Plant Reproduction

, Volume 31, Issue 1, pp 89–105 | Cite as

Regulation of floral meristem activity through the interaction of AGAMOUS, SUPERMAN, and CLAVATA3 in Arabidopsis

  • Akira Uemura
  • Nobutoshi Yamaguchi
  • Yifeng Xu
  • WanYi Wee
  • Yasunori Ichihashi
  • Takamasa Suzuki
  • Arisa Shibata
  • Ken Shirasu
  • Toshiro Ito
Original Article
Part of the following topical collections:
  1. Plant Reproduction Research in Asia

Key message

Floral meristem size is redundantly controlled by CLAVATA3, AGAMOUS , and SUPERMAN in Arabidopsis.


The proper regulation of floral meristem activity is key to the formation of optimally sized flowers with a fixed number of organs. In Arabidopsis thaliana, multiple regulators determine this activity. A small secreted peptide, CLAVATA3 (CLV3), functions as an important negative regulator of stem cell activity. Two transcription factors, AGAMOUS (AG) and SUPERMAN (SUP), act in different pathways to regulate the termination of floral meristem activity. Previous research has not addressed the genetic interactions among these three genes. Here, we quantified the floral developmental stage-specific phenotypic consequences of combining mutations of AG, SUP, and CLV3. Our detailed phenotypic and genetic analyses revealed that these three genes act in partially redundant pathways to coordinately modulate floral meristem sizes in a spatial and temporal manner. Analyses of the ag sup clv3 triple mutant, which developed a mass of undifferentiated cells in its flowers, allowed us to identify downstream targets of AG with roles in reproductive development and in the termination of floral meristem activity. Our study highlights the role of AG in repressing genes that are expressed in organ initial cells to control floral meristem activity.


Arabidopsis thaliana Floral meristem CLAVATA3 AGAMOUS SUPERMAN Reproductive development 



The authors would like to thank Akie Takahashi and Taeko Kawakami for technical assistance, and Elliot Meyerowitz for providing pWUS::GFP-ER lines. This work was supported by Grants from Japan Science and Technology Agency “Precursory Research for Embryonic Science and Technology (No. JPMJPR15QA),” a JSPS KAKENHI (No. 16H01468), the NAIST Foundation, the Sumitomo Foundation, the Takeda Foundation, and the Mishima Kaiun Memorial Foundation to N.Y.; a Grant from JSPS KAKENHI (No. 15H05955) to T. S.; a Grant from Japan Science and Technology Agency “Precursory Research for Embryonic Science and Technology (No. JPMJPR15Q2)” to Y.I.; Grants from JSPS KAKENHI (Nos. 15H05959 and 17H06172) to K.S.; and Grants from the NAIST Foundation, the Mitsubishi Foundation, and JSPS KAKENHI (15H01234, 15H01356, 15H02405, and 17H05843) to T.I.

Supplementary material

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  1. Adamczyk BJ, Lehti-Shiu MD, Fernandez DE (2007) The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. Plant J 50:1007–1019CrossRefPubMedGoogle 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 9:841–857CrossRefPubMedPubMedCentralGoogle Scholar
  3. Besnard F, Refahi Y, Morin V, Marteaux B, Brunoud G, Chambrier P, Rozier F, Mirabet V, Legrand J, Laine S, Thevenon E, Farcot E, Cellier C, Das P, Bishopp A, Dumas R, Parcy F, Helariutta Y, Boudaoud A, Godin C, Traas J, Guedon Y, Vernoux T (2014) Cytokinin signaling inhibitory fields provide robustness to phyllotaxis. Nature 505:417–421CrossRefPubMedGoogle Scholar
  4. Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844PubMedGoogle Scholar
  5. Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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
  7. Brand U, Fletcher JC, Hode M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619CrossRefPubMedGoogle Scholar
  8. Breuil-Broyer S, Trehin C, Morel P, Boltz V, Sun B, Chambrier P, Ito T, Negrutiu I (2016) Analysis of the Arabidopsis superman allelic series and the interactions with other genes demonstrate developmental robustness and joint specification of male–female boundary, flower meristem termination and carpel compartmentalization. Ann Bot 117:905–923CrossRefPubMedPubMedCentralGoogle Scholar
  9. Byzova MV, Franken J, Aarts MG, de Almeida-Engler J, Engler G, Mariani C, Van Lookeren Campagne MM, Angenent GC (1999) Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. Gene Dev 13:1002–1014CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 135:1235–1245CrossRefPubMedGoogle Scholar
  11. Chandler JW (2011) Founder cell specification. Trends Plant Sci 16:607–613CrossRefPubMedGoogle Scholar
  12. Chandler JW, Werr W (2014) Arabidopsis floral phytomer development: auxin response relative to biphasic modes of organ initiation. J Exp Bot 65:3097–3110CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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
  14. Crawford BCW, Yanofsky MF (2011) HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development 138:2999–3009CrossRefPubMedGoogle Scholar
  15. Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS (2013) Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. PNAS 110:7074–7079CrossRefPubMedPubMedCentralGoogle Scholar
  16. Doerner P (2001) Plant meristems: a menage a trois to end it all. Curr Biol 11:785–787CrossRefGoogle Scholar
  17. Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14:547–558CrossRefPubMedPubMedCentralGoogle Scholar
  18. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914CrossRefPubMedGoogle Scholar
  20. Frerichs A, Thoma R, Abdallah AT, Frommolt P, Werr W, Chandler JW (2016) The founder-cell transcriptome in the Arabidopsis apetala1 cauliflower inflorescence meristem. BMC Genom 17:855CrossRefGoogle Scholar
  21. 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 132:429–438CrossRefPubMedGoogle Scholar
  22. Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of Arabidopsis shoot meristem. Development 134:3539–3548CrossRefPubMedGoogle Scholar
  23. Gruel J, Landrein B, Tarr P, Schuster C, Refahi Y, Sampathkumar A, Hamant O, Meyerowitz EM, Jonsson H (2016) An epidermis-driven mechanism positions and scales stem cell niches in plants. Sci Adv 2:e1500989CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hwang YS, Quail PH (2008) Phytochrome-regulated PIL1 derepression is developmentally modulated. Plant Cell Physiol 49:501–511CrossRefPubMedGoogle Scholar
  25. Ikeda M, Mitsuba N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21:3493–3505CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ito T, Sakai H, Meyerowitz EM (2003) Whorl-specific expression of the SUPERMAN gene of Arabidopsis is mediated by cis elements in the transcribed region. Curr Biol 13:1524–1530CrossRefPubMedGoogle Scholar
  27. Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferrelra M, Rlechmann JL, Meyerowitz EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360CrossRefPubMedGoogle Scholar
  28. 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 19:3516–3529CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jiao Y, Meyerowitz EM (2010) Cell-type specific analysis of translating RNAs in developing flowers reveals new levels new levels of control. Mol Syst Biol 6:419CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kamata N, Okada H, Komeda Y, Takahashi T (2013) Mutations in epidermis-specific HD-ZIP IV genes affect floral organ identity in Arabidopsis thaliana. Plant J 75:430–440CrossRefPubMedGoogle Scholar
  31. Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11:830–842CrossRefPubMedGoogle Scholar
  32. Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–848CrossRefPubMedGoogle Scholar
  34. Krizek BA (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150:1916–1929CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, Hepworth SR, Haughn GW (2007) The Arabidopsis BEL1-LIKE HOMEODOMAIN Protein SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leat margins. Plant Cell 19:2719–2735CrossRefPubMedPubMedCentralGoogle Scholar
  36. Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96PubMedGoogle Scholar
  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 105:805–814CrossRefPubMedGoogle Scholar
  38. Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649CrossRefPubMedGoogle Scholar
  39. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes controls dispersal in Arabidopsis. Nature 404:766–770CrossRefPubMedGoogle Scholar
  40. 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 23:3654–3670CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lohmann JU, Hong RL, Hode M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803CrossRefPubMedGoogle Scholar
  42. Magnani E, Hake S (2008) KNOX lost the OX: the Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 20:875–887CrossRefPubMedPubMedCentralGoogle Scholar
  43. Mantegazza O, Gregis V, Mendes MA, Morandini P, Alves-Ferreira M, Patreze CM, Nardeli SM, Kater MM, Colombo L (2014) Analysis of the Arabidopsis REM gene family predicts functions during flower development. Ann Bot 114:1507–1515CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815CrossRefPubMedGoogle Scholar
  45. Meyerowitz EM (1997) Control of cell division patterns in developing shoots and flowers of Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol 62:369–375CrossRefPubMedGoogle Scholar
  46. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956CrossRefPubMedPubMedCentralGoogle Scholar
  47. Morita MT, Sakaguchi K, Kiyose S, Taira K, Kato K, Nakamura M, Tasaka M (2006) A C2H2-type zinc finger protein, SGR5, is involved in early events of gravitropism in Arabidopsis inflorescence stems. Plant J 47:619–628CrossRefPubMedGoogle Scholar
  48. Nag A, Yang Y, Jack T (2007) DORNROSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis. Plant Mol Biol 65:219–232CrossRefPubMedGoogle Scholar
  49. Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195CrossRefPubMedGoogle Scholar
  50. Nole-Wilson S, Krizek BA (2006) AINTEGUMENTA contributes to organ polarity and regulates growth of lateral organs in combination with YABBY genes. Plant Physiol 141:977–987CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ó’Maoiléidigh DS, Wuest SE, Rae L, Raganelli A, Ryan PT, Kwasniewska K, Das P, Lohan AJ, Loftus B, Graciet E, Wellmer F (2013) Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell 25:2482–2503CrossRefPubMedCentralGoogle Scholar
  52. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294CrossRefPubMedGoogle Scholar
  53. Ohno CK, Reddy GV, Heisler MG, Meyerowitz EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131:1111–1122CrossRefPubMedGoogle Scholar
  54. Okamuro JK, de Boer BGW, Lotys-Prass C, Szeto W, Jofuku KD (1996) Flowers into shoots: photo and hormonal control of a meristem identity switch in Arabidopsis. PNAS 93:13831–13836CrossRefPubMedPubMedCentralGoogle Scholar
  55. Pastore JJ, Limpuangthip Yamaguchi Y, Wu MF, Sang Y, Han SK, Malaspina L, Chavdaroff N, Yamaguchi A, Wagner D (2011) LATE MERISTEM IDENTITY2 acts together with LEAFY to activate APETALA1. Development 138:3189–3198CrossRefPubMedPubMedCentralGoogle Scholar
  56. Perales M, Rodriguez K, Snipes S, Yadav RK, Diaz-Mendoza Reddy GV (2016) Threshold-dependent transcriptional discrimination underlies stem cell homeostasis. PNAS 113:6298–6306CrossRefGoogle Scholar
  57. Prunet N, Yang W, Das P, Meyerowitz EM, Jack TP (2017) SUPERMAN prevents class B gene expression and promotes stem cell termination in the fourth whorl of Arabidopsis thaliana flowers. PNAS 114:7166–7171CrossRefPubMedPubMedCentralGoogle Scholar
  58. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110CrossRefPubMedGoogle Scholar
  59. Rodriguez K, Perales M, Snipes S, Yadav RK, Diaz-Mendoza M, Reddy GV (2016) DNA-dependent homodimerization, sub-cellular partitioning, and protein destabilization control WUSCHEL levels and spatial patterning. PNAS 113:6307–6315CrossRefGoogle Scholar
  60. Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:e1003374CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378:199–203CrossRefPubMedGoogle Scholar
  62. Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL (1999) The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant J 20:433–445CrossRefPubMedGoogle Scholar
  63. Sawa S, Ito T, Shimura Y, Okada K (1999) FILAMENTOUS FLOWER Controls the formation and development of Arabidopsis inflorescences and floral meristems. Plant Cell 11:69–86PubMedPubMedCentralGoogle Scholar
  64. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem population of Arabidopsis shoot meristem is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644CrossRefPubMedGoogle Scholar
  65. Schuster C, Gaillochet C, Lohmann JU (2015) Arabidopsis HECATE genes function in phytohormone control during gynoecium development. Development 142:3343–3350CrossRefPubMedPubMedCentralGoogle Scholar
  66. Smith HMS, Campbell BC, Hake S (2004) Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH. Curr Biol 14:812–817CrossRefPubMedGoogle Scholar
  67. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sun B, Ito T (2015) Regulation of floral stem cell termination. Front Plant Sci 6:17PubMedPubMedCentralGoogle Scholar
  69. Sun B, Xu Y, Ng KH, Ito T (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Gene Dev 23:1791–1804CrossRefPubMedPubMedCentralGoogle Scholar
  70. Sun B, Looi LS, Guo S, He Z, Gan ES, Huang J, Xu Y, Wee WY, Ito T (2014) Timing mechanism dependent on cell division is invoked by polycomb eviction in plant stem cells. Science 343:498–499CrossRefGoogle Scholar
  71. Supek F, Bosnjak M, Skunca N, Smuc T (2011) REVIGO summarizes and visualizes long lists of Gene Ontology terms. PLoS ONE 6:e21800CrossRefPubMedPubMedCentralGoogle Scholar
  72. Szczesny T, Routier-Kierzkowska AL, Kwiatkowska D (2009) Influence of clavata3-2 mutation on early flower development in Arabidopsis thaliana: quantitative analysts of changing geometry. J Exp Bot 60:679–695CrossRefPubMedGoogle Scholar
  73. Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386CrossRefPubMedGoogle Scholar
  74. Tan QK, Irish VF (2006) The Arabidopsis zinc finger-homeodomain genes encode proteins with unique biochemical properties that are coordinately expressed during floral development. Plant Physiol 140:1095–1108CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129CrossRefPubMedPubMedCentralGoogle Scholar
  76. Townsley BT, Covington MF, Ichihashi Y, Zumstein K, Sinha NR (2015) Brad-seq: breath adapter directional sequencing: a streamlined, ultra-simple and fast library preparation and fast library preparation protocol for strand specific mRNA library construction. Front Plant Sci 6:366CrossRefPubMedPubMedCentralGoogle Scholar
  77. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698CrossRefPubMedGoogle Scholar
  78. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859CrossRefPubMedGoogle Scholar
  79. 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 20:430–443CrossRefPubMedGoogle Scholar
  80. Winter CM, Yamaguchi N, Wu MF, Wagner D (2015) Transcriptional programs regulated by LEAFY and APETALA1 at the time of flower formation. Physiol Plant 155:55–73CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wu MF, Yamaguchi N, Xiao J, Bargmann B, Estelle M, Sang Y, Wagner D (2015) Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate. eLife 4:e09269PubMedPubMedCentralGoogle Scholar
  82. Xing S, Zachgo S (2008) ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J 53:790–801CrossRefPubMedGoogle Scholar
  83. Yamaguchi N, Komeda Y (2013) The role of CORYMBOSA1/BIG and auxin in the growth of Arabidopsis pedicel and internode. Plant Sci 209:64–74CrossRefPubMedGoogle Scholar
  84. Yamaguchi N, Wu MF, Winter CM, Berns MC, Nole-Wilson S, Yamaguchi A, Coupland G, Krizek B, Wagner D (2013) A molecular framework for auxin-mediated initiation of flower primordia. Dev Cell 24:271–282CrossRefPubMedGoogle Scholar
  85. Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344:638–641CrossRefPubMedGoogle Scholar
  86. Yamaguchi N, Jeong CW, Nole-Wilson S, Krizek BA, Wagner D (2016) AINTEGUMENTA and AINTEGUMENTA-LIKE6/PLETHORA3 Induce LEAFY Expression in Response to Auxin to Promote the Onset of Flower Formation in Arabidopsis. Plant Physiol 170:283–293CrossRefPubMedGoogle Scholar
  87. Yamaguchi N, Huang J, Xu Y, Tanoi K, Ito T (2017) Fine-tuning of auxin homeostasis governs the transition from floral stem cell maintenance to gynoecium formation. Nat Commun 8:1125CrossRefPubMedPubMedCentralGoogle Scholar
  88. 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 346:35–39CrossRefPubMedGoogle Scholar
  89. Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, Kay SA, Meyerowitz EM (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 547:377–380CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Akira Uemura
    • 1
  • Nobutoshi Yamaguchi
    • 1
    • 2
  • Yifeng Xu
    • 3
  • WanYi Wee
    • 3
  • Yasunori Ichihashi
    • 2
    • 4
  • Takamasa Suzuki
    • 5
  • Arisa Shibata
    • 4
  • Ken Shirasu
    • 4
    • 6
  • Toshiro Ito
    • 1
  1. 1.Biological SciencesNara Institute of Science and TechnologyIkomaJapan
  2. 2.Precursory Research for Embryonic Science and TechnologyJapan Science and Technology AgencyKawaguchi-shiJapan
  3. 3.Temasek Life Sciences Laboratory, 1 Research LinkNational University of SingaporeSingaporeRepublic of Singapore
  4. 4.RIKEN Center for Sustainable Resource ScienceYokohamaJapan
  5. 5.Department of Biological Chemistry, College of Bioscience and BiotechnologyChubu UniversityKasugaiJapan
  6. 6.Graduate School of ScienceThe University of TokyoBunkyoJapan

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