Journal of Plant Growth Regulation

, Volume 30, Issue 2, pp 242–254 | Cite as

The Hormonal Regulation of Flower Development

  • J. W. Chandler


Homeotic genes comprising the ABCE classes partly detail the genetic networks that control aspects of floral organ initiation, development, and architecture, but less is known about how these gene functions are translated into changes at the cellular level in growth and cellular differentiation that are involved in the formation of diverse floral organs with specific shapes and sizes. Hormones are the principal transducers of genetic information, and due to recent advances in understanding hormone function in floral development, it is timely to review some of these findings. Flower development is the result of a regulated balance between meristem size and coordination and organ initiation. Floral meristem size is regulated by cytokinin, gibberellin, and auxin, and auxin plays a major role in organ initiation and organogenesis. How hormones contribute to the development of each organ is partly known, with stamen development reliant on almost all hormones, petal development is affected by gibberellins, auxin, and jasmonic acid, and gynoecium development is predominantly regulated by auxin. Furthermore, the interconnections between genetic hierarchies and hormones are being elucidated, and as almost all hormone groups are implicated in floral development, points of hormone crosstalk are being revealed.


Flower development Auxin Floral meristem Gibberellins Inflorescence meristem Genetic hierarchy 



The author gratefully acknowledges financial support from the Deutsche Forschungsgemeinschaft via SFB572.


  1. Abas L, Benjamins R, Malenica N, Paciorek T, Wiśniewska J, Mouliner-Anzola JC, Sieberen T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256PubMedGoogle Scholar
  2. 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 9:841–857PubMedGoogle Scholar
  3. Aloni R, Schwalm K, Langhans K, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis. Planta 216:853–941Google Scholar
  4. Aloni R, Aloni E, Langhaus M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328PubMedGoogle Scholar
  5. 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 5:569–579PubMedGoogle Scholar
  6. Bak S, Tax FE, Reldmann KA, Galbraith DW, Feyereisen R (2001) CYP83B1, a Cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:101–111PubMedGoogle Scholar
  7. Barazesh S, McSteen P (2008) Hormonal control of grass inflorescence development. Trends Plant Sci 13:656–662PubMedGoogle Scholar
  8. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–4067PubMedGoogle Scholar
  9. Bennett M, Alvarez J, Bossinger G, Smyth DR (1995) Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J 8:505–520Google Scholar
  10. Bernier G, Périlleux C (2005) A physiological overview of the genetics of flowering time control. Plant Biotechnol J 3:3–16PubMedGoogle Scholar
  11. Bhalerao RP, Bennett MJ (2003) The case for morphogens in plants. Nat Cell Biol 5:939–943PubMedGoogle Scholar
  12. Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800PubMedGoogle Scholar
  13. Bossinger G, Smyth DR (1996) Initiation patterns of flower and floral organ development in Arabidopsis thaliana. Development 122:1093–1102PubMedGoogle Scholar
  14. Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedGoogle Scholar
  15. 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
  16. Brioudes F, Joly C, Szécsi J, Varaud E, Leroux J, Bellvert F, Bertrand C, Bendahmane M (2009) Jasmonate controls late development stages of petal growth in Arabidopsis thaliana. Plant J 60:1070–1080PubMedGoogle Scholar
  17. Bull-Hereñu K, Claßen-Bockhoff R (2010) Open and closed inflorescences: more than simple opposites. J Exp Bot. doi: 10.1093/jxb/erq262
  18. Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587PubMedGoogle Scholar
  19. Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774PubMedGoogle Scholar
  20. Chandler J (2009) Auxin as compère in plant hormone crosstalk. Planta 231:1–12PubMedGoogle Scholar
  21. Chapple C (1998) Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu Rev Plant Physiol Plant Mol Biol 49:311–343PubMedGoogle Scholar
  22. Cheng Y, Zhao Y (2007) A role for auxin in flower development. J Integr Plant Biol 49:99–104Google Scholar
  23. 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 131:1055–1064PubMedGoogle Scholar
  24. 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
  25. Cheng Y, Qin G, Dai X, Zhao Z (2007) NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis. Proc Natl Acad Sci USA 104:18825–18829PubMedGoogle Scholar
  26. Cheng Y, Qin G, Dai X, Zhao Y (2008) NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis. Proc Natl Acad Sci USA 105:21017–21022PubMedGoogle Scholar
  27. Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5:e1000440PubMedGoogle Scholar
  28. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418PubMedGoogle Scholar
  29. 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
  30. Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451PubMedGoogle Scholar
  31. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedGoogle Scholar
  32. Cowling RJ, Kamiya Y, Seto H, Harberd NP (1998) Gibberellin dose-response regulation of GA4 gene transcript levels in Arabidopsis. Plant Physiol 117:1195–1203PubMedGoogle Scholar
  33. Crone W, Lord EM (1994) Floral initiation and development in wildtype Arabidopsis thaliana (Brassicaceae) and in the organ identity mutants apetala2–1 and agamous-1. Can J Bot 72:384–401Google Scholar
  34. Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239–1241PubMedGoogle Scholar
  35. D’Agostino IB, Kieber JJ (1999) Molecular mechanisms of cytokinin action. Curr Opin Plant Biol 2:359–364PubMedGoogle Scholar
  36. Davis S (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ 32:1201–1210PubMedGoogle Scholar
  37. Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384PubMedGoogle Scholar
  38. Ditta G, Pinyopich A, Robles P, Pealz S, Yanovsky M (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940PubMedGoogle Scholar
  39. Dodsworth S (2009) A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol 336:1–9PubMedGoogle Scholar
  40. Duan QH, Wang DH, Xu ZH, Bai SN (2008) Stamen development in Arabidopsis is arrested by organ-specific overexpression of a cucumber ethylene synthesis gene CsACO2. Planta 228:537–543PubMedGoogle Scholar
  41. Ecklund DM, Ståldal V, Valsecchi I, Cierlik I, Eriksson C, Hiratsu K, Ohme-Takagi M, Sundström JF, Thelander M, Ezcurra I, Sundberg E (2010) The Arabidopsis thaliana STYLISH1 protein acts as a transcriptional activator regulating auxin biosynthesis. Plant Cell 22:349–363Google Scholar
  42. Ellis CM, Nagpall P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) Auxin Response Factor1 and Auxin Response Factor2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574PubMedGoogle Scholar
  43. Eriksson S, Stransfeld L, Adamski NM, Breuninger H, Lenhard M (2010) KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis. Curr Biol 20:527–532PubMedGoogle Scholar
  44. Estruch JJ, Granell A, Hansen G, Prinsen E, Redig P, Van Onckelen H, Schwarz-Sommer Z, Sommer H, Spena A (1993) Floral development and expression of floral homeotic genes are influenced by cytokinins. Plant J 4:379–384PubMedGoogle Scholar
  45. Feng XL, Ni WM, Elge S, Mueller-Roeber B, Xu ZH, Xue HW (2006) Auxin flow in anther filaments is critical for pollen grain development through regulating pollen mitosis. Plant Mol Biol 61:215–226PubMedGoogle Scholar
  46. Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jamonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759PubMedGoogle Scholar
  47. Friml J, Vieten A, Sauer M, Weijers D, Schwaz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153PubMedGoogle Scholar
  48. Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134:3849–3859PubMedGoogle Scholar
  49. Galinha C, Bilsborough G, Tsiantis M (2009) Hormonal input in plant meristems: a balancing act. Semin Cell Dev Biol 20:1149–1156PubMedGoogle Scholar
  50. Gallivotti A, Barazesh S, Malcomber S, Hall D, Jackson D, Schmidt R, McSteen P (2008) Sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proc Natl Acad Sci USA 105:15196–15201Google Scholar
  51. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedGoogle Scholar
  52. Giulini A, Wang J, Jackson D (2004) Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 430:1031–1034PubMedGoogle Scholar
  53. Gómez-Mena C, de Folter S, Costa MMR, Angenent GC, Sablowski R (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132:429–438PubMedGoogle Scholar
  54. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz E (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci U S A 106:16529–16534PubMedGoogle Scholar
  55. Grieneisen VA, Xu J, Marée AFM, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013PubMedGoogle Scholar
  56. Grove M, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen D, Steffens GL, Flippen-Anderson J, Cook JC (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217Google Scholar
  57. Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131:1089–1100PubMedGoogle Scholar
  58. Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type function in plants with different body plans. Curr Biol 12:1557–1565PubMedGoogle Scholar
  59. Hay A, Craft J, Tsiantis M (2004) Plant hormones and homeoboxes: bridging the gap? Bioessays 26:395–404PubMedGoogle Scholar
  60. Hedden P (1999) Recent advances in gibberellin biosynthesis. J Exp Bot 50:553–563Google Scholar
  61. Heisler MGB, Atkinson A, Bylstra YH, Walsh R, Smyth DR (2001) SPATULA, a gene that controls a development of carpel margin tissues in Arabidopsis encodes a bHLH protein. Development 128:1089–1098PubMedGoogle Scholar
  62. Hou X, Hu WW, Shen L, Lee LYC, Tao Z, Han JH, Ju H (2008) Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiol 147:1126–1142PubMedGoogle Scholar
  63. Hu Y, Bao F, Li J (2000) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction. Plant J 24:693–701PubMedGoogle Scholar
  64. Hu Y, Xie Q, Chua NH (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961PubMedGoogle Scholar
  65. Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai WC, Hanada A, Alonso JM, Ecker JR, Swain SM, Yamaguchi S, Kamiya Y, Sun T-p (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20:320–336PubMedGoogle Scholar
  66. Huang S, Cerny RE, Qi Y, Bhat D, Aydt CM, Hanson DD, Malloy KP, Ness L (2003) Transgenic studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol 131:1270–1282PubMedGoogle Scholar
  67. Hutchison KW, Singer PB, McInnes S, Diaz-Sala C, Greenwood MS (1999) Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin. Plant Physiol 120:827–831PubMedGoogle Scholar
  68. Inada S, Shimmen T (2001) Involvement of cortical microtubules in plastic extension regulated by gibberellin in Lemna minor root. Plant Cell Physiol 42:395–403PubMedGoogle Scholar
  69. 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 19:3516–3529PubMedGoogle Scholar
  70. Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16:S1–S17PubMedGoogle Scholar
  71. Jacobsen SE, Olszewski NE (1991) Characterization of the arrest in anther development associated with gibberellin deficiency of the gib-1 mutant of tomato. Plant Physiol 97:409–414PubMedGoogle Scholar
  72. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Philips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565PubMedGoogle Scholar
  73. Kahana A, Silberstein L, Kessler N, Goldstein RS, Perl-Treves R (1999) Expression of ACC oxidase genes differs among sex genotypes and sex phases in cucumber. Plant Mol Biol 41:517–528PubMedGoogle Scholar
  74. Kanno A, Saeki H, Kameya T, Saedler H, Theissen G (2003) Heterotropic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol Biol 52:831–841PubMedGoogle Scholar
  75. Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent G (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:1000090Google Scholar
  76. Kaufmann K, Wellmer F, Muiño JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueño F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89PubMedGoogle Scholar
  77. Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21:3839–3849PubMedGoogle Scholar
  78. Koornneef M, van der Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 58:257–263Google Scholar
  79. Krizek BA, Fletcher J (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698PubMedGoogle Scholar
  80. Kuppusamy KT, Walcher CL, Nemhauser J (2009) Cross-regulatory mechanisms in hormone signaling. Plant Mol Biol 69:375–381PubMedGoogle Scholar
  81. Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652–655PubMedGoogle Scholar
  82. Kuusk S, Sohlberg JJ, Ecklund M, Sundberg E (2006) Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner. Plant J 47:99–111PubMedGoogle Scholar
  83. Lamb RS, Hill TA, Tan QK, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086PubMedGoogle Scholar
  84. Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96PubMedGoogle Scholar
  85. 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
  86. Leyser O (2005) Auxin distribution and plant pattern formation: how many angels can dance on the point of PIN? Cell 121:819–822PubMedGoogle Scholar
  87. Li X, Qin G, Chen Z, Gu H, Qu LJ (2008) A gain-of-function mutation of transcriptional factor PTL results in curly leaves, dwarfism and male sterility by affecting auxin homeostasis. Plant Mol Biol 66:315–327PubMedGoogle Scholar
  88. Li XG, Su YH, Zhao XY, Li W, Gao XQ, Zhang XS (2010) Cytokinin overproduction-caused alteration of flower development is partially mediated by CUC2 and CUC3 in Arabidopsis. Gene 450:109–120PubMedGoogle Scholar
  89. Lindsay DL, Sawhney VP, Bonham-Smith PC (2006) Cytokinin-induced changes in CLAVATA1 and WUSCHEL expression temporally coincide with altered floral development in Arabidopsis. Plant Sci 170:1111–1117Google Scholar
  90. Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Somin R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803PubMedGoogle Scholar
  91. Mandaokar A, Kumar VD, Amway M, Browse J (2003) Microarray and differential display identify genes involved in jasmonate-dependent anther development. Plant Mol Biol 52:775–786PubMedGoogle Scholar
  92. Mandaokar A, Thines B, Shin B, Lange BM, Choi G, Koo YJ, Choi YD, Choi G, Browse J (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profilig. Plant J 46:984–1008PubMedGoogle Scholar
  93. McSteen P (2010) Auxin and monocot development. Cold Spring Harb Perspect Biol 2(3):a001479PubMedGoogle Scholar
  94. McSteen P, Malcomber S, Skirpan A, Lunde C, Wu X, Kellogg E, Hake S (2007) Barren inflorescence2 encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiol 144:1000–1011PubMedGoogle Scholar
  95. Mikkelsen MD, Hansen CH, Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275:33712–33717PubMedGoogle Scholar
  96. Morita Y, Kyozuka J (2007) Characterisation of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport. Plant Cell Physiol 48:540–549PubMedGoogle Scholar
  97. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:111–130Google Scholar
  98. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed J (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118PubMedGoogle Scholar
  99. Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127:3877–3888PubMedGoogle Scholar
  100. Ng KH, Yu H, Ito T (2009) AGAMOUS controls GIANT KILLER, a multifunctional chromatin modifier in reproductive organ patterning and differentiation. PLoS Biol 7:e1000251PubMedGoogle Scholar
  101. Ogawa T, Uchimiya H, Yamada MK (2007) Mutual regulation of Arabidopsis thaliana ethylene-responsive element binding protein and a plant floral homeotic gene, APETALA2. Ann Bot 99:239–244PubMedGoogle Scholar
  102. Olszewski NE, Sun T, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism and response pathways. Plant Cell S2002:s61–s80Google Scholar
  103. Østergaard L (2008) Don’t leaf now. The making of a fruit. Curr Opin Plant Biol 12:1–6Google Scholar
  104. Pagnussat GC, Alante-Saez M, Bowman J, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–1689PubMedGoogle Scholar
  105. Peer WA, Banyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898–1911PubMedGoogle Scholar
  106. Pekker I, Alvarez JP, Esched Y (2005) Auxin response factors mediate Arabidopsis organ symmetry via modulation of Kanadi activity. Plant Cell 17:2899–2910PubMedGoogle Scholar
  107. Pelaz S, Tapia-López R, Alvarez-Buylla ER, Yanovsky M (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 11:182–184PubMedGoogle Scholar
  108. Pfluger J, Zambryski P (2004) The role of SEUSS in auxin response and floral organ patterning. Development 131:4697–4707PubMedGoogle Scholar
  109. Przemeck GK, Mattsson J, Hardtke CS, Sung ZR, Berleth T (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200:229–237PubMedGoogle Scholar
  110. Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol 135:978–988PubMedGoogle Scholar
  111. Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274PubMedGoogle Scholar
  112. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518PubMedGoogle Scholar
  113. 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
  114. Rieu I, Ruiz-Rivero O, Fernadez-Garcia N, Griffiths J, Powers SJ, Gong F, Linhartova T, Eriksson S, Nilsson O, Thomas SG, Phillips AL, Hedden P (2008) The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J 53:488–504PubMedGoogle Scholar
  115. Růžička K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212PubMedGoogle Scholar
  116. Sablowski R (2010) Genes and functions controlled by floral identity genes. Semin Cell Dev Biol 21:94–99PubMedGoogle Scholar
  117. Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The Auxin Response Factor 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261PubMedGoogle Scholar
  118. Sessions RA, Zambryski PC (1995) Arabidopsis gynoecium structure in the wild type and in ettin mutants. Development 121:1519–1532PubMedGoogle Scholar
  119. Sessions RA, Nemhauser JL, McCall A, Roe JL, Feldman KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481–4491PubMedGoogle Scholar
  120. Silverstone AL, Chang C-w, Krol E, Sun T-p (1997) Developmental regulation of the biosynthetic gene GA1 in Arabidopsis thaliana. Plant J 12:9–19PubMedGoogle Scholar
  121. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedGoogle Scholar
  122. Sohlberg JJ, Myrenås M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E (2006) STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. Plant J 47:112–123PubMedGoogle Scholar
  123. Ståldal V, Sundberg E (2009) The role of auxin in style development and apical-basal patterning of the Arabidopsis thaliana gynoecium. Plant Sig Behav 4:83–85Google Scholar
  124. Stinzi A, Browse J (2000) The Arabidopsis male-sterile mutant opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:12837–12842Google Scholar
  125. Szécsi J, Joly C, Bordji K, Varaud E, Cock JM, Dumas C, Bendahmane M (2006) BIGPETALp, a bHLH transcription factor, is involved in the control of Arabidopsis petal size. EMBO J 25:3912–3920PubMedGoogle Scholar
  126. Tabata R, Ikezaki M, Fujibe T, Aida M, Tian C, 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
  127. Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85PubMedGoogle Scholar
  128. Tobeña-Santamaria R, Bliek M, Ljung K, Sandberg G, Mol JN, Souer E, Koes R (2002) FLOOZY of Petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture. Genes Dev 16:753–763PubMedGoogle Scholar
  129. Treml BS, Winderl S, Radykewicz R, Herz M, Schweizer G, Hutzler P, Glawischnig E, Torres-Ruiz RA (2005) The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development 132:4063–4074PubMedGoogle Scholar
  130. Veit B (2009) Hormone mediated regulation of the shoot apical meristem. Plant Mol Biol 69:397–408PubMedGoogle Scholar
  131. Venglat SP, Sawhney VK (1996) Benzylaminopurine induces phenocopies of floral meristem and organ identity mutants in wild-type Arabidopsis plants. Planta 198:480–487PubMedGoogle Scholar
  132. Vroemen CW, Mordhurst AP, Albrecht C, Kwaaitaal MACJ, De Vries S (2003) The CUP-SHAPED COTLYEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15:1563–1577PubMedGoogle Scholar
  133. Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584PubMedGoogle Scholar
  134. Wang Z, Liang Y, Li C, Xu Y, Lan L, Zhao D, Chen C, Xu Z, Xue Y, Chong K (2005) Microarray analysis for gene expression involved in anther development in rice (Oryza sativa L.). Plant Mol Biol 58:721–737PubMedGoogle Scholar
  135. Weiss J, Delgado-Benarroch L, Egea-Cortines M (2005) Genetic control of floral size and proportions. Int J Dev Biol 49:513–525PubMedGoogle Scholar
  136. Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326PubMedGoogle Scholar
  137. Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PloS 2:e117Google Scholar
  138. Wenzel CL, Schuetz M, Yu Q, Mattsson J (2007) Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49:387–398PubMedGoogle Scholar
  139. Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt R (2004) Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131:6083–6091PubMedGoogle Scholar
  140. 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 USA 101:1775–1780PubMedGoogle Scholar
  141. Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130PubMedGoogle Scholar
  142. Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408PubMedGoogle Scholar
  143. Xu YL, Li L, Gage DA, Zeevaart JA (1998) Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis. Plant Cell 11:927–936Google Scholar
  144. Yadav SR, Vijayraghavan U (2008) OsMADS1 as a transcriptional regulator of rice floral organ fate affects auxin and cytokinin signaling pathways. Dev Biol 319:587–598Google Scholar
  145. Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T (2007) Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol 143:1362–1371PubMedGoogle Scholar
  146. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOX proteins activate cytokinin biosynthesis. Curr Biol 15:1566–1571PubMedGoogle Scholar
  147. Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H, Wenig X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc Natl Acad Sci USA 107:6100–6105PubMedGoogle Scholar
  148. Yu H, Ito T, Zhao YX, Peng JR, Kumar P, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 101:7827–7832PubMedGoogle Scholar
  149. Zhang J, Nodzyńskia T, Pěnčík A, Rolčík J, Friml J (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA 107:918–922PubMedGoogle Scholar
  150. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465(7301):1089–1092PubMedGoogle Scholar
  151. Ziegelhoffer EC, Medrano LJ, Meyerowitz EM (2000) Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development. Proc Natl Acad Sci USA 97:7633–7638PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Institute of Developmental Biology, Cologne Bioresearch CentreCologneGermany

Personalised recommendations