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.
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References
Aagaard JE, Willis JH, Phillips PC (2006) Relaxed selection among duplicate floral regulatory genes in Lamiales. J Mol Evol 63:493–503
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
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
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
Baum DA, Yoon HS, Oldham RL (2005) Molecular evolution of the transcription factor LEAFY in Brassicaceae. Mol Phylogenet Evol 37:1–14
Benlloch R, Berbel A, Serrano-Mislata A, Madueno F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot (Lond) 100:659–676
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
Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844
Blazquez MA, Ferrandiz C, Madueno F, Parcy F (2006) How floral meristems are built. Plant Mol Biol 60:855–870
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
Bomblies K, Doebley JF (2005) Molecular evolution of FLORICAULA/LEAFY orthologs in the Andropogoneae (Poaceae). Mol Biol Evol 22:1082–1094
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
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
Breitling R, Gerber JK (2000) Origin of the paired domain. Dev Genes Evol 210:644–650
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
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
Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587
Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493
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
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
Chen L, Cheng JC, Castle L, Sung ZR (1997) EMF genes regulate Arabidopsis inflorescence development. Plant Cell 9:2011–2024
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
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
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
Conaway RC, Brower CS, Conaway JW (2002) Emerging roles of ubiquitin in transcription regulation. Science 296:1254–1258
Cronk QC (2001) Plant evolution and development in a post-genomic context. Nat Rev Genet 2:607–619
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
Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405
Frohlich MW, Chase MW (2007) After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450:1184–1189
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
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
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
Huala E, Sussex IM (1992) LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development. Plant Cell 4:901–903
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
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
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
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
Kim PM, Lu LJ, Xia Y, Gerstein MB (2006) Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314:1938–1941
Kodadek T, Sikder D, Nalley K (2006) Keeping transcriptional activators under control. Cell 127:261–264
Lamb RS, Hill TA, Tan QK, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086
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
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
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
Lipford JR, Deshaies RJ (2003) Diverse roles for ubiquitin-dependent proteolysis in transcriptional activation. Nat Cell Biol 5:845–850
Lohmann JU, Weigel D (2002) Building beauty: the genetic control of floral patterning. Dev Cell 2:135–142
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
Longabaugh WJ, Davidson EH, Bolouri H (2009) Visualization, documentation, analysis, and communication of large-scale gene regulatory networks. Biochim Biophys Acta 1789:363–374
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
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
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
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
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
Parcy F (2005) Flowering: a time for integration. Int J Dev Biol 49:585–593
Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566
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
Pouteau S, Nicholls D, Tooke F, Coen E, Battey N (1997) The induction and maintenance of flowering in impatiens. Development 124:3343–3351
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
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
Robles P, Pelaz S (2005) Flower and fruit development in Arabidopsis thaliana. Int J Dev Biol 49:633–643
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
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
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
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
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
Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781
Sessions A, Yanofsky MF, Weigel D (2000) Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–782
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
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
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
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
Theissen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot (Lond) 100:603–619
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
Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584
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
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
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
Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500
Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859
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
Yoon HS, Baum DA (2004) Transgenic study of parallelism in plant morphological evolution. Proc Natl Acad Sci U S A 101:6524–6529
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
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
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.
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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
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DOI: https://doi.org/10.1007/s12374-009-9028-8