Skip to main content
SpringerLink
Log in

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

Plant Reproduction volume 31, pages 89–105 (2018)Cite this article

Key message

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • 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 50:1007–1019

    Article  CAS  PubMed  Google Scholar 

  • 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 9:841–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 505:417–421

    Article  CAS  PubMed  Google Scholar 

  • Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844

    CAS  PubMed  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114:599–615

    CAS  PubMed  Google Scholar 

  • 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 289:617–619

    Article  CAS  PubMed  Google Scholar 

  • 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 117:905–923

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 13:1002–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 135:1235–1245

    Article  CAS  PubMed  Google Scholar 

  • Chandler JW (2011) Founder cell specification. Trends Plant Sci 16:607–613

    Article  CAS  PubMed  Google Scholar 

  • Chandler JW, Werr W (2014) Arabidopsis floral phytomer development: auxin response relative to biphasic modes of organ initiation. J Exp Bot 65:3097–3110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121:2057–2067

    CAS  Google Scholar 

  • Crawford BCW, Yanofsky MF (2011) HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development 138:2999–3009

    Article  CAS  PubMed  Google Scholar 

  • 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 110:7074–7079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doerner P (2001) Plant meristems: a menage a trois to end it all. Curr Biol 11:785–787

    Article  Google Scholar 

  • Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14:547–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–W70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914

    Article  CAS  PubMed  Google Scholar 

  • 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 17:855

    Article  Google Scholar 

  • 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 132:429–438

    Article  CAS  PubMed  Google Scholar 

  • Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of Arabidopsis shoot meristem. Development 134:3539–3548

    Article  CAS  PubMed  Google Scholar 

  • 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:e1500989

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang YS, Quail PH (2008) Phytochrome-regulated PIL1 derepression is developmentally modulated. Plant Cell Physiol 49:501–511

    Article  CAS  PubMed  Google Scholar 

  • 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 21:3493–3505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:1524–1530

    Article  CAS  PubMed  Google Scholar 

  • 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 430:356–360

    Article  CAS  PubMed  Google Scholar 

  • 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 19:3516–3529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:419

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 75:430–440

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11:830–842

    Article  CAS  PubMed  Google Scholar 

  • 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 18:560–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 313:845–848

    Article  CAS  PubMed  Google Scholar 

  • Krizek BA (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150:1916–1929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:2719–2735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96

    CAS  PubMed  Google Scholar 

  • 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 105:805–814

    Article  CAS  PubMed  Google Scholar 

  • 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 199:639–649

    Article  CAS  PubMed  Google Scholar 

  • Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes controls dispersal in Arabidopsis. Nature 404:766–770

    Article  CAS  PubMed  Google Scholar 

  • 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 23:3654–3670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:793–803

    Article  CAS  PubMed  Google Scholar 

  • 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 20:875–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 114:1507–1515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 95:805–815

    Article  CAS  PubMed  Google Scholar 

  • Meyerowitz EM (1997) Control of cell division patterns in developing shoots and flowers of Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol 62:369–375

    Article  CAS  PubMed  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 47:619–628

    Article  CAS  PubMed  Google Scholar 

  • Nag A, Yang Y, Jack T (2007) DORNROSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis. Plant Mol Biol 65:219–232

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195

    Article  CAS  PubMed  Google Scholar 

  • Nole-Wilson S, Krizek BA (2006) AINTEGUMENTA contributes to organ polarity and regulates growth of lateral organs in combination with YABBY genes. Plant Physiol 141:977–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:2482–2503

    Article  PubMed Central  Google Scholar 

  • Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294

    Article  CAS  PubMed  Google Scholar 

  • Ohno CK, Reddy GV, Heisler MG, Meyerowitz EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131:1111–1122

    Article  CAS  PubMed  Google Scholar 

  • 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 93:13831–13836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 138:3189–3198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perales M, Rodriguez K, Snipes S, Yadav RK, Diaz-Mendoza Reddy GV (2016) Threshold-dependent transcriptional discrimination underlies stem cell homeostasis. PNAS 113:6298–6306

    Article  Google Scholar 

  • 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 114:7166–7171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  • 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 113:6307–6315

    Article  Google Scholar 

  • Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:e1003374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378:199–203

    Article  CAS  PubMed  Google Scholar 

  • 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 20:433–445

    Article  CAS  PubMed  Google Scholar 

  • Sawa S, Ito T, Shimura Y, Okada K (1999) FILAMENTOUS FLOWER Controls the formation and development of Arabidopsis inflorescences and floral meristems. Plant Cell 11:69–86

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 100:635–644

    Article  CAS  PubMed  Google Scholar 

  • Schuster C, Gaillochet C, Lohmann JU (2015) Arabidopsis HECATE genes function in phytohormone control during gynoecium development. Development 142:3343–3350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith HMS, Campbell BC, Hake S (2004) Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH. Curr Biol 14:812–817

    Article  CAS  PubMed  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun B, Ito T (2015) Regulation of floral stem cell termination. Front Plant Sci 6:17

    PubMed  PubMed Central  Google Scholar 

  • 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 23:1791–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 343:498–499

    Article  Google Scholar 

  • Supek F, Bosnjak M, Skunca N, Smuc T (2011) REVIGO summarizes and visualizes long lists of Gene Ontology terms. PLoS ONE 6:e21800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 60:679–695

    Article  CAS  PubMed  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386

    Article  CAS  PubMed  Google Scholar 

  • 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 140:1095–1108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–W129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:366

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 437:693–698

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859

    Article  CAS  PubMed  Google Scholar 

  • 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 20:430–443

    Article  CAS  PubMed  Google Scholar 

  • Winter CM, Yamaguchi N, Wu MF, Wagner D (2015) Transcriptional programs regulated by LEAFY and APETALA1 at the time of flower formation. Physiol Plant 155:55–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e09269

    PubMed  PubMed Central  Google Scholar 

  • Xing S, Zachgo S (2008) ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J 53:790–801

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi N, Komeda Y (2013) The role of CORYMBOSA1/BIG and auxin in the growth of Arabidopsis pedicel and internode. Plant Sci 209:64–74

    Article  CAS  PubMed  Google Scholar 

  • 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 24:271–282

    Article  CAS  PubMed  Google Scholar 

  • 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 344:638–641

    Article  CAS  PubMed  Google Scholar 

  • 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 170:283–293

    Article  CAS  PubMed  Google Scholar 

  • 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 8:1125

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 346:35–39

    Article  CAS  PubMed  Google Scholar 

  • 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 547:377–380

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Author notes

  1. Nobutoshi Yamaguchi and Yifeng Xu have contributed equally to this work.

Authors and Affiliations

  1. Biological Sciences, Nara Institute of Science and Technology, 8916-5, Takayama, Ikoma, Nara, 630-0192, Japan

    Akira Uemura, Nobutoshi Yamaguchi & Toshiro Ito

  2. Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, 4-1-8, Honcho, Kawaguchi-shi, Saitama, 332-0012, Japan

    Nobutoshi Yamaguchi & Yasunori Ichihashi

  3. Temasek Life Sciences Laboratory, 1 Research Link, National University of Singapore, Singapore, 117604, Republic of Singapore

    Yifeng Xu & WanYi Wee

  4. RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro, Tsurumi, Yokohama, Kanagawa, 230-0045, Japan

    Yasunori Ichihashi, Arisa Shibata & Ken Shirasu

  5. Department of Biological Chemistry, College of Bioscience and Biotechnology, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi, 487-8501, Japan

    Takamasa Suzuki

  6. Graduate School of Science, The University of Tokyo, Bunkyo, Tokyo, 113-0033, Japan

    Ken Shirasu

Authors
  1. Akira Uemura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nobutoshi Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yifeng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. WanYi Wee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasunori Ichihashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takamasa Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Arisa Shibata
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ken Shirasu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Toshiro Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Toshiro Ito.

Additional information

Communicated by Tetsuya Higashiyama.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uemura, A., Yamaguchi, N., Xu, Y. et al. Regulation of floral meristem activity through the interaction of AGAMOUS, SUPERMAN, and CLAVATA3 in Arabidopsis . Plant Reprod 31, 89–105 (2018). https://doi.org/10.1007/s00497-017-0315-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-017-0315-0

Keywords

search

Navigation