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Overexpression of AtAP1M3 regulates flowering time and floral development in Arabidopsis and effects key flowering-related genes in poplar

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Abstract

APETALA1 plays a crucial role in the transition from vegetative to reproductive phase and in floral development. In this study, to determine the effect of AP1 expression on flowering time and floral organ development, transgenic Arabidopsis and poplar overexpressing of AtAP1M3 (Arabidopsis AP1 mutant by dominant negative mutation) were generated. Transgenic Arabidopsis with e35Spro::AtAP1M3 displayed phenotypes with delayed-flowering compared to wild-type and flowers with abnormal sepals, petals and stamens. In addition, transgenic Arabidopsis plants exhibited reduced growth vigor compared to the wild-type plants. Ectopic expression of AtAP1M3 in poplar resulted in up- or down-regulation of some endogenous key flowering-related genes, including floral meristems identity gene LFY, B-class floral organ identity genes AP3 and PI, flowering pathway integrator FT1 and flower repressors TFL1 and SVP. These results suggest that AtAP1M3 regulates flowering time and floral development in plants.

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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 

  • An X, Ye M, Wang D, Wang Z, Cao G, Zheng H, Zhang Z (2011a) Ectopic expression of a poplar APETALA3-like gene in tobacco causes early flowering and fast growth. Biotechnol Lett 33:1239–1247

    Article  CAS  PubMed  Google Scholar 

  • An XM, Wang DM, Wang ZL, Li B, Bo WH, Cao GL, Zhang ZY (2011b) Isolation of a LEAFY homolog from Populus tomentosa: expression of PtLFY in P. tomentosa floral buds and PtLFY-IR-mediated gene silencing in tobacco (Nicotiana tabacum). Plant Cell Rep 30:89–100

    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 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043

    Article  PubMed  Google Scholar 

  • Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83

    Article  CAS  PubMed  Google Scholar 

  • Brunner AM, Li J, DiFazio SP, Shevchenko O, Montgomery BE, Mohamed R, Wei H, Ma C, Elias AA, VanWormer K (2007) Genetic containment of forest plantations. Tree Genet Genomes 3:75–100

    Article  Google Scholar 

  • Chen Z, Yang X, Su X, Rao P, Gao K, Lei B, An X (2015) Identification and expression analysis of APETALA1 homologues in poplar. Acta Physiol Plant 37:50

    Article  Google Scholar 

  • Chi Y, Huang F, Liu H, Yang S, Yu D (2011) An APETALA1-like gene of soybean regulates flowering time and specifies floral organs. J Plant Physiol 168:2251–2259

    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 

  • Duan Y-X, Fan J, Guo W-W (2010) Regeneration and characterization of transgenic kumquat plants containing the Arabidopsis APETALA1 gene. Plant Cell Tiss Organ Cult 100:273–281

    Article  CAS  Google Scholar 

  • Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M (2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 14:703–712

    Article  CAS  PubMed  Google Scholar 

  • Fernando DD, Zhang S (2006) Constitutive expression of the SAP1 gene from willow (Salix discolor) causes early flowering in Arabidopsis thaliana. Dev Genes Evol 216:19–28

    Article  CAS  PubMed  Google Scholar 

  • Hsu CY, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, DePamphilis CW, Luthe DS, Yuceer C (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 108:10756–10761

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang H, Wang S, Jiang J, Liu G, Li H, Chen S, Xu H (2014) Overexpression of BpAP1 induces early flowering and produces dwarfism in Betula platyphylla × Betula pendula. Physiol Plantarum 151:495–506

    Article  CAS  Google Scholar 

  • Irish VF (2010) The flowering of Arabidopsis flower development. Plant J 61:1014–1028

    Article  CAS  PubMed  Google Scholar 

  • Jeon JS, Jang S, Lee S, Nam J, Kim C, Lee SH, Chung YY, Kim SR, Lee YH, Cho YG, An G (2000) leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12:871–884

    CAS  PubMed Central  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 

  • Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueno F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89

    Article  CAS  PubMed  Google Scholar 

  • Kotoda N, Wada M, Kusaba S, Kano-Murakami Y, Masuda T, Soejima J (2002) Overexpression of MdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic Arabidopsis. Plant Sci 162:679–687

    Article  CAS  Google Scholar 

  • Kotoda N, Hayashi H, Suzuki M, Igarashi M, Hatsuyama Y, Kidou S, Igasaki T, Nishiguchi M, Yano K, Shimizu T, Takahashi S, Iwanami H, Moriya S, Abe K (2010) Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus × domestica Borkh.). Plant Cell Physiol 51:561–575

    Article  CAS  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 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−∆∆C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524

    Article  CAS  PubMed  Google Scholar 

  • Mohamed R, Wang C-T, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng X, Meilan R, Strauss SH, Brunner AM (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688

    Article  CAS  PubMed  Google Scholar 

  • Pabón-Mora N, Ambrose BA, Litt A (2012) Poppy APETALA1/FRUITFULL orthologs control flowering time, branching, perianth identity, and fruit development. Plant Physiol 158:1685–1704

    Article  PubMed Central  PubMed  Google Scholar 

  • Peña L, Martín-Trillo M, Juárez J, Pina JA, Navarro L, Martínez-Zapater JM (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotechnol 19:263–267

    Article  PubMed  Google Scholar 

  • Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615

    CAS  PubMed  Google Scholar 

  • Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral identity in Arabidopsis. Development 126:1109–1120

    CAS  PubMed  Google Scholar 

  • Rottmann WH, Meilan R, Sheppard LA, Brunner AM, Skinner JS, Ma C, Cheng S, Jouanin L, Pilate G, Strauss SH (2000) Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J 22:235–245

    Article  CAS  PubMed  Google Scholar 

  • Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13

    Article  CAS  PubMed  Google Scholar 

  • Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5–26

    Article  CAS  Google Scholar 

  • Sun Y, Fan Z, Li X, Li J, Yin H (2014) The APETALA1 and FRUITFUL homologs in Camellia japonica and their roles in double flower domestication. Mol Breed 33:821–834

    Article  CAS  Google Scholar 

  • Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584

    Article  CAS  PubMed  Google Scholar 

  • Wang C-T, Puzey J, Page G, Brunner AM (2009) Genes regulating flowering and dormancy in Populus. In: Proceedings of the 30th southern tree improvement conference, Virginia Tech, Blacksburg, VA, USA, 31 May–3 Jun 2009, p 116

  • Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500

    Article  CAS  PubMed  Google Scholar 

  • Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26:519–527

    Article  CAS  PubMed  Google Scholar 

  • Xiang L, Li X, Qin D, Guo F, Wu C, Miao L, Sun C (2012) Functional analysis of FLOWERING LOCUS T orthologs from spring orchid (Cymbidium goeringii Rchb. f.) that regulates the vegetative to reproductive transition. Plant Physiol Biochem 58:98–105

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (2013AA102703, 2011AA100201), the National Natural Science Foundation of China (31170631, J1103516), the Changjiang Scholars and Innovative Research Team Program of China (IRT13047) and the Fundamental Research Funds for the Central Universities (BLYJ201410). We thank Steven H. Strauss and Amy M. Brunner (Oregon State University, Corvallis, OR, USA) for providing the plasmid e35Spro::AtAP1M3.

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    Authors and Affiliations

    1. National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of the Ministry of Education, College of Biological Sciences and Biotechnology, Beijing Forestry University, P.O. Box 118, No. 35 Qinghua East Road, Haidian District, Beijing, 100083, China

      Zhong Chen, Meixia Ye, Weihua Liao, Huandi Ma, Kai Gao, Bingqi Lei & Xinmin An

    2. Beijing Center for Physical and Chemical Analysis, Beijing, 100094, China

      Xiaoxing Su

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    1. Zhong Chen
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    Correspondence to Xinmin An.

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    Zhong Chen and Meixia Ye have contributed equally to this work.

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    11248_2015_9870_MOESM1_ESM.tif

    Fig. S1 a Comparison of the deduced protein sequence of AP1 and AP1M3. The black box indicates the amino acid substitution resulting from the mutation in the gene sequence. b Schematic representation of the transformation vectors, e35Spro::AtAP1M3. LB, left border; e35Spro, enhanced cauliflower mosaic virus 35S promoter; E9term, E9 terminator; NPTII, neomycin phosphotransferase II gene; NOS-P, nopaline synthase promoter; NOS-T, nopaline synthase terminator; MAR, matrix attachment region; RB, right border. (TIFF 1281 kb)

    11248_2015_9870_MOESM2_ESM.tif

    Fig. S2 The process of genetic transformation of leaves of P. tomentosa with e35Spro::AtAP1M3. a Culture of poplar leaves in pre-culture medium. b Induction of multiple shoots in shoot regeneration medium from poplar leaf explants. c The production of shoots in the rooting medium. d Self-rooting shoots. e Transgenic P. tomentosa transformed with e35Spro::AtAP1M3. f Establishment of transgenic poplar in potting medium. (TIFF 2799 kb)

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    Chen, Z., Ye, M., Su, X. et al. Overexpression of AtAP1M3 regulates flowering time and floral development in Arabidopsis and effects key flowering-related genes in poplar. Transgenic Res 24, 705–715 (2015). https://doi.org/10.1007/s11248-015-9870-z

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