar 

  • Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587

    Article  PubMed  CAS  Google Scholar 

  • Huala E, Sussex IM (1992) LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development. Plant Cell 4:901–903

    Article  PubMed  Google Scholar 

  • Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A 104:19369–19374

    Article  PubMed  Google Scholar 

  • Kato K, Ohta K, Komata Y, Araki T, Kanahama K, Kanahama Y (2005) Morphological and molecular analyses of the tomato floral mutant leafy inflorescence, a new allele of falsiflora. Plant Sci 169:131–138

    Article  CAS  Google Scholar 

  • Kelly AJ, Bonnlander MB, Meeks-Wagner DR (1995) NFL, the tobacco homolog of FLORICAULA and LEAFY, is transcriptionally expressed in both vegetative and floral meristems. Plant Cell 7:225–234

    Article  PubMed  CAS  Google Scholar 

  • Kempin SA, Mandel MA, Yanofsky MF (1993) Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol 103:1041–1046

    Article  PubMed  CAS  Google Scholar 

  • Kim PM, Lu LJ, Xia Y, Gerstein MB (2006) Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314:1938–1941

    Article  PubMed  CAS  Google Scholar 

  • Kodadek T, Sikder D, Nalley K (2006) Keeping transcriptional activators under control. Cell 127:261–264

    Article  PubMed  CAS  Google Scholar 

  • Lamb RS, Hill TA, Tan QK, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086

    PubMed  CAS  Google Scholar 

  • Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, Pupko T, Ben-Tal N (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33:W299–302

    Article  PubMed  CAS  Google Scholar 

  • Laux T, Mayer KFX, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96

    PubMed  CAS  Google Scholar 

  • Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS, Yanofsky MF (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11:1007–1018

    Article  PubMed  CAS  Google Scholar 

  • Lipford JR, Deshaies RJ (2003) Diverse roles for ubiquitin-dependent proteolysis in transcriptional activation. Nat Cell Biol 5:845–850

    Article  PubMed  CAS  Google Scholar 

  • Lohmann JU, Weigel D (2002) Building beauty: the genetic control of floral patterning. Dev Cell 2:135–142

    Article  PubMed  CAS  Google Scholar 

  • Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803

    Article  PubMed  CAS  Google Scholar 

  • Longabaugh WJ, Davidson EH, Bolouri H (2009) Visualization, documentation, analysis, and communication of large-scale gene regulatory networks. Biochim Biophys Acta 1789:363–374

    PubMed  CAS  Google Scholar 

  • Maizel A, Busch MA, Tanahashi T, Perkovic J, Kato M, Hasebe M, Weigel D (2005) The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308:260–263

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Castilla LP, Alvarez-Buylla ER (2003) Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proc Natl Acad Sci U S A 100:13407–13412

    Article  PubMed  CAS  Google Scholar 

  • Molinero-Rosales N, Jamilena M, Zurita S, Gomez P, Capel J, Lozano R (1999) FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J 20:685–693

    Article  PubMed  CAS  Google Scholar 

  • Moore MJ, Bell CD, Soltis PS, Soltis DE (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci U S A 104:19363–19368

    Article  PubMed  Google Scholar 

  • Ordidge M, Chiurugwi T, Tooke F, Battey NH (2005) LEAFY, TERMINAL FLOWER1 and AGAMOUS are functionally conserved but do not regulate terminal flowering and floral determinacy in Impatiens balsamina. Plant J 44:985–1000

    Article  PubMed  CAS  Google Scholar 

  • Parcy F (2005) Flowering: a time for integration. Int J Dev Biol 49:585–593

    Article  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  PubMed  CAS  Google Scholar 

  • Parcy F, Bomblies K, Weigel D (2002) Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral meristem identity in Arabidopsis. Development 129:2519–2527

    PubMed  CAS  Google Scholar 

  • Pouteau S, Nicholls D, Tooke F, Coen E, Battey N (1997) The induction and maintenance of flowering in impatiens. Development 124:3343–3351

    PubMed  CAS  Google Scholar 

  • Rao NN, Prasad K, Kumar PR, Vijayraghavan U (2008) Distinct regulatory role for RFL, the rice LFY homolog, in determining flowering time and plant architecture. Proc Natl Acad Sci U S A 105:3646–3651

    Article  PubMed  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 

  • Robles P, Pelaz S (2005) Flower and fruit development in Arabidopsis thaliana. Int J Dev Biol 49:633–643

    Article  PubMed  CAS  Google Scholar 

  • Rottmann WH, Meilan R, Sheppard LA, Brunner AM, Skinner JS, Ma C, Cheng S, Jouanin L, Pilate G, Strauss SH (2000) Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J 22:235–245

    Article  PubMed  CAS  Google Scholar 

  • Rudall PJ, Remizowa MV, Prenner G, Prychid CJ, Tuckett RE, Sokoloff DD (2009) Nonflowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units of Hydatellaceae and its bearing on the origin of the flower. Am J Bot 96:67–82

    Article  Google Scholar 

  • Ruiz-Garcia L, Madueno F, Wilkinson M, Haughn G, Salinas J, Martinez-Zapater JM (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell 9:1921–1934

    Article  PubMed  CAS  Google Scholar 

  • Saddic LA, Huvermann B, Bezhani S, Su Y, Winter CM, Kwon CS, Collum RP, Wagner D (2006) The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133:1673–1682

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130:6001–6012

    Article  PubMed  CAS  Google Scholar 

  • Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781

    Article  PubMed  Google Scholar 

  • Sessions A, Yanofsky MF, Weigel D (2000) Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–782

    Article  PubMed  CAS  Google Scholar 

  • Shu G, Amaral W, Hileman LC, Baum DA (2000) LEAFY and the evolution of rosette flowering in violet cress (Jonopsidium acaule, Brassicaceae). Am J Bot 87:634–641

    Article  PubMed  Google Scholar 

  • Souer E, van der Krol A, Kloos D, Spelt C, Bliek M, Mol J, Koes R (1998) Genetic control of branching pattern and floral identity during petunia inflorescence development. Development 125:733–742

    PubMed  CAS  Google Scholar 

  • Souer E, Rebocho AB, Bliek M, Kusters E, de Bruin RA, Koes R (2008) Patterning of inflorescences and flowers by the F-Box protein DOUBLE TOP and the LEAFY homolog ABERRANT LEAF AND FLOWER of petunia. Plant Cell 20:2033–2048

    Article  PubMed  CAS  Google Scholar 

  • Southerton SG, Strauss SH, Olive MR, Harcourt RL, Decroocq V, Zhu X, Llewellyn DJ, Peacock WJ, Dennis ES (1998) Eucalyptus has a functional equivalent of the Arabidopsis floral meristem identity gene LEAFY. Plant Mol Biol 37:897–910

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot (Lond) 100:603–619

    Article  Google Scholar 

  • Wada M, Cao QF, Kotoda N, Soejima J, Masuda T (2002) Apple has two orthologues of FLORICAULA/LEAFY involved in flowering. Plant Mol Biol 49:567–577

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Wellmer F, Dilks K, William D, Smith MR, Kumar PP, Riechmann JL, Greenland AJ, Meyerowitz EM (2004) Floral induction in tissue culture: a system for the analysis of LEAFY-dependent gene regulation. Plant J 39:273–282

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Chen J, Wen J, Tadege M, Li G, Liu Y, Mysore KS, Ratet P, Chen R (2008) Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol 146:1759–1772

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1993) LEAFY controls meristem identity in Arabidopsis. In: Amasino R (ed) Cellular communications in plants. Plenum, New York, pp 115–122

    Google Scholar 

  • Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • William DA, Su Y, Smith MR, Lu M, Baldwin DA, Wagner D (2004) Genomic identification of direct target genes of LEAFY. Proc Natl Acad Sci U S A 101:1775–1780

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Baum DA (2004) Transgenic study of parallelism in plant morphological evolution. Proc Natl Acad Sci U S A 101:6524–6529

    Article  PubMed  CAS  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 U S A 99:16336–16341

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Ito T, Wellmer F, Meyerowitz EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36:157–161

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank M. Blazquez, E. Gomez-Minguet, M. Monniaux, T. Spencer, and S. Perry for the critical reading of the manuscript. E.M. is supported by a Ph.D. grant from the French Ministry of Research. The work in our laboratory is supported by the ANR-07-BLAN-0211-01 (“Plant TF-Code”) and ATIP+ from the CNRS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to François Parcy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moyroud, E., Tichtinsky, G. & Parcy, F. The LEAFY Floral Regulators in Angiosperms: Conserved Proteins with Diverse Roles. J. Plant Biol. 52, 177–185 (2009). https://doi.org/10.1007/s12374-009-9028-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-009-9028-8

Keywords

Navigation