Flower Development in the Asterid Lineage

Part of the Methods in Molecular Biology book series (MIMB, volume 1110)


A complete understanding of the genetic control of flower development requires a comparative approach, involving species from across the angiosperm lineage. Using the accessible model plant Arabidopsis thaliana many of the genetic pathways that control development of the reproductive growth phase have been delineated. Research in other species has added to this knowledge base, revealing that, despite the myriad of floral forms found in nature, the genetic blueprint of flower development is largely conserved. However, these same studies have also highlighted differences in the way flowering is controlled in evolutionarily diverse species. Here, we review flower development in the eudicot asterid lineage, a group of plants that diverged from the rosid family, which includes Arabidopsis, 120 million years ago. Work on model species such as Antirrhinum majus, Petunia hybrida, and Gerbera hybrida has prompted a reexamination of textbook models of flower development; revealed novel mechanisms controlling floral gene expression; provided a means to trace evolution of key regulatory genes; and stimulated discussion about genetic redundancy and the fate of duplicated genes.


Flower development Asterids Floral meristem Floral organ identity (A)BC model 



We are grateful to Chiara Airoldi for comments on the manuscript. Our research is funded by grants from the Biotechnology and Biological Sciences Research Council.


  1. 1.
    Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc Biol Sci 268:2211–2220PubMedCentralPubMedGoogle Scholar
  2. 2.
    Siriwardana NS, Lamb RS (2012) The poetry of reproduction: the role of LEAFY in Arabidopsis thaliana flower formation. Int J Dev Biol 56:207–221PubMedGoogle Scholar
  3. 3.
    Wagner D, Sablowski RWM, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584PubMedGoogle Scholar
  4. 4.
    Wagner D, Wellmer F, Dilks K et al (2004) Floral induction in tissue culture: a system for the analysis of LEAFY-dependent gene regulation. Plant J 39:273–282PubMedGoogle Scholar
  5. 5.
    William DA, Su Y, Smith MR et al (2004) Genomic identification of direct target genes of LEAFY. Proc Natl Acad Sci U S A 101:1775–1780PubMedCentralPubMedGoogle Scholar
  6. 6.
    Winter CM, Austin RS, Blanvillain-Baufumé S et al (2011) LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus. Dev Cell 20:430–443PubMedGoogle Scholar
  7. 7.
    Moyroud E, Minguet EG, Ott F et al (2011) Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor. Plant Cell 23:1293–1306PubMedCentralPubMedGoogle Scholar
  8. 8.
    Benlloch R, Berbel A, Serrano-Mislata A, Madueño F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot 100:659–676PubMedGoogle Scholar
  9. 9.
    Weigel D, Alvarez J, Smyth DR et al (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859PubMedGoogle Scholar
  10. 10.
    Coen ES, Romero JM, Doyle S et al (1990) Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 21:1311–1322Google Scholar
  11. 11.
    Souer E, van der Krol A, Kloos D et al (1998) Genetic control of branching pattern and floral identity during Petunia inflorescence development. Development 125:733–742PubMedGoogle Scholar
  12. 12.
    Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedGoogle Scholar
  13. 13.
    Huijser P, Klein J, Lönnig WE et al (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J 11:1239–1249PubMedGoogle Scholar
  14. 14.
    Immink R, Hannapel D, Ferrario S et al (1999) A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126:5117–5126PubMedGoogle Scholar
  15. 15.
    Vandenbussche M, Zethof J, Souer E et al (2003) Toward the analysis of the Petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C and D floral organ identity functions require SEPALLATA-like MADS box genes in Petunia. Plant Cell 15:2680–2693PubMedCentralPubMedGoogle Scholar
  16. 16.
    Rijpkema A, Gerats T, Vandenbussche M (2006) Genetics of floral development in Petunia. Adv Bot Res 44:237–278Google Scholar
  17. 17.
    Levin JZ, Meyerowitz EM (1995) UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7:529–548PubMedCentralPubMedGoogle Scholar
  18. 18.
    Wilkinson MD, Haughn GW (1995) UNUSUAL FLORAL ORGANS Controls Meristem Identity and Organ Primordia Fate in Arabidopsis. Plant Cell 7:1485–1499PubMedCentralPubMedGoogle Scholar
  19. 19.
    Rijpkema AS, Vandenbussche M, Koes R et al (2010) Variations on a theme: changes in the floral ABCs in angiosperms. Semin Cell Dev Biol 21:100–107PubMedGoogle Scholar
  20. 20.
    Ingram GC, Goodrich J, Wilkinson MD et al (1995) Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7:1501–1510PubMedCentralPubMedGoogle Scholar
  21. 21.
    Allen KD, Sussex IM (1996) Falsiflora and anantha control early stages of floral meristem development in tomato (Lycopersicon esculentum Mill.). Planta 200:254–264Google Scholar
  22. 22.
    Lippman ZB, Cohen O, Alvarez JP et al (2008) The making of a compound inflorescence in tomato and related nightshades. PloS Biol 6:e288PubMedCentralPubMedGoogle Scholar
  23. 23.
    Souer E, Rebocho AB, Bliek M et al (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 20:2033–2048PubMedCentralPubMedGoogle Scholar
  24. 24.
    Causier B, Schwarz-Sommer Z, Davies B (2010) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21:73–79PubMedGoogle Scholar
  25. 25.
    Keck E, McSteen P, Carpenter R, Coen E (2003) Separation of genetic functions controlling organ identity in flowers. EMBO J 22:1058–1066PubMedGoogle Scholar
  26. 26.
    Maes T, Van de Steene N, Zethof J et al (2001) Petunia Ap2-like genes and their role in flower and seed development. Plant Cell 13:229–244PubMedCentralPubMedGoogle Scholar
  27. 27.
    Ditta G, Pinyopich A, Robles P et al (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940PubMedGoogle Scholar
  28. 28.
    Pelaz S, Tapia-López R, Alvarez-Buylla ER, Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 11:182–184PubMedGoogle Scholar
  29. 29.
    Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529PubMedGoogle Scholar
  30. 30.
    Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedGoogle Scholar
  31. 31.
    Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931–936PubMedGoogle Scholar
  32. 32.
    Davies B, Cartolano M, Schwarz-Sommer Z (2006) Flower development: the Antirrhinum perspective. Adv Bot Res 44:279–321Google Scholar
  33. 33.
    Litt A (2007) An evaluation of the A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int J Plant Sci 168:73–91Google Scholar
  34. 34.
    Gregis V, Sessa A, Dorca-Fornell C, Kater MM (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant J 60:626–637PubMedGoogle Scholar
  35. 35.
    Bowman JL, Sakai H, Jack T et al (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114:599–615PubMedGoogle Scholar
  36. 36.
    Simon R, Carpenter R, Doyle S, Coen E (1994) Fimbriata controls flower development by mediating between meristem and organ identity genes. Cell 78:99–107PubMedGoogle Scholar
  37. 37.
    Yellina AL, Orashakova S, Lange S et al (2010) Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). Evodevo 1:13PubMedCentralPubMedGoogle Scholar
  38. 38.
    Wuest SE, O’Maoileidigh DS, Rae L et al (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. PNAS 109:13452–13457PubMedGoogle Scholar
  39. 39.
    Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587PubMedGoogle Scholar
  40. 40.
    Lenhard M, Bohnert A, Jürgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814PubMedGoogle Scholar
  41. 41.
    Lohmann JU, Hong RL, Hobe M et al (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803PubMedGoogle Scholar
  42. 42.
    Das P, Ito T, Wellmer F et al (2009) Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development 136:1605–1611PubMedGoogle Scholar
  43. 43.
    Maier AT, Stehling-Sun S, Wollmann H et al (2009) Dual roles of the bZIP transcription factor PERIANTHIA in the control of floral architecture and homeotic gene expression. Development 136:1613–1620PubMedGoogle Scholar
  44. 44.
    Bao X, Franks RG, Levin JZ, Liu Z (2004) Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems. Plant Cell 16:1478–1489PubMedCentralPubMedGoogle Scholar
  45. 45.
    Bomblies K, Dagenais N, Weigel D (1999) Redundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2. Dev Biol 216:260–264PubMedGoogle Scholar
  46. 46.
    Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002PubMedGoogle Scholar
  47. 47.
    Franks RG, Wang C, Levin JZ, Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129:253–263PubMedGoogle Scholar
  48. 48.
    Goodrich J, Puangsomlee P, Martin M et al (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44–51PubMedGoogle Scholar
  49. 49.
    Krizek BA, Lewis MW, Fletcher JC (2006) RABBIT EARS is a second-whorl repressor of AGAMOUS that maintains spatial boundaries in Arabidopsis flowers. Plant J 45:369–383PubMedGoogle Scholar
  50. 50.
    Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991PubMedGoogle Scholar
  51. 51.
    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 121:27–35PubMedGoogle Scholar
  52. 52.
    Causier B, Bradley D, Cook H, Davies B (2009) Conserved intragenic elements were critical for the evolution of the floral C-function. Plant J 58:41–52PubMedGoogle Scholar
  53. 53.
    Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365PubMedCentralPubMedGoogle Scholar
  54. 54.
    Deyholos MK, Sieburth LE (2000) Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron. Plant Cell 12:1799–1810PubMedCentralPubMedGoogle Scholar
  55. 55.
    Dinh TT, Girke T, Liu X et al (2012) The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139:1978–1986PubMedGoogle Scholar
  56. 56.
    Cartolano M, Castillo R, Efremova N et al (2007) A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nat Genet 39:901–905PubMedGoogle Scholar
  57. 57.
    Tsuchimoto S, van der Krol AR, Chua NH (1993) Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell 5:843–853PubMedCentralPubMedGoogle Scholar
  58. 58.
    McSteen PC, Vincent CA, Doyle S et al (1998) Control of floral homeotic gene expression and organ morphogenesis in Antirrhinum. Development 125:2359–2369PubMedGoogle Scholar
  59. 59.
    Motte P, Saedler H, Schwarz-Sommer Z (1998) STYLOSA and FISTULATA: regulatory components of the homeotic control of Antirrhinum floral organogenesis. Development 125:71–84PubMedGoogle Scholar
  60. 60.
    Cartolano M, Efremova N, Kuckenberg M et al (2009) Enhanced AGAMOUS expression in the centre of the Arabidopsis flower causes ectopic expression over its outer expression boundaries. Planta 230:857–862PubMedCentralPubMedGoogle Scholar
  61. 61.
    Sridhar VV, Surendrarao A, Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133:3159–3166PubMedGoogle Scholar
  62. 62.
    Navarro C, Efremova N, Golz JF et al (2004) Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development. Development 131:3649–3659PubMedGoogle Scholar
  63. 63.
    Melzer R, Theissen G (2009) Reconstitution of ‘floral quartets’ in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res 37:2723–2736PubMedCentralPubMedGoogle Scholar
  64. 64.
    Jack T, Fox GL, Meyerowitz EM (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76:703–716PubMedGoogle Scholar
  65. 65.
    Schwarz-Sommer Z, Hue I, Huijser P et al (1992) Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J 11:251–263PubMedGoogle Scholar
  66. 66.
    Manchado-Rojo M, Delgado-Benarroch L, Roca MJ et al (2012) Quantitative levels of Deficiens and Globosa during late petal development show a complex transcriptional network topology of B function. Plant J 72:294–307PubMedGoogle Scholar
  67. 67.
    Airoldi CA (2010) Determination of sexual organ development. Sex Plant Reprod 23:53–62PubMedGoogle Scholar
  68. 68.
    Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356PubMedGoogle Scholar
  69. 69.
    Kramer EM, Dorit RL, Irish VF (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149:765–783PubMedGoogle Scholar
  70. 70.
    Kim S, Yoo MJ, Albert VA et al (2004) Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication. Am J Bot 91:2102–2118PubMedGoogle Scholar
  71. 71.
    Vandenbussche M, Theissen G, Van de Peer Y, Gerats T (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res 31:4401–4409PubMedCentralPubMedGoogle Scholar
  72. 72.
    Causier B, Castillo R, Xue Y et al (2010) Tracing the evolution of the floral homeotic B- and C-function genes through genome synteny. Mol Biol Evol 27:2651–2664PubMedGoogle Scholar
  73. 73.
    Vandenbussche M, Zethof J, Royaert S et al (2004) The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16:741–754PubMedCentralPubMedGoogle Scholar
  74. 74.
    van der Krol AR, Brunelle A, Tsuchimoto S, Chua NH (1993) Functional analysis of petunia floral homeotic MADS box gene pMADS1. Genes Dev 7:1214–1228PubMedGoogle Scholar
  75. 75.
    Rijpkema AS, Royaert S, Zethof J, van der Weerden G, Gerats T, Vandenbussche M (2006) Analysis of the Petunia TM6 MADS box gene reveals functional divergence within the DEF/AP3 lineage. Plant Cell 18:1819–1832PubMedCentralPubMedGoogle Scholar
  76. 76.
    de Martino G, Pan I, Emmanuel E, Levy A, Irish VF (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18:1833–1845PubMedCentralPubMedGoogle Scholar
  77. 77.
    Broholm SK, Pöllänen E, Ruokolainen S et al (2010) Functional characterization of B class MADS-box transcription factors in Gerbera hybrida. J Exp Bot 61:75–85PubMedGoogle Scholar
  78. 78.
    Yanofsky MF, Ma H, Bowman JL et al (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39PubMedGoogle Scholar
  79. 79.
    Bradley D, Carpenter R, Sommer H et al (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72:85–95PubMedGoogle Scholar
  80. 80.
    Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166:1011–1023PubMedGoogle Scholar
  81. 81.
    Causier B, Castillo R, Zhou J et al (2005) Evolution in action: following function in duplicated floral homeotic genes. Curr Biol 15:1508–1512PubMedGoogle Scholar
  82. 82.
    Liljegren SJ, Ditta GS, Eshed Y et al (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770PubMedGoogle Scholar
  83. 83.
    Favaro R, Pinyopich A, Battaglia R et al (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611PubMedCentralPubMedGoogle Scholar
  84. 84.
    Pinyopich A, Ditta GS, Savidge B et al (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88PubMedGoogle Scholar
  85. 85.
    Colombo M, Brambilla V, Marcheselli R et al (2010) A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Dev Biol 337:294–302PubMedGoogle Scholar
  86. 86.
    Davies B, Motte P, Keck E et al (1999) PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 18:4023–4034PubMedGoogle Scholar
  87. 87.
    Davies B, Di Rosa A, Eneva T et al (1996) Alteration of tobacco floral organ identity by expression of combinations of Antirrhinum MADS-box genes. Plant J 10:663–677PubMedGoogle Scholar
  88. 88.
    Airoldi CA, Bergonzi S, Davies B (2010) Single amino acid change alters the ability to specify male or female organ identity. Proc Natl Acad Sci U S A 107:18898–18902PubMedCentralPubMedGoogle Scholar
  89. 89.
    Davies B, Egea-Cortines M, de Andrade Silva E et al (1996) Multiple interactions amongst floral homeotic proteins. EMBO J 15:4330–4343PubMedGoogle Scholar
  90. 90.
    Yu D, Kotilainen M, Pöllänen E et al (1999) Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J 17:51–62PubMedGoogle Scholar
  91. 91.
    Heijmans K, Ament K, Rijpkema AS et al (2012) Redefining C and D in the Petunia ABC. Plant Cell 24:2305–2317PubMedCentralPubMedGoogle Scholar
  92. 92.
    Fourquin C, Ferrándiz C (2012) Functional analyses of AGAMOUS family members in Nicotiana benthamiana clarify the evolution of early and late roles of C-function genes in eudicots. Plant J 71:990–1001PubMedGoogle Scholar
  93. 93.
    Angenent GC, Franken J, Busscher M et al (1995) A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7:1569–1582PubMedCentralPubMedGoogle Scholar
  94. 94.
    Colombo L, Franken J, Koetje E et al (1995) The petunia MADS-box gene FBP11 determines ovule identity. Plant Cell 7:1859–1868PubMedCentralPubMedGoogle Scholar
  95. 95.
    Pnueli L, Hareven D, Broday L et al (1994) The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6:175–186PubMedCentralPubMedGoogle Scholar
  96. 96.
    Angenent GC, Franken J, Busscher M et al (1994) Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J 5:33–44PubMedGoogle Scholar
  97. 97.
    Ferrario S, Immink RG, Shchennikova A (2003) et al The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15:914–925PubMedCentralPubMedGoogle Scholar
  98. 98.
    Zahn LM, Kong H, Leebens-Mack JH et al (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223PubMedGoogle Scholar
  99. 99.
    Pelaz S, Ditta GS, Baumann E et al (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203PubMedGoogle Scholar
  100. 100.
    Ampomah-Dwamena C, Morris BA, Sutherland P et al (2002) Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol 130:605–617PubMedCentralPubMedGoogle Scholar
  101. 101.
    Kotilainen M, Elomaa P, Uimari A et al (2000) GRCD1, an AGL2-like MADS box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 12:1893–1902PubMedCentralPubMedGoogle Scholar
  102. 102.
    Uimari A, Kotilainen M, Elomaa P et al (2004) Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proc Natl Acad Sci U S A 101:15817–15822PubMedCentralPubMedGoogle Scholar
  103. 103.
    de Folter S, Immink RG, Kieffer M et al (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17:1424–1433PubMedCentralPubMedGoogle Scholar
  104. 104.
    Causier B, Cook H, Davies B (2003) An Antirrhinum ternary complex factor specifically interacts with C-function and SEPALLATA-like MADS-box factors. Plant Mol Biol 52:1051–1062PubMedGoogle Scholar
  105. 105.
    Leseberg CH, Eissler CL, Wang X et al (2008) Interaction study of MADS-domain proteins in tomato. J Exp Bot 59:2253–2265PubMedGoogle Scholar
  106. 106.
    Immink RGH, Gadella TWJ Jr, Ferrario S et al (2002) Analysis of MADS box protein-protein interactions in living plant cells. Proc Natl Acad Sci U S A 99:2416–2421PubMedCentralPubMedGoogle Scholar
  107. 107.
    Immink RG, Tonaco IA, de Folter S et al (2009) SEPALLATA3: the ‘glue’ for MADS box transcription factor complex formation. Genome Biol 10:R24PubMedCentralPubMedGoogle Scholar
  108. 108.
    Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471PubMedGoogle Scholar
  109. 109.
    Galliot C, Stuurman J, Kuhlemeier C (2006) The genetic dissection of floral pollination syndromes. Curr Opin Plant Biol 9:78–82PubMedGoogle Scholar
  110. 110.
    Chen F, Tholl D, D’Auria JC et al (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494PubMedCentralPubMedGoogle Scholar
  111. 111.
    Luo D, Carpenter R, Vincent C et al (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799PubMedGoogle Scholar
  112. 112.
    Luo D, Carpenter R, Copsey L et al (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99:367–376PubMedGoogle Scholar
  113. 113.
    Cubas P, Coen E, Zapater JM (2001) Ancient asymmetries in the evolution of flowers. Curr Biol 11:1050–1052PubMedGoogle Scholar
  114. 114.
    Galego L, Almeida J (2002) Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev 16:880–891PubMedGoogle Scholar
  115. 115.
    Corley SB, Carpenter R, Copsey L, Coen E (2005) Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci U S A 102:5068–5073PubMedCentralPubMedGoogle Scholar
  116. 116.
    Perez-Rodriguez M, Jaffe FW, Butelli E et al (2005) Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132:359–370PubMedGoogle Scholar
  117. 117.
    Green AA, Kennaway JR, Hanna AI et al (2010) Genetic control of organ shape and tissue polarity. PloS Biol 8:e1000537PubMedCentralPubMedGoogle Scholar
  118. 118.
    Cui ML, Copsey L, Green AA et al (2010) Quantitative control of organ shape by combinatorial gene activity. PloS Biol 8:e1000538PubMedCentralPubMedGoogle Scholar
  119. 119.
    Zik M, Irish VF (2003) Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15:207–222PubMedCentralPubMedGoogle Scholar
  120. 120.
    Gómez-Mena C, de Folter S, Costa MM et al (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132:429–438PubMedGoogle Scholar
  121. 121.
    Kaufmann K, Muiño JM, Jauregui R et al (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:e1000090PubMedCentralPubMedGoogle Scholar
  122. 122.
    Kaufmann K, Wellmer F, Muiño JM et al (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89PubMedGoogle Scholar
  123. 123.
    Immink RG, Posé D, Ferrario S et al (2012) Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol 160:433–449PubMedCentralPubMedGoogle Scholar
  124. 124.
    Deng W, Ying H, Helliwell CA et al (2011) FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci U S A 108:6680–6685PubMedCentralPubMedGoogle Scholar
  125. 125.
    Bey M, Stüber K, Fellenberg K et al (2004) Characterization of antirrhinum petal development and identification of target genes of the class B MADS box gene DEFICIENS. Plant Cell 16:3197–3215PubMedCentralPubMedGoogle Scholar
  126. 126.
    Cui R, Han J, Zhao S et al (2010) Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). Plant J 61:767–781PubMedGoogle Scholar
  127. 127.
    Airoldi CA, Davies B (2012) Gene duplication and the evolution of plant MADS-box transcription factors. J Genet Genomics 39:157–165PubMedGoogle Scholar

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© Springer Science+Business Media, New York 2014

Authors and Affiliations

  1. 1.Centre for Plant Sciences, School of BiologyUniversity of LeedsLeedsUK

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