Plant Molecular Biology Reporter

, Volume 31, Issue 4, pp 1031–1039 | Cite as

Isolation and Characterization of an APETALA1-Like Gene from Pear (Pyrus pyrifolia)

  • Yuexue Liu
  • Jin Kong
  • Tianzhong Li
  • Yi Wang
  • Aide Wang
  • Zhenhai Han
Brief Communication


To study the early steps of flower initiation and development in pear (Pyrus pyrifolia), a MADS-box gene, PpAP1, a putative APETALA1 (AP1) pear ortholog from Pyrus pyrifolia, was isolated. The deduced amino acid sequence of PpAP1 indicated high sequence identity with members of the MADS-box family of transcription factors, particularly the AP1/SQUA family of MADS-box proteins, which control floral-meristem and floral-organ identities. PpAP1 was expressed mainly in reproductive tissues such as inflorescence shoot apices and in flowers. Moreover, no transcription was detected in leaves, and only trace amounts were detected in vegetative shoot apices. In flowers, PpAP1 transcripts were restricted to the outer three whorls, mainly in sepals. mRNA expression patterns of PpAP1 suggest that it might play a role in both flowering and flower development. As low expression of PpAP1 was detected in stamens, this suggested that it was not an A-function gene. Overexpression of PpAP1 in Arabidopsis resulted in early-flowering phenotypes, thus indicating that PpAP1 played a similar role to that of its Arabidopsis homolog. Moreover, multiple floral organs were observed in transgenic lines, thus suggesting that PpAP1 has a broader role that than of classical A-function genes. These results indicated that PpAP1 plays important roles in regulating vegetative to reproductive development in plants, and is also involved in the development of floral organs.


APETALA1-like Flowering time Pyrus pyrifolia Expression Function 


  1. 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 309:1052–1056PubMedCrossRefGoogle Scholar
  2. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013PubMedCrossRefGoogle Scholar
  3. Atkinson CJ, Taylor L (1994) The influence of autumn temperature on flowering time and cropping of Pyrus communis cv. Conference. J Hortic Sci 69:1067–1075Google Scholar
  4. Batjer LP, Thompson AH (1949) Effect of boric acid sprays applied during bloom upon the set of pear fruits. Proc Am Soc Hortic Sci 53:141–142Google Scholar
  5. Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489PubMedCrossRefGoogle Scholar
  6. Berbel A, Navarro C, Ferrandiz C, Canas LA, Madueno F, Beltran JP (2001) Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. Plant J 25:441–451PubMedCrossRefGoogle Scholar
  7. Calonje M, Cubas P, Martínez-Zapater JM, Carmona MJ (2004) Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol 135:1491–1501PubMedCrossRefGoogle Scholar
  8. Chen MK, Lin IC, Yang CH (2008) Functional analysis of three lily (Lilium longiflorum) APETALA1-like MADS box genes in regulating floral transition and formation. Plant Cell Physiol 49:704–717PubMedCrossRefGoogle Scholar
  9. 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 168:2251–2259PubMedCrossRefGoogle Scholar
  10. Costa J, Bosch M, Blanco A (1995) Growth and cropping of ‘Blanquilla’ pear trees treated with paclobutrazol. J Hortic Sci 70:433–443Google Scholar
  11. Flachowsky H, Peil A, Sopanen T, Elo A, Hanke V (2007) Overexpression of BpMADS4 from silver birch (Betula pendula Roth.) induces early flowering in apple (Malus × domestica Borkh.). Plant Breed 126:137–145CrossRefGoogle Scholar
  12. Fornara F, Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550–550, e552PubMedCrossRefGoogle Scholar
  13. Freiman A, Shlizerman L, Golobovitch S, Korchinsky ZYR, Cohen Y, Samach A, Chevreau E, Le Roux P-M, Patocchi A, Flaishman MA (2012) Development of a transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2. Planta 235:1239–1251PubMedCrossRefGoogle Scholar
  14. Goloveshkina EN, Shulga OA, Shchennikova AV, Kamionskaya AM, Skryabin KG (2010) Constitutive expression of the sunflower and Chrysanthemum genes of the AP1/FUL group changes flowering timing in transgenic tobacco plants. Dokl Biol Sci 434:322–324PubMedCrossRefGoogle Scholar
  15. Irish VF, Sussex IM (1990) Function of the apetala-1 Gene during Arabidopsis floral development. Plant Cell 2:741–753PubMedGoogle Scholar
  16. Jang S, An K, Lee S, An G (2002) Characterization of tobacco MADS-box genes involved in floral initiation. Plant Cell Physiol 43:230–238PubMedCrossRefGoogle Scholar
  17. Kaufmann K, Melzer S, Theissen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347:183–198PubMedCrossRefGoogle Scholar
  18. 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 328:85–89PubMedCrossRefGoogle Scholar
  19. Kotoda N, Wada M, Komori S, Kidou S, Abe K, Masuda T, Soejima J (2000) Expression pattern of homologues of floral meristem identity genes LFY and AP1 during flower development in apple. J Am Soc Hortic Sci 125(4):398–403Google Scholar
  20. Kotoda N, Wada M, Kusaba S, Murakami YK, Masuda T, Soejima J (2002) Overexpression of MdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic Arabidopsis. Plant Sci 162:679–687CrossRefGoogle Scholar
  21. Li C, Xie H, Zhang L, Xu Y, Li YF, Ma RC (2012) Molecular characterization of the PpMADS1 gene from peach. Tree Genet Genomes 8:831–840. doi:10.1007/s11295-012-0468-9
  22. Li HY, Liu FF, Liu GF, Wang S, Guo XH, Jing J (2012) Molecular cloning and expression analysis of 13 MADS-box genes in Betula platyphylla. Plant Mol Biol Rep 30:149–157CrossRefGoogle Scholar
  23. Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833PubMedGoogle Scholar
  24. Lu SJ, Wei H, Wang Y, Wang HM, Yang RF, Zhang XB, Tu JM (2012) Overexpression of a transcription factor OsMADS15 modifies plant architecture and flowering time in rice (Oryza sativa L.). Plant Mol Biol Rep 30:1461–1469. doi:10.1007/s11105-012-0468-9 Google Scholar
  25. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277PubMedCrossRefGoogle Scholar
  26. Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524PubMedCrossRefGoogle Scholar
  27. Matsuda N, Ikeda K, Kurosaka M, Takashina T, Isuzugawa K, Endo T, Omura M (2009) Early flowering phenotype in transgenic pears (Pyrus communis L.) expressing the CiFT gene. J Jpn Soc Hortic Sci 78(4):410–416CrossRefGoogle Scholar
  28. Michaels SD (2009) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12:75–80PubMedCrossRefGoogle Scholar
  29. Mishiba K, Nishihara M, Nakatsuka T, Abe Y, Hirano H, Yokoi T, Kikuchi A, Yamamura S (2005) Consistent transcriptional silencing of 35S-driven transgenes in gentian. Plant J 44:541–556PubMedCrossRefGoogle Scholar
  30. Moyroud E, Kusters E, Monniaux M, Koes R, Parcy F (2010) LEAFY blossoms. Trends Plant Sci 15:346–352PubMedCrossRefGoogle Scholar
  31. Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26(4):385–394PubMedCrossRefGoogle Scholar
  32. Peña L, Martin-Trillo M, Juarez J, Pina JA, Navarro L, Martinez-Zapater JM (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nature Biotechnol 19:263–267CrossRefGoogle Scholar
  33. Pillitterri LJ, Lovatt CJ, Walling LL (2004) Isolation and characterization of LEAFY and APETALA1 homologues from Citrus sinensis L. Osbeck ‘Washington’. J Am Soc Hortic Sci 129:846–856Google Scholar
  34. Shan H, Zhang N, Liu C, Xu G, Zhang J, Chen Z, Kong H (2007) Patterns of gene duplication and functional diversification during the evolution of the AP1/SQUA subfamily of plant MADS-box genes. Mol Phylogenet Evol 44:26–41PubMedCrossRefGoogle Scholar
  35. Shannon S, Meeks-Wagner DR (1991) A mutation in the arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892PubMedGoogle Scholar
  36. Shchennikova AV, Shulga OA, Skryabin KG, Angenent GC (2004) Identification and characterization of four Chrysanthemum MADS-Box genes, belonging to the APETALA1/FRUITFULL and SEPALLATA3 subfamilies. Plant Physiol 134:1632–1641PubMedCrossRefGoogle Scholar
  37. Shulga OA, Mitiouchkina TY, Shchennikova AV, Skryabin KG, Dolgov SV (2011) Overexpression of AP1-like genes from Asteraceae induces early-flowering in transgenic Chrysanthemum plants. In Vitro Cell Dev Biol Plant 47:553–560CrossRefGoogle Scholar
  38. Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037PubMedCrossRefGoogle Scholar
  39. Wang ZJ, Huang JQ, Huang YJ, Chen FF, Zheng BS (2012) Cloning and characterization of a homologue of the FLORICAULA/LEAFY gene in hickory (Carya cathayensis Sarg). Plant Mol Biol Rep 30:794–805CrossRefGoogle Scholar
  40. Wagner D, Sablowski RWM, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584PubMedCrossRefGoogle Scholar
  41. Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500PubMedCrossRefGoogle Scholar
  42. Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26(12):519–527PubMedCrossRefGoogle Scholar
  43. Wigge PA, Kim MC, Jaeger KE, Bushch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059PubMedCrossRefGoogle Scholar
  44. 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 101:1775–1780PubMedCrossRefGoogle Scholar
  45. Wu W, Chen F, Jing D, Liu Z, Ma L (2012) Isolation and characterization of an AGAMOUS-like gene from Magnolia wufengensis (Magnoliaceae). Plant Mol Biol Rep 30:690–698CrossRefGoogle Scholar
  46. Yalovsky S, Rodriguez-Concepcion M, Bracha K, Toledo-Ortiz G, Gruissem W (2000) Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12:1257–1266PubMedGoogle Scholar
  47. Vandenbussche M, Theissen G, Van de Peer Y, Gerats T (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res 31:4401–4409PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Yuexue Liu
    • 1
    • 2
  • Jin Kong
    • 2
  • Tianzhong Li
    • 2
  • Yi Wang
    • 2
  • Aide Wang
    • 1
  • Zhenhai Han
    • 2
  1. 1.College of HorticultureShenyang Agricultural UniversityShenyangChina
  2. 2.College of Agronomy and BiotechnologyChina Agricultural UniversityBeijingChina

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