Flower Development in Arabidopsis: There Is More to It Than Learning Your ABCs

  • Nathanaël Prunet
  • Thomas P. JackEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1110)


The field of Arabidopsis flower development began in the early 1980s with the initial description of several mutants including apetala1, apetala2, and agamous that altered floral organ identity (Koornneef and van der Veen, Theor Appl Genet 58:257–263, 1980; Koornneef et al., J Hered 74:265–272, 1983). By the end of the 1980s, these mutants were receiving more focused attention to determine precisely how they affected flower development (Komaki et al., Development 104:195–203, 1988; Bowman et al., Plant Cell 1:37–52, 1989). In the last quarter century, impressive progress has been made in characterizing the gene products and molecular mechanisms that control the key events in flower development. In this review, we briefly summarize the highlights of work from the past 25 years but focus on advances in the field in the last several years.


Flower development Arabidopsis Meristem Transcription factor Transcriptional network Floral determinacy Boundary Founder cells Homeotic genes 


  1. 1.
    Koornneef M, van der Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 58:257–263PubMedGoogle Scholar
  2. 2.
    Koornneef M, van Elden J, Hanhart CJ, Stam P, Braaksma FJ, Feenstra WJ (1983) Linkage map of Arabidopsis thaliana. J Hered 74:265–272Google Scholar
  3. 3.
    Komaki MK, Okada K, Nishino E, Shimura Y (1988) Isolation and characterization of novel mutants of Arabidopsis thaliana defective in flower development. Development 104:195–203Google Scholar
  4. 4.
    Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52PubMedCentralPubMedGoogle Scholar
  5. 5.
    Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedCentralPubMedGoogle Scholar
  6. 6.
    Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedGoogle Scholar
  7. 7.
    Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedGoogle Scholar
  8. 8.
    Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277PubMedGoogle Scholar
  9. 9.
    Jofuku KD, den Boer BGW, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225PubMedCentralPubMedGoogle Scholar
  10. 10.
    Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560PubMedGoogle Scholar
  11. 11.
    Jack T, Brockman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697PubMedGoogle Scholar
  12. 12.
    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 346:35–39PubMedGoogle Scholar
  13. 13.
    Mizukami Y, Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71:119–131PubMedGoogle Scholar
  14. 14.
    Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky MF (1992) Manipulation of flower structure in transgenic tobacco. Cell 71:133–143PubMedGoogle Scholar
  15. 15.
    Krizek BA, Meyerowitz EM (1996) The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122:11–22PubMedGoogle Scholar
  16. 16.
    Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203PubMedGoogle Scholar
  17. 17.
    Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940PubMedGoogle Scholar
  18. 18.
    Theissen G, Saedler H (2001) Floral quartets. Nature 409:469–471PubMedGoogle Scholar
  19. 19.
    Theissen G (2001) Development of floral organ identity; stories from the MADS house. Curr Opin Plant Biol 4:75–85PubMedGoogle Scholar
  20. 20.
    Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101PubMedGoogle Scholar
  21. 21.
    Riechmann JL, Meyerowitz EM (1998) The AP2/EBEBP family of plant transcription factors. Biol Chem 379:633–646PubMedGoogle Scholar
  22. 22.
    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 93:4793–4798PubMedCentralPubMedGoogle Scholar
  23. 23.
    Riechmann JL, Wang M, Meyerowitz EM (1996) DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res 24:3134–3141PubMedCentralPubMedGoogle Scholar
  24. 24.
    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 18:5370–5379PubMedGoogle Scholar
  25. 25.
    Fan H-Y, Hu Y, Tudor M, Ma H (1997) Specific interactions between K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J 12:999–1010PubMedGoogle Scholar
  26. 26.
    Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529PubMedGoogle Scholar
  27. 27.
    Immink RG, Tonaco IA, de Folter S, Shchennikova A, van Dijk AD, Busscher-Lange J, Borst JW, Angenent GC (2009) SEPALLATA3: the ‘glue’ for MADS box transcription factor complex formation. Genome Biol 10:R24PubMedCentralPubMedGoogle Scholar
  28. 28.
    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 109:1560–1565PubMedCentralPubMedGoogle Scholar
  29. 29.
    Pelaz S, Tapia-Lopez R, Alvarez-Buylla ER, Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 11:182–184PubMedGoogle Scholar
  30. 30.
    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
  31. 31.
    Melzer R, Verelst W, Theissen G (2009) The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro. Nucleic Acids Res 37:144–157PubMedCentralPubMedGoogle Scholar
  32. 32.
    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
  33. 33.
    Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR (1993) Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119:721–743Google Scholar
  34. 34.
    Castillejo C, Romera-Branchat M, Pelaz S (2005) A new role of the Arabidopsis SEPALLATA3 gene revealed by its constitutive expression. Plant J 43:586–596PubMedGoogle Scholar
  35. 35.
    Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2:741–753PubMedCentralPubMedGoogle Scholar
  36. 36.
    Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002PubMedGoogle Scholar
  37. 37.
    Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025PubMedGoogle Scholar
  38. 38.
    Wollmann H, Mica E, Todesco M, Long JA, Weigel D (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137:3633–3642PubMedGoogle Scholar
  39. 39.
    Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741PubMedCentralPubMedGoogle Scholar
  40. 40.
    Zhao L, Kim Y-J, Dinh TT, Chen X (2007) miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J 51:840–849PubMedCentralPubMedGoogle Scholar
  41. 41.
    Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527PubMedGoogle Scholar
  42. 42.
    Jung J-H, Seo J-H, Reyes JL, Yun J, Chua NH, Park C-M (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19:2736–2748PubMedCentralPubMedGoogle Scholar
  43. 43.
    Wurschum T, Gross-Hardt R, Laux T (2006) APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18:295–307PubMedCentralPubMedGoogle Scholar
  44. 44.
    Long JA, Woody S, Poethig S, Meyerowitz EM, Barton MK (2002) Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129:2797–2806PubMedGoogle Scholar
  45. 45.
    Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523PubMedGoogle Scholar
  46. 46.
    Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386PubMedGoogle Scholar
  47. 47.
    Smith ZR, Long JA (2010) Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464:423–426PubMedCentralPubMedGoogle Scholar
  48. 48.
    Krogan NT, Hogan K, Long JA (2012) APETALA2 recruits the co-repressor TOPLESS and histone deacetylase HDA19 to negatively regulate multiple floral organ identity genes in Arabidopsis. Development 139:4189–4190Google Scholar
  49. 49.
    Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438PubMedCentralPubMedGoogle Scholar
  50. 50.
    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 22:2156–2170PubMedCentralPubMedGoogle Scholar
  51. 51.
    Bomblies K, Dagenais N, Weigel D (1999) Redundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2. Dev Biol 216:260–264PubMedGoogle Scholar
  52. 52.
    Deyholos M, Sieburth L (2000) Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron. Plant Cell 12:1799–1810PubMedCentralPubMedGoogle Scholar
  53. 53.
    Dinh TT, Girke T, Liu X, Yant L, Schmid M, Chen X (2012) The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139:1978–1986PubMedGoogle Scholar
  54. 54.
    Wilkinson MD, Haughn GW (1995) UNUSUAL FLORAL ORGANS controls meristem identity and organ primordia fate in Arabidopsis. Plant Cell 7:1485–1499PubMedCentralPubMedGoogle Scholar
  55. 55.
    Levin JZ, Meyerowitz EM (1995) UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7:529–548PubMedCentralPubMedGoogle Scholar
  56. 56.
    Lee I, Wolfe DS, Weigel D (1997) A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr Biol 7:95–104PubMedGoogle Scholar
  57. 57.
    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 135:1235–1245PubMedGoogle Scholar
  58. 58.
    Sablowski RWM, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103PubMedGoogle Scholar
  59. 59.
    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 20:430–443PubMedGoogle Scholar
  60. 60.
    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 328:85–89PubMedGoogle Scholar
  61. 61.
    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:e1000090PubMedCentralPubMedGoogle Scholar
  62. 62.
    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 33:13452–13457Google Scholar
  63. 63.
    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 23:1791–1804PubMedGoogle Scholar
  64. 64.
    Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360PubMedGoogle Scholar
  65. 65.
    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 19:3516–3529PubMedCentralPubMedGoogle Scholar
  66. 66.
    Busch W, Miotk A, Ariel FD, Zhao Z, Forner J, Daum G, Suzaki T, Schuster C, Schultheiss SJ, Leibfried A, Haubeiss S, Ha N, Chan RL, Lohmann JU (2010) Transcriptional control of a plant stem cell niche. Dev Cell 18:849–861PubMedGoogle Scholar
  67. 67.
    Chandler JW (2011) Founder cell specification. Trends Plant Sci 16:607–613PubMedGoogle Scholar
  68. 68.
    Hill JP, Lord EM (1989) Floral development in Arabidopsis thaliana: a comparison of the wild-type and the homeotic pistillata mutant. Can J Bot 67:2922–2936Google Scholar
  69. 69.
    Bossinger G, Smyth DR (1996) Initiation patterns of flower and floral organ development in Arabidopsis thaliana. Development 122:1093–1102PubMedGoogle Scholar
  70. 70.
    Crone W, Lord EM (1994) Floral initiation and development in wild-type Arabidopsis thaliana (Brassicaceae) and in the organ identity mutants apetala2-1 and agamous-1. Can J Bot 72:384–401Google Scholar
  71. 71.
    Jenik PD, Irish VF (2000) Regulation of cell proliferation patterns by homeotic genes during Arabidopsis floral development. Development 127:1267–1276PubMedGoogle Scholar
  72. 72.
    Furner IJ, Pumphrey J (1993) Cell fate in the inflorescence meristem and floral buttress of Arabidopsis thaliana. Plant J 4:917–931Google Scholar
  73. 73.
    Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684PubMedCentralPubMedGoogle Scholar
  74. 74.
    Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518PubMedCentralPubMedGoogle Scholar
  75. 75.
    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 426:255–260PubMedGoogle Scholar
  76. 76.
    Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799PubMedGoogle Scholar
  77. 77.
    Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191PubMedGoogle Scholar
  78. 78.
    Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118PubMedGoogle Scholar
  79. 79.
    Tabata R, Ikezaki M, Fujibe T, Aida M, Tian CE, Ueno Y, Yamamoto KT, Machida Y, Nakamura K, Ishiguro S (2010) Arabidopsis auxin response factor6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51:164–175PubMedGoogle Scholar
  80. 80.
    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 15:1899–1911PubMedGoogle Scholar
  81. 81.
    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 76:171–185PubMedGoogle Scholar
  82. 82.
    Lampugnani ER, Kilinc A, Smyth DR (2012) Auxin controls petal initiation in Arabidopsis. Development 140:185–194PubMedGoogle Scholar
  83. 83.
    Nag A, Yang Y, Jack T (2007) DORNRÖSCHEN-LIKE, and AP2 gene necessary for stamen emergence in Arabidopsis. Plant Mol Biol 65:219–232PubMedGoogle Scholar
  84. 84.
    Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci U S A 100:2987–2991PubMedCentralPubMedGoogle Scholar
  85. 85.
    Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916PubMedGoogle Scholar
  86. 86.
    Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120PubMedGoogle Scholar
  87. 87.
    Breuil-Broyer S, Morel P, de Almeida-Engler J, Coustham V, Negrutiu I, Trehin C (2004) High-resolution boundary analysis during Arabidopsis thaliana flower development. Plant J 38:182–192PubMedGoogle Scholar
  88. 88.
    Schultz EA, Pickett FB, Haughn GW (1991) The FLO10 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers. Plant Cell 3:1221–1237PubMedCentralPubMedGoogle Scholar
  89. 89.
    Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114:599–615PubMedGoogle Scholar
  90. 90.
    Sakai H, Krizek BA, Jacobsen SE, Meyerowitz EM (2000) Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem development. Plant Cell 12:1607–1618PubMedCentralPubMedGoogle Scholar
  91. 91.
    Aida M, Ishida T, Fukaki H, Fujusawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857PubMedCentralPubMedGoogle Scholar
  92. 92.
    Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15:1563–1577PubMedCentralPubMedGoogle Scholar
  93. 93.
    Baker CC, Sieber P, Wellmer F, Meyerowitz EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr Biol 15:303–315PubMedGoogle Scholar
  94. 94.
    Aida M, Tasaka M (2006) Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex. Plant Mol Biol 60:915–928PubMedGoogle Scholar
  95. 95.
    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 131:4311–4322PubMedGoogle Scholar
  96. 96.
    Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) Micro-RNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046PubMedGoogle Scholar
  97. 97.
    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 134:1051–1060PubMedGoogle Scholar
  98. 98.
    Larue CT, Wen J, Walker JC (2009) A microRNA-transcription factor module regulates lateral organ size and patterning in Arabidopsis. Plant J 58:450–463PubMedGoogle Scholar
  99. 99.
    Griffith ME, da Silva Conceicao A, Smyth DR (1999) PETAL LOSS gene regulates initiation and orientation of second whorl organs in the Arabidopsis flower. Development 126:5635–5644PubMedGoogle Scholar
  100. 100.
    Brewer PB, Howles PA, Dorian K, Griffith ME, Ishida T, Kaplan-Levy RN, Kilinc A, Smyth DR (2004) PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower. Development 131:4035–4045PubMedGoogle Scholar
  101. 101.
    Lampugnani ER, Kilinc A, Smyth DR (2012) PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana. Plant J 71:724–735PubMedGoogle Scholar
  102. 102.
    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
  103. 103.
    Takeda S, Matsumoto N, Okada K (2004) RABBIT EARS, encoding a SUPERMAN-like zinc finger protein, regulates petal development in Arabidopsis thaliana. Development 131:425–434PubMedGoogle Scholar
  104. 104.
    Huang T, Lopez-Giraldez F, Townsend JP, Irish VF (2012) RBE controls microRNA164 expression to effect floral organogenesis. Development 139:2161–2169PubMedGoogle Scholar
  105. 105.
    Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991PubMedGoogle Scholar
  106. 106.
    Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378:199–203PubMedGoogle Scholar
  107. 107.
    Jack T, Fox GL, Meyerowitz EM (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and post-transcriptional regulation determine floral organ identity. Cell 76:703–716PubMedGoogle Scholar
  108. 108.
    Prunet N, Morel P, Negrutiu I, Trehin C (2009) Time to stop: flower meristem termination. Plant Physiol 150:1764–1772PubMedCentralPubMedGoogle Scholar
  109. 109.
    Hiratsu K, Ohta M, Matsui K, Ohme-Takagi M (2002) The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowers. FEBS Lett 514:351–354PubMedGoogle Scholar
  110. 110.
    Yun JY, Weigel D, Lee I (2002) Ectopic expression of SUPERMAN suppresses development of petals and stamens. Plant Cell Physiol 43:52–57PubMedGoogle Scholar
  111. 111.
    Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G (1997) A polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44–51PubMedGoogle Scholar
  112. 112.
    Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM (2004) HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell 16:2586–2600PubMedCentralPubMedGoogle Scholar
  113. 113.
    Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619PubMedGoogle Scholar
  114. 114.
    Jaber E, Thiele K, Kindzierski V, Loderer C, Rybak K, Jurgens G, Mayer U, Sollner R, Wanner G, Assaad FF (2010) A putative TRAPPII tethering factor is required for cell plate assembly during cytokinesis in Arabidopsis. New Phytol 187:751–763PubMedGoogle Scholar
  115. 115.
    Clark SE, Running M, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418PubMedGoogle Scholar
  116. 116.
    Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067Google Scholar
  117. 117.
    Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851PubMedGoogle Scholar
  118. 118.
    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 131:3737–3749PubMedGoogle Scholar
  119. 119.
    Sieburth LE, Running MP, Meyerowitz EM (1995) Genetic separation of third and fourth whorl functions of AGAMOUS. Plant Cell 7:1249–1258PubMedCentralPubMedGoogle Scholar
  120. 120.
    Alvarez J, Smyth DR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126:2356–2375Google Scholar
  121. 121.
    Das P, Ito T, Wellmer F, Vernoux T, Dedieu A, Traas J, Meyerowitz EM (2009) Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development 136:1605–1611PubMedGoogle Scholar
  122. 122.
    Fletcher JC (2001) The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 128:1323–1333PubMedGoogle Scholar
  123. 123.
    Jacobsen SE, Running MP, Meyerowitz EM (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126:5231–5243PubMedGoogle Scholar
  124. 124.
    Ji L, Liu X, Yan J, Wang W, Yumul RE, Kim YJ, Dinh TT, Liu J, Cui X, Zheng B, Agarwal M, Liu C, Cao X, Tang G, Chen X (2011) ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 7:e1001358PubMedCentralPubMedGoogle Scholar
  125. 125.
    Liu X, Huang J, Wang Y, Khanna K, Xie Z, Owen HA, Zhao D (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 416–428Google Scholar
  126. 126.
    Liu X, Kim YJ, Muller R, Yumul RE, Liu C, Pan Y, Cao X, Goodrich J, Chen X (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of polycomb group proteins. Plant Cell 23:3654–3670PubMedCentralPubMedGoogle Scholar
  127. 127.
    Maier AT, Stehling-Sun S, Wollmann H, Demar M, Hong RL, Haubeiss S, Weigel D, Lohmann JU (2009) Dual roles of the bZIP transcription factor PERIANTHIA in the control of floral architecture and homeotic gene expression. Development 136:1613–1620PubMedGoogle Scholar
  128. 128.
    Prunet N, Morel P, Thierry AM, Eshed Y, Bowman JL, Negrutiu I, Trehin C (2008) REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell 20:901–919PubMedCentralPubMedGoogle Scholar
  129. 129.
    Sun B, Ito T (2010) Floral stem cells: from dynamic balance towards termination. Biochem Soc Trans 38:613–616PubMedGoogle Scholar
  130. 130.
    Zuniga-Mayo VM, Marsch-Martinez N, de Folter S (2012) JAIBA, a class-II HD-ZIP transcription factor involved in the regulation of meristematic activity, and important for correct gynoecium and fruit development in Arabidopsis. Plant J 71:314–326PubMedGoogle Scholar
  131. 131.
    Yumul RE, Kim YJ, Liu X, Wang R, Xiao L, Chen X (2013) POWERDRESS and diversified expression of the MIR172 gene family bolster the floral stem cell network. PLoS Genet 9(1):e1003218PubMedCentralPubMedGoogle Scholar
  132. 132.
    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 126:2387–2396PubMedGoogle Scholar
  133. 133.
    Carles CC, Fletcher JC (2009) The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev 23:2723–2728PubMedGoogle Scholar
  134. 134.
    Cheng Y, Kato N, Wang W, Li J, Chen X (2003) Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev Cell 4:53–66PubMedGoogle Scholar
  135. 135.
    Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Genet Dev 11:449–456PubMedGoogle Scholar
  136. 136.
    Smith MR, Willmann MR, Wu G, Berardini TZ, Moller B, Weijers D, Poethig RS (2009) Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc Natl Acad Sci U S A 106:5424–5429PubMedCentralPubMedGoogle Scholar
  137. 137.
    Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135:1481–1491PubMedGoogle Scholar
  138. 138.
    Williams L, Grigg SP, Xie M, Christensen C, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668PubMedGoogle Scholar
  139. 139.
    Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76PubMedCentralPubMedGoogle Scholar
  140. 140.
    Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–180PubMedGoogle Scholar
  141. 141.
    Chen X, Liu J, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129:1085–1094PubMedGoogle Scholar
  142. 142.
    Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495PubMedGoogle Scholar
  143. 143.
    Cartolano M, Castillo R, Efremova N, Kuckenberg M, Zethof J, Gerats T, Schwartz-Sommer Z (2007) A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nat Genet 39:901–905PubMedGoogle Scholar
  144. 144.
    Jack T, Sieburth L, Meyerowitz EM (1997) Targeted misexpression of AGAMOUS in whorl 2 of Arabidopsis flowers. Plant J 11:825–839PubMedGoogle Scholar
  145. 145.
    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 132:429–438PubMedGoogle Scholar
  146. 146.
    Chuang C-F, Meyerowitz EM (2000) Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc Natl Acad Sci U S A 97:4985–4990PubMedCentralPubMedGoogle Scholar
  147. 147.
    Mizukami Y, Ma H (1995) Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA. Plant Mol Biol 28:767–784PubMedGoogle Scholar
  148. 148.
    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
  149. 149.
    Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815PubMedGoogle Scholar
  150. 150.
    Sieburth LE, Drews GN, Meyerowitz EM (1998) Non-autonomy of AGAMOUS function in flower development: use of a Cre/loxP method for mosaic analysis in Arabidopsis. Development 125:4303–4312PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, New York 2014

Authors and Affiliations

  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA

Personalised recommendations