Flower Development: Open Questions and Future Directions

  • Frank WellmerEmail author
  • John L. Bowman
  • Brendan DaviesEmail author
  • Cristina FerrándizEmail author
  • Jennifer C. FletcherEmail author
  • Robert G. FranksEmail author
  • Emmanuelle GracietEmail author
  • Veronica Gregis
  • Toshiro ItoEmail author
  • Thomas P. JackEmail author
  • Yuling JiaoEmail author
  • Martin M. Kater
  • Hong MaEmail author
  • Elliot M. Meyerowitz
  • Nathanaël Prunet
  • José Luis RiechmannEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1110)


Almost three decades of genetic and molecular analyses have resulted in detailed insights into many of the processes that take place during flower development and in the identification of a large number of key regulatory genes that control these processes. Despite this impressive progress, many questions about how flower development is controlled in different angiosperm species remain unanswered. In this chapter, we discuss some of these open questions and the experimental strategies with which they could be addressed. Specifically, we focus on the areas of floral meristem development and patterning, floral organ specification and differentiation, as well as on the molecular mechanisms underlying the evolutionary changes that have led to the astounding variations in flower size and architecture among extant and extinct angiosperms.


Flower development Floral meristems ABC model Floral evolution 


  1. 1.
    Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61(6):1001–1013PubMedGoogle Scholar
  2. 2.
    Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68(12):2013–2037PubMedGoogle Scholar
  3. 3.
    Andres F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13(9):627–639PubMedGoogle Scholar
  4. 4.
    Long J, Barton MK (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev Biol 218(2):341–353PubMedGoogle Scholar
  5. 5.
    Grbic V, Bleecker AB (2000) Axillary meristem development in Arabidopsis thaliana. Plant J 21(2):215–223PubMedGoogle Scholar
  6. 6.
    Hempel FD, Feldman LJ (1994) Bi-directional inflorescence development in Arabidopsis thaliana: acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192:276–286Google Scholar
  7. 7.
    Hempel FD, Zambryski PC, Feldman LJ (1998) Photoinduction of flower identity in vegetatively biased primordia. Plant Cell 10(10):1663–1676PubMedCentralPubMedGoogle Scholar
  8. 8.
    Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2(8):755–767PubMedCentralPubMedGoogle Scholar
  9. 9.
    Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282(5397):2226–2230PubMedGoogle Scholar
  10. 10.
    Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426(6964):255–260PubMedGoogle Scholar
  11. 11.
    Yamaguchi N, Wu MF, Winter CM, Berns MC, Nole-Wilson S, Yamaguchi A, Coupland G, Krizek BA, Wagner D (2013) A molecular framework for auxin-mediated initiation of flower primordia. Dev Cell 24(3):271–282PubMedGoogle Scholar
  12. 12.
    Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69(5):843–859PubMedGoogle Scholar
  13. 13.
    Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3(8):771–781PubMedCentralPubMedGoogle Scholar
  14. 14.
    Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395(6702):561–566PubMedGoogle Scholar
  15. 15.
    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(9):1673–1682PubMedGoogle Scholar
  16. 16.
    Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285(5427):582–584PubMedGoogle Scholar
  17. 17.
    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(6):1775–1780PubMedCentralPubMedGoogle Scholar
  18. 18.
    Winter CM, Austin RS, Blanvillain-Baufume S, Reback MA, Monniaux M, Wu MF, Sang Y, Yamaguchi A, Yamaguchi N, Parker JE, Parcy F, Jensen ST, Li H, Wagner D (2011) LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev Cell 20(4):430–443PubMedGoogle Scholar
  19. 19.
    Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127(4):725–734PubMedGoogle Scholar
  20. 20.
    Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueno F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328(5974):85–89PubMedGoogle Scholar
  21. 21.
    Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth D (1993) Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119:721–743Google Scholar
  22. 22.
    Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267(5197):522–525PubMedGoogle Scholar
  23. 23.
    Gregis V, Sessa A, Colombo L, Kater MM (2008) AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J 56(6):891–902PubMedGoogle Scholar
  24. 24.
    Grandi V, Gregis V, Kater MM (2012) Uncovering genetic and molecular interactions among floral meristem identity genes in Arabidopsis thaliana. Plant J 69(5):881–893PubMedGoogle Scholar
  25. 25.
    Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16(5):711–722PubMedGoogle Scholar
  26. 26.
    Chandler JW, Jacobs B, Cole M, Comelli P, Werr W (2011) DORNROSCHEN-LIKE expression marks Arabidopsis floral organ founder cells and precedes auxin response maxima. Plant Mol Biol 76(1–2):171–185PubMedGoogle Scholar
  27. 27.
    Nag A, Yang Y, Jack T (2007) DORNROSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis. Plant Mol Biol 65(3):219–232PubMedGoogle Scholar
  28. 28.
    Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12(4):507–518PubMedCentralPubMedGoogle Scholar
  29. 29.
    Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9(6):841–857PubMedCentralPubMedGoogle Scholar
  30. 30.
    Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon A, Neff MM, Girke T, Springer PS (2012) Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci U S A 109(51):21146–21151PubMedCentralPubMedGoogle Scholar
  31. 31.
    Lampugnani ER, Kilinc A, Smyth DR (2012) PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana. Plant J 71(5):724–735PubMedGoogle Scholar
  32. 32.
    Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131(17):4311–4322PubMedGoogle Scholar
  33. 33.
    Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134(6):1051–1060PubMedGoogle Scholar
  34. 34.
    Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B (2004) CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131(4):915–922PubMedGoogle Scholar
  35. 35.
    Mizukami Y, Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71(1):119–131PubMedGoogle Scholar
  36. 36.
    Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346(6279):35–39PubMedGoogle Scholar
  37. 37.
    Lenhard M, Bohnert A, Jurgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105(6):805–814PubMedGoogle Scholar
  38. 38.
    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 105:793–803PubMedGoogle Scholar
  39. 39.
    Sun B, Xu Y, Ng KH, Ito T (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev 23(15):1791–1804PubMedGoogle Scholar
  40. 40.
    Payne T, Johnson SD, Koltunow AM (2004) KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development 131(15):3737–3749PubMedGoogle Scholar
  41. 41.
    Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126(11):2387–2396PubMedGoogle Scholar
  42. 42.
    Gomez-Mena C, de Folter S, Costa MM, Angenent GC, Sablowski R (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132(3):429–438PubMedGoogle Scholar
  43. 43.
    Sun B, Ito T (2010) Floral stem cells: from dynamic balance towards termination. Biochem Soc Trans 38(2):613–616PubMedGoogle Scholar
  44. 44.
    Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114(3):599–615PubMedGoogle Scholar
  45. 45.
    Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378(6553):199–203PubMedGoogle Scholar
  46. 46.
    Davies B, Egea-Cortines M, de Andrade SE, Saedler H, Sommer H (1996) Multiple interactions amongst floral homeotic MADS box proteins. EMBO J 15(16):4330–4343PubMedGoogle Scholar
  47. 47.
    Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci U S A 93(10):4793–4798PubMedCentralPubMedGoogle Scholar
  48. 48.
    Egea-Cortines M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18(19):5370–5379PubMedGoogle Scholar
  49. 49.
    Melzer R, Theissen G (2009) Reconstitution of ‘floral quartets’ in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res 37(8):2723–2736PubMedCentralPubMedGoogle Scholar
  50. 50.
    Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409(6819):525–529PubMedGoogle Scholar
  51. 51.
    Gamboa A, Paez-Valencia J, Acevedo GF, Vazquez-Moreno L, Alvarez-Buylla RE (2001) Floral transcription factor AGAMOUS interacts in vitro with a leucine-rich repeat and an acid phosphatase protein complex. Biochem Biophys Res Commun 288(4):1018–1026PubMedGoogle Scholar
  52. 52.
    Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26(4):385–394PubMedGoogle Scholar
  53. 53.
    Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS Interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158(1):423–438PubMedCentralPubMedGoogle Scholar
  54. 54.
    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(5):1051–1062PubMedGoogle Scholar
  55. 55.
    Gregis V, Sessa A, Colombo L, Kater MM (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18(6):1373–1382PubMedCentralPubMedGoogle Scholar
  56. 56.
    Hill K, Wang H, Perry SE (2008) A transcriptional repression motif in the MADS factor AGL15 is involved in recruitment of histone deacetylase complex components. Plant J 53(1):172–185PubMedGoogle Scholar
  57. 57.
    Masiero S, Imbriano C, Ravasio F, Favaro R, Pelucchi N, Gorla MS, Mantovani R, Colombo L, Kater MM (2002) Ternary complex formation between MADS-box transcription factors and the histone fold protein NF-YB. J Biol Chem 277(29):26429–26435PubMedGoogle Scholar
  58. 58.
    Sridhar VV, Surendrarao A, Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133(16):3159–3166PubMedGoogle Scholar
  59. 59.
    Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC, Kaufmann K (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A 109(5):1560–1565PubMedCentralPubMedGoogle Scholar
  60. 60.
    Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11(12):830–842PubMedGoogle Scholar
  61. 61.
    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 U S A 108(16):6680–6685PubMedCentralPubMedGoogle Scholar
  62. 62.
    Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7(4):e1000090PubMedCentralPubMedGoogle Scholar
  63. 63.
    Immink RG, Pose D, Ferrario S, Ott F, Kaufmann K, Valentim FL, de Folter S, van der Wal F, van Dijk AD, Schmid M, Angenent GC (2012) Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol 160(1):433–449PubMedCentralPubMedGoogle Scholar
  64. 64.
    Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci U S A 109(33):13452–13457PubMedCentralPubMedGoogle Scholar
  65. 65.
    Kieffer M, Master V, Waites R, Davies B (2011) TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J 68(1):147–158PubMedCentralPubMedGoogle Scholar
  66. 66.
    Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2(7):e117PubMedCentralPubMedGoogle Scholar
  67. 67.
    Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22(7):2156–2170PubMedCentralPubMedGoogle Scholar
  68. 68.
    Ge X, Chang F, Ma H (2010) Signaling and transcriptional control of reproductive development in Arabidopsis. Curr Biol 20(22):R988–R997PubMedGoogle Scholar
  69. 69.
    Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci U S A 101(20):7827–7832PubMedCentralPubMedGoogle Scholar
  70. 70.
    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(5):1055–1064PubMedGoogle Scholar
  71. 71.
    Ito T, Ng KH, Lim TS, Yu H, Meyerowitz EM (2007) The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19(11):3516–3529PubMedCentralPubMedGoogle Scholar
  72. 72.
    Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127(18):3877–3888PubMedGoogle Scholar
  73. 73.
    Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283(5409):1911–1914PubMedGoogle Scholar
  74. 74.
    Jun J, Fiume E, Roeder AH, Meng L, Sharma VK, Osmont KS, Baker C, Ha CM, Meyerowitz EM, Feldman LJ, Fletcher JC (2010) Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol 154(4):1721–1736PubMedCentralPubMedGoogle Scholar
  75. 75.
    Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12(20):1718–1727PubMedGoogle Scholar
  76. 76.
    Hord CL, Chen C, Deyoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18(7):1667–1680PubMedCentralPubMedGoogle Scholar
  77. 77.
    Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15(12):2792–2804PubMedCentralPubMedGoogle Scholar
  78. 78.
    Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16(15):2021–2031PubMedGoogle Scholar
  79. 79.
    Sablowski R (2010) Genes and functions controlled by floral organ identity genes. Semin Cell Dev Biol 21(1):94–99PubMedGoogle Scholar
  80. 80.
    Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Genet Dev 11(4):449–456PubMedGoogle Scholar
  81. 81.
    Pelaz S, Tapia-Lopez R, Alvarez-Buylla ER, Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 11(3):182–184PubMedGoogle Scholar
  82. 82.
    Sundberg E, Ferrándiz C, Østergaard, L., ed (2009) Gynoecium patterning in Arabidopsis: a basic plan behind a complex structure. In: Annual plant reviews volume 38: fruit development and seed dispersal. Oxford, UK: Blackwell Publishing Ltd pp 35–69Google Scholar
  83. 83.
    Chang F, Wang Y, Wang S, Ma H (2011) Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol 14(1):66–73PubMedGoogle Scholar
  84. 84.
    Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434PubMedGoogle Scholar
  85. 85.
    Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322Google Scholar
  86. 86.
    Singh MB, Bhalla PL (2007) Control of male germ-cell development in flowering plants. Bioessays 29(11):1124–1132PubMedGoogle Scholar
  87. 87.
    Golubovskaya IN (1979) Genetic control of meiosis. Int Rev Cytol 58:247–290PubMedGoogle Scholar
  88. 88.
    Hamant O, Ma H, Cande WZ (2006) Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57:267–302PubMedGoogle Scholar
  89. 89.
    Ma H (2006) A molecular portrait of Arabidopsis meiosis. Arabidopsis Book 4:e0095PubMedCentralPubMedGoogle Scholar
  90. 90.
    Mercier R, Grelon M (2008) Meiosis in plants: ten years of gene discovery. Cytogenet Genome Res 120(3–4):281–290PubMedGoogle Scholar
  91. 91.
    Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190(3):523–544PubMedGoogle Scholar
  92. 92.
    Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, Ma H, Reiss B (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A 101(29):10596–10601PubMedCentralPubMedGoogle Scholar
  93. 93.
    Li W, Yang X, Lin Z, Timofejeva L, Xiao R, Makaroff CA, Ma H (2005) The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol 138(2):965–976PubMedCentralPubMedGoogle Scholar
  94. 94.
    Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754PubMedGoogle Scholar
  95. 95.
    Wijeratne AJ, Chen C, Zhang W, Timofejeva L, Ma H (2006) The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol Biol Cell 17(3):1331–1343PubMedCentralPubMedGoogle Scholar
  96. 96.
    Kelliher T, Walbot V (2012) Hypoxia triggers meiotic fate acquisition in maize. Science 337(6092):345–348. doi: 10.1126/science.1220080 PubMedGoogle Scholar
  97. 97.
    Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72(1):85–95PubMedGoogle Scholar
  98. 98.
    Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ (1996) Diversification of C-function activity in maize flower development. Science 274(5292):1537–1540PubMedGoogle Scholar
  99. 99.
    Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4(9):1483–1493PubMedGoogle Scholar
  100. 100.
    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(4983):931–936PubMedGoogle Scholar
  101. 101.
    Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5(3):569–579PubMedGoogle Scholar
  102. 102.
    Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol 41(6):710–718PubMedGoogle Scholar
  103. 103.
    Kramer EM, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago PM (2007) Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. Plant Cell 19(3):750–766PubMedCentralPubMedGoogle Scholar
  104. 104.
    Mondragon-Palomino M, Theissen G (2011) Conserved differential expression of paralogous DEFICIENS- and GLOBOSA-like MADS-box genes in the flowers of Orchidaceae: refining the ‘orchid code’. Plant J 66(6):1008–1019PubMedGoogle Scholar
  105. 105.
    Mouradov A, Hamdorf B, Teasdale RD, Kim JT, Winter KU, Theissen G (1999) A DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. Dev Genet 25(3):245–252PubMedGoogle Scholar
  106. 106.
    Shindo S, Ito M, Ueda K, Kato M, Hasebe M (1999) Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev 1(3):180–190PubMedGoogle Scholar
  107. 107.
    Sundstrom J, Carlsbecker A, Svensson ME, Svenson M, Johanson U, Theiβen G, Engstrom P (1999) MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. Dev Genet 25(3):253–266PubMedGoogle Scholar
  108. 108.
    Tandre K, Svenson M, Svensson ME, Engstrom P (1998) Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J 15(5):615–623PubMedGoogle Scholar
  109. 109.
    Litt A (2007) An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int J Plant Sci 168(1):73–91Google Scholar
  110. 110.
    Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65(6):991–1002PubMedGoogle Scholar
  111. 111.
    Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1(1):37–52PubMedCentralPubMedGoogle Scholar
  112. 112.
    Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424(6944):85–88PubMedGoogle Scholar
  113. 113.
    Gustafson-Brown C, Savidge B, Yanofsky MF (1994) Regulation of the arabidopsis floral homeotic gene APETALA1. Cell 76(1):131–143PubMedGoogle Scholar
  114. 114.
    Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2(8):741–753PubMedCentralPubMedGoogle Scholar
  115. 115.
    Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360(6401):273–277PubMedGoogle Scholar
  116. 116.
    Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377(6549):522–524PubMedGoogle Scholar
  117. 117.
    Benlloch R, d’Erfurth I, Ferrandiz C, Cosson V, Beltran JP, Canas LA, Kondorosi A, Madueno F, Ratet P (2006) Isolation of mtpim proves Tnt1 a useful reverse genetics tool in Medicago truncatula and uncovers new aspects of AP1-like functions in legumes. Plant Physiol 142(3):972–983PubMedCentralPubMedGoogle Scholar
  118. 118.
    Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y, Lifschitz E (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci U S A 106(20):8392–8397PubMedCentralPubMedGoogle Scholar
  119. 119.
    Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296(5566):343–346PubMedGoogle Scholar
  120. 120.
    Pabon-Mora N, Ambrose BA, Litt A (2012) Poppy APETALA1/FRUITFULL orthologs control flowering time, branching, perianth identity, and fruit development. Plant Physiol 158(4):1685–1704PubMedCentralPubMedGoogle Scholar
  121. 121.
    Keck E, McSteen P, Carpenter R, Coen E (2003) Separation of genetic functions controlling organ identity in flowers. EMBO J 22(5):1058–1066PubMedGoogle Scholar
  122. 122.
    Cartolano M, Castillo R, Efremova N, Kuckenberg M, Zethof J, Gerats T, Schwarz-Sommer Z, Vandenbussche M (2007) A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nat Genet 39(7):901–905PubMedGoogle Scholar
  123. 123.
    Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pouplana L, Martinez-Castilla L, Yanofsky MF (2000) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci U S A 97(10):5328–5333PubMedCentralPubMedGoogle Scholar
  124. 124.
    Theiβen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43(5):484–516Google Scholar
  125. 125.
    Hasebe M, Wen CK, Kato M, Banks JA (1998) Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proc Natl Acad Sci U S A 95(11):6222–6227PubMedCentralPubMedGoogle Scholar
  126. 126.
    Münster T, Faigl W, Saedler H, Theissen G (2002) Evolutionary aspects of MADS-box genes in the eusporangiate fern Ophioglossum. Plant Biol 4(4):474–483Google Scholar
  127. 127.
    Svensson ME, Engström P (2002) Closely related MADS-box genes in club moss (Lycopodium) show broad expression patterns and are structurally similar to, but phylogenetically distinct from, typical seed plant MADS-box genes. New Phytol 154(2):439–450Google Scholar
  128. 128.
    Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Munster T, Theissen G, Nozaki H, Ito M (2005) Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci U S A 102(7):2436–2441PubMedCentralPubMedGoogle Scholar
  129. 129.
    Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112(1):1–20PubMedGoogle Scholar
  130. 130.
    Edelman GM, Gally JA (2001) Degeneracy and complexity in biological systems. Proc Natl Acad Sci U S A 98(24):13763–13768PubMedCentralPubMedGoogle Scholar
  131. 131.
    Whitacre JM (2010) Degeneracy: a link between evolvability, robustness and complexity in biological systems. Theor Biol Med Model 7:6PubMedCentralPubMedGoogle Scholar
  132. 132.
    Whitacre J, Bender A (2010) Degeneracy: a design principle for achieving robustness and evolvability. J Theor Biol 263(1):143–153PubMedGoogle Scholar
  133. 133.
    Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jonsson H, Traas J, Meyerowitz EM (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8(10):e1000516PubMedCentralPubMedGoogle Scholar
  134. 134.
    Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci U S A 103(5):1633–1638PubMedCentralPubMedGoogle Scholar
  135. 135.
    Chickarmane VS, Gordon SP, Tarr PT, Heisler MG, Meyerowitz EM (2012) Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc Natl Acad Sci U S A 109(10):4002–4007PubMedCentralPubMedGoogle Scholar
  136. 136.
    Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15(21):1899–1911PubMedGoogle Scholar
  137. 137.
    Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322(5908):1650–1655PubMedGoogle Scholar
  138. 138.
    Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S, Boudaoud A, Kuhlemeier C (2012) Mechanical regulation of auxin-mediated growth. Curr Biol 22(16):1468–1476PubMedGoogle Scholar
  139. 139.
    Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312(5779):1491–1495PubMedGoogle Scholar
  140. 140.
    Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755PubMedGoogle Scholar
  141. 141.
    Philippe H, Brinkmann H, Lavrov DV, Littlewood DT, Manuel M, Worheide G, Baurain D (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9(3):e1000602PubMedCentralPubMedGoogle Scholar
  142. 142.
    Yang Z, Rannala B (2012) Molecular phylogenetics: principles and practice. Nat Rev Genet 13(5):303–314PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, New York 2014

Authors and Affiliations

  1. 1.Smurfit Institute of GeneticsTrinity College DublinDublinIreland
  2. 2.School of Biological SciencesMonash UniversityClaytonAustralia
  3. 3.Centre for Plant Sciences, School of BiologyUniversity of LeedsLeedsUK
  4. 4.Instituto de Biología Molecular y Celular de PlantasConsejo Superior de Investigaciones Científi cas-Universidad Politécnica de ValenciaValenciaSpain
  5. 5.Plant Gene Expression Center, USDA-ARS/UCBerkeleyUSA
  6. 6.Department of Plant and Microbial BiologyUniversity of California at BerkeleyBerkeleyUSA
  7. 7.Department of Plant and Microbial BiologyNorth Carolina State UniversityRaleighUSA
  8. 8.Smurfit Institute of GeneticsTrinity CollegeDublinIreland
  9. 9.Dipartimento di Scienze Biomolecolari e BiotecnologieUniversita degli Studi di MilanoMilanItaly
  10. 10.Temasek Life Sciences LaboratoryNational University of SingaporeSingaporeSingapore
  11. 11.Department of Biological Sciences, Faculty of ScienceNational University of SingaporeSingaporeSingapore
  12. 12.Department of Biological SciencesDartmouth CollegeHanoverUSA
  13. 13.State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina
  14. 14.State Key Laboratory of Genetic Engineering, Institute of Plant Biology, School of Life SciencesFudan UniversityShanghaiChina
  15. 15.Center for Evolutionary Biology, School of Life SciencesFudan UniversityShanghaiChina
  16. 16.Division of BiologyCalifornia Institute of TechnologyPasadenaUSA
  17. 17.Center for Research in Agricultural Genomics CSIC-IRTA- UAB-UBUniversidad Autónoma de BarcelonaBarcelonaSpain
  18. 18.Institució Catalana de Recerca i Estudis AvançatsBarcelonaSpain

Personalised recommendations