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Functional Analysis of the FT Homolog from Eustoma grandiflorum Reveals Its Role in Regulating A and C Functional MADS Box Genes to Control Floral Transition and Flower Formation

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Abstract

High temperatures cause rosetting and the continued vegetative growth of Eustoma grandiflorum. Eustoma requires a period of cold treatment to promote flowering. Ortholog of flowering time gene FT (EgFT) was isolated and characterized from E. grandiflorum. The ectopic expression of EgFT significantly promotes flowering in transgenic E. grandiflorum even when grown at high (28–30 °C) temperature conditions without any cold treatment. In addition, a severe defect in stamen and carpel formation in which they are converted into sepal/petal-like structures were observed in transgenic E. grandiflorum that strongly expressed EgFT. This homeotic conversion was correlated with the upregulation of A (EgAP1/EgFUL) and E (EgSEP1/3) and downregulation of C (EgAG) functional MADS box genes in transgenic E. grandiflorum. In wild-type E. grandiflorum, EgFT mRNA was detected in leaves and was expressed higher in young than in mature flower buds. In flowers, EgFT mRNA was strongly expressed in sepals, moderately expressed in petal, and was almost undetectable in stamen and carpel. This expression pattern was very similar to that found for EgAP1 and completely inverse to that found for EgAG. These results indicated that EgFT is able to promote flowering and regulate sepal/petal formation by activating the A/E genes and suppressing the C gene in E. grandiflorum. 35S::EgFT also caused early flowering in transgenic Arabidopsis. However, the flower organ formation and the expression of the Arabidopsis AG gene were not affected. Thus, the ability for EgFT to regulate EgAG expression may represent a distinct mechanism in E. grandiflorum for the regulation of flower organ formation.

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References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    Article  CAS  PubMed  Google Scholar 

  • Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154:516–520

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • An H, Roussot C, Suarez-Lopez P, Corbesier L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626

    Article  CAS  PubMed  Google Scholar 

  • Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    Article  CAS  PubMed  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  CAS  PubMed  Google Scholar 

  • D’Aloia M, Bonhomme D, Bouche F, Tamseddak K, Ormenese S, Torti S, Coupland G, Perilleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65:972–979

    Article  PubMed  Google Scholar 

  • Gamborg O, Miller R, Ojima K (1968) Nutrients requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  CAS  PubMed  Google Scholar 

  • Halliday KJ, Salter MG, Thingnaes E, Whitelam GC (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J 33:875–885

    Article  CAS  PubMed  Google Scholar 

  • Hayama R, Agashe B, Luley E, King R, Coupland G (2007) A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 19:2988–3000

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hisamatsu T, Koshioka M, Oyama N, Mander LN (1999) The relationship between endogenous gibberellins and rosetting in Eustoma grandiflorum. J Jpn Soc Hortic Sci 68:527–533

    Article  CAS  Google Scholar 

  • Hisamatsu T, Koshioka M, Mander LN (2004) Regulation of gibberellin biosynthesis and stem elongation by low temperature in Eustoma grandiflorum. J Hortic Sci Biotechnol 79:354–359

    CAS  Google Scholar 

  • Hou CJ, Yang CH (2009) Functional analysis of FT and TFL1 orthologs from orchid (Oncidium Gower Ramsey) that regulate the vegetative to reproductive transition. Plant Cell Physiol 50:1544–1557

    Article  CAS  PubMed  Google Scholar 

  • Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci U S A 97:9789–9794

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ichimura K, Korenaga M (1998) Improvement of vase life and petal color expression in several cultivars of cut Eustoma flowers using sucrose with 8-hydroxy-quinoline sulfate. Bull Natl Res Inst Veg Ornam Plants Tea 13:31–39

    CAS  Google Scholar 

  • Igasaki T, Watanabe Y, Nishiguchi M, Kotoda N (2008) The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar. Plant Cell Physiol 49:291–300

    Article  CAS  PubMed  Google Scholar 

  • Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054

    Article  CAS  PubMed  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    Article  CAS  PubMed  Google Scholar 

  • Komeda Y (2004) Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol 55:521–535

    Article  CAS  PubMed  Google Scholar 

  • Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M (1991) Isolation of higher plant developmental mutants. Symp Soc Exp Biol 45:1–19

    CAS  PubMed  Google Scholar 

  • Levy YY, Dean C (1998) The transition to flowering. Plant Cell 10:1973–1989

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, John Paul Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci U S A 15:6398–6403

    Article  Google Scholar 

  • Lin MK, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka K, Miura E, Xoconostle-Cazares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833

    CAS  PubMed Central  PubMed  Google Scholar 

  • Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10:427–435

    Article  CAS  PubMed  Google Scholar 

  • Mathieu J, Warthmann N, Kuttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060

    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 Central  PubMed  Google Scholar 

  • Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137:149–156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mino M, Oka M, Tasaka Y, Iwabuchi M (2003) Thermoinduction of genes encoding the enzymes of gibberellin biosynthesis and a putative negative regulator of gibberellin signal transduction in Eustoma grandiflorum. Plant Cell Rep 22:159–165

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–479

    Article  CAS  Google Scholar 

  • Nakano Y, Kawashima H, Kinoshita T, Yoshikawa H, Hisamatsu T (2011) Characterization of FLC, SOC1 and FT homologs in Eustoma grandiflorum: effects of vernalization and post-vernalization conditions on flowering and gene expression. Physiol Plant 141:383–393

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa K, Kano A, Kanematsu K, Korenaga M (1991) Effects of air temperature and time on rosette formation in seedlings of Eustoma grandiflorum (Raf.) Shinn. Sci Hortic 48:171–176

    Article  Google Scholar 

  • Ohkawa K, Korenaga M, Yoshizumi T (1993) Influence of temperature prior to seed ripening and at germination on rosette formation and bolting of Eustoma grandiflorum. Sci Hortic 53:225–230

    Article  Google Scholar 

  • Ohkawa K, Yoshizumi T, Korenaga M, Kanematsu K (1994) Reversal of heat-induced rosetting in Eustoma grandiflorum with low temperatures. Hortscience 29:165–166

    Google Scholar 

  • Oka M, Tasaka Y, Iwabuchi M, Mino M (2001) Elevated sensitivity to gibberellin by vernalization in the vegetative rosette plants of Eustoma grandiflorum and Arabidopsis thaliana. Plant Sci 160:1237–1245

    Article  CAS  PubMed  Google Scholar 

  • Onouchi H, Igeño MI, Périlleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12:885–900

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peng YJ, Shih CF, Yang JY, Tan CM, Hsu WH, Huang YP, Liao PC, Yang CH (2013) A RING-Type E3 ligase controls anther dehiscence by activating the jasmonate biosynthetic pathway gene defective in anther dehiscence1 in Arabidopsis. Plant J. 74:310–327

  • Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857

    Article  CAS  PubMed  Google Scholar 

  • Roh SM, Lawson RH (1988) Tissue culture in the improvement of Eustoma. HortSci 23:658

    Google Scholar 

  • Samach A, Wigge PA (2005) Ambient temperature perception in plants. Curr Opin Plant Biol 8:483–486

    Article  PubMed  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289

    Article  CAS  PubMed  Google Scholar 

  • Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  PubMed  Google Scholar 

  • Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci U S A 106:4555–4560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036

    Article  CAS  PubMed  Google Scholar 

  • Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85

    Article  CAS  PubMed  Google Scholar 

  • Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471

    Article  CAS  PubMed  Google Scholar 

  • Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter K, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149

    Article  CAS  PubMed  Google Scholar 

  • Thiruvengadam M, Yang CH (2009) Ectopic expression of two MADS box genes from orchid (Oncidium Gower Ramsey) and lily (Lilium longiflorum) alters flower transition and formation in Eustoma grandiflorum. Plant Cell Rep 28:1463–1473

    Article  CAS  PubMed  Google Scholar 

  • Tzeng TY, Chen HY, Yang CH (2002) Ectopic expression of carpel-specific MADS box genes from lily and lisianthus causes similar homeotic conversion of sepal and petal in Arabidopsis. Plant Physiol 130:1827–1836

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006

    Article  CAS  PubMed  Google Scholar 

  • Wigge PA (2011) FT, a mobile developmental signal in plants. Curr Biol 21:R374–R378

    Article  CAS  PubMed  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto A, Fujita K, Takabe T (2010) Ectopic expression of DnaK chaperone from a halotolerant cyanobacterium Aphanothece halophytica induced the bolting without cold treatment in Eustoma grandiflorum. Plant Biotechnol 27:489–493

    Article  Google Scholar 

  • Yanagida M, Mino M, Iwabuchi M, Ogawa K (2004) Reduced glutathione is a novel regulator of vernalization-induced bolting in the rosette plant Eustoma grandiflorum. Plant Cell Physiol 45:129–137

    Article  CAS  PubMed  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 

  • Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, dePamphilis CW, Ma H (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zeevaart JA (2008) Leaf-produced floral signals. Curr Opin Plant Biol 11:541–547

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants to C-H Y from the National Science Council, Taiwan, ROC, grant number: NSC98-2622-B-005-001-CC2 and NSC99-2622-B-005-001-CC2. This work was also supported in part by the Ministry of Education, Taiwan, R.O.C. under the ATU plan.

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  1. Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan, 40227, Republic of China

    K.-H. Li, T.-H. Chuang, C.-J. Hou & C.-H. Yang

  2. Agricultural Biotechnology Center, National Chung Hsing University, Taichung, Taiwan, 40227, Republic of China

    C.-H. Yang

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  1. K.-H. Li
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Fig. S1

Detection of EgGA20ox, EgGA3ox, and EgSPY genes expression in 35S::EgFT transgenic E. grandiflorum plant. The result showed that the expression of these three genes in severe 35S::EgFT-1 transgenic plant was similar to that observed in wild-type plants (WT). (PDF 57 kb)

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Li, KH., Chuang, TH., Hou, CJ. et al. Functional Analysis of the FT Homolog from Eustoma grandiflorum Reveals Its Role in Regulating A and C Functional MADS Box Genes to Control Floral Transition and Flower Formation. Plant Mol Biol Rep 33, 770–782 (2015). https://doi.org/10.1007/s11105-014-0789-y

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