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Ectopic expression of a hyacinth AGL6 homolog caused earlier flowering and homeotic conversion in Arabidopsis

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Abstract

MADS-box genes are involved in floral organ development. Here we report that an AGL6(Agamous-like 6)-like MADS-box gene, HoAGL6, was isolated from Hyacinthus orientalis L. Expression pattern analysis demonstrated that HoAGL6 transcript was detected in inflorescence buds, tepals, carpels and ovules, but not in stamina, leaves or scales. Transgenic Arabidopsis plants ectopically expressing HoAGL6 exhibited novel phenotypes of significantly reduced plant size, extremely early flowering, and losing inflorescence indeterminacy. In addition, wide homeotic conversion of sepals, petals, and leaves into carpel-like or ovary structures, and disappearance or number reduction of stamens in 35S::HoAGL6 Arabidopsis plants were also observed. RT-PCR analysis indicated that the expressions of flowering time gene SOC1 and flower meristem identity gene LFY were significantly up-regulated in 35S::HoAGL6 transgenic Arabidopsis plants, and the expression levels of floral organ identity genes AG and SEP1 in leaves were also elevated. These results indicated that HoAGL6 was involved in the regulation of flower transition and flower organ formation.

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References

  1. Kater M M, Dreni L, Colombo L. Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot, 2006, 57(13): 3433–3444

    Article  PubMed  CAS  Google Scholar 

  2. Purugganan M D, Rounsley S D, Schmidt R J, et al. Molecular evolution of flower development: Diversification of the plant MADS-box regulatory gene family. Genetics, 1995, 140: 345–356

    PubMed  CAS  Google Scholar 

  3. Coen E S, Meyerowitz E M. The war of the whorls: Genetic interaction controlling flower development. Nature, 1991, 353: 31–37

    Article  PubMed  CAS  Google Scholar 

  4. Theissen G, Saedler H. Floral quartets. Nature, 2001, 409: 469–471

    Article  PubMed  CAS  Google Scholar 

  5. Theissen G, Becker A, Di Rosa, et al. A short history of MADS-box genes in plants. Plant Mol Biol, 2000, 42: 115–149

    Article  PubMed  CAS  Google Scholar 

  6. Pinyopich A, Ditta G S, Baumann E, et al. Unraveling the redundant roles of MADS-box genes during carpel and fruit development. Nature, 2003, 424: 85–88

    Article  PubMed  CAS  Google Scholar 

  7. Angenent G C, Franken J, Busscher M, et al. A novel class of MADS-box genes is involved in ovule development in petunia. Plant Cell, 1995, 7: 1569–1582

    Article  PubMed  CAS  Google Scholar 

  8. Favaro R, Pinyopich A, Battaglia R, et al. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell, 2003, 15: 2603–2611

    Article  PubMed  CAS  Google Scholar 

  9. Pelaz S, Ditta G S, Baumann E, et al. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 2000, 405: 200–203

    Article  PubMed  CAS  Google Scholar 

  10. Pelaz S, Tapia-Lopez R, Alvarez-Buylla E R, et al. Conversion of leaves into petals in Arabidopsis. Curr Biol, 2001, 11: 182–184

    Article  PubMed  CAS  Google Scholar 

  11. Honma T, Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 2001, 409: 525–529

    Article  PubMed  CAS  Google Scholar 

  12. Theissen G. Development of floral organ identity: Stories from the MADS house. Curr Opin Biol, 2001, 4: 75–85

    Article  CAS  Google Scholar 

  13. Drews G N, Bowman J L, Meyerowitz E M. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell, 1991, 65: 991–1002

    Article  PubMed  CAS  Google Scholar 

  14. Mandel M A, Gustafson-Brown C, Savidge B, et al. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature, 1992, 360: 273–277

    Article  PubMed  CAS  Google Scholar 

  15. Jofuku K D, den Boer B G W, van Montagu M, et al. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell, 1994, 6: 1211–1225

    Article  PubMed  CAS  Google Scholar 

  16. Colombo L, Franken J, Koetje E, et al. The petunia MADS box gene FBP11 determines ovule identity. Plant Cell, 1995, 7: 1859–1868

    Article  PubMed  CAS  Google Scholar 

  17. Krizek B A, Meyerowitz E M. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development, 1996, 122: 11–22

    PubMed  CAS  Google Scholar 

  18. Parenicová L, de Folter S, Kieffer M, et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: New openings to the MADS world. Plant Cell, 2003, 15: 1538–1551

    Article  PubMed  Google Scholar 

  19. de Folter S, Immink R G H, Kieffer M, et al. Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell, 2005, 17: 1424–1433

    Article  PubMed  Google Scholar 

  20. Alvarez-Buylla E R, Pelaz S, Liljegren S J, et al. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA, 2000, 97: 5328–5333

    Article  PubMed  CAS  Google Scholar 

  21. Gregis V, Sessa A, Colombo L, et al. AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell, 2006, 18: 1373–1382

    Article  PubMed  CAS  Google Scholar 

  22. Michaels S D, Amasino R M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell, 1999, 11: 949–956

    Article  PubMed  CAS  Google Scholar 

  23. Sheldon C C, Rouse D T, Finnegan E J, et al. The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA, 2000, 97: 3753–3758

    Article  PubMed  CAS  Google Scholar 

  24. Onouchi H, Igeño M I, Périlleux C, et al. Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell, 2000, 12: 885–900

    Article  PubMed  CAS  Google Scholar 

  25. Ferrario S, Immink R G, Shchennikova A, et al. The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell, 2003, 15: 914–925

    Article  PubMed  CAS  Google Scholar 

  26. Bowman J L, Alvarez J, Weigel D, et al. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development, 1993, 119: 721–743.

    CAS  Google Scholar 

  27. Liljegren S J, Gustafson-Brown C, Pinyopich A, et al. Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell, 1999, 11: 1007–1018

    Article  PubMed  CAS  Google Scholar 

  28. Ma H, Yanofsky M F, Meyerowitz E M. AGL1–AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev, 1991, 5: 484–495

    Article  PubMed  CAS  Google Scholar 

  29. Mouradov A, Glassick T V, Hamdorf B A, et al. Family of MADS-box genes expressed early in male and female reproductive structure of monterey pine. Plant Physiol, 1998, 117: 55–61

    Article  PubMed  CAS  Google Scholar 

  30. Shindo S, Ito M, Ueda K, et al. Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev, 1999, 1: 180–190

    Article  PubMed  CAS  Google Scholar 

  31. Tsuchimoto S, Mayama T, van der Krol A, et al. The whorl-specific action of a petunia class B floral homeotic gene. Genes to Cells, 2000, 5(2): 89–99

    Article  PubMed  CAS  Google Scholar 

  32. Boss P K, Sensi E, Hua C, et al. Cloning and characterization of grapevine (Vitis vinifera L.). MADS-box genes expressed during inflorescence and berry development. Plant Sci, 2002, 162(6): 887–895

    Article  CAS  Google Scholar 

  33. Mena M, Mandel M A, Lerner D R, et al. A characterization of the MADS-box gene family in maize. Plant J, 1995, 8: 845–854

    PubMed  CAS  Google Scholar 

  34. Zhao T, Ni Z, Dai Y, et al. Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.). Mol Genet Genomics, 2006, 276(4): 334–350

    Article  PubMed  CAS  Google Scholar 

  35. Yao J L, Dong Y H, Kvarnheden A, et al. Seven MADS-box genes in apple are expressed in different parts of the fruit. J Am Soc Hortic Sci, 1999, 124: 8–13

    CAS  Google Scholar 

  36. Petersen K, Didion T, Andersen C H, et al. MADS-box genes from perennial ryegrass differentially expressed during transition from vegetative to reproductive growth. J Plant Physiol, 2004, 161(4): 439–447

    Article  PubMed  CAS  Google Scholar 

  37. Becker A, Saedler H, Theissen G. Distinct MADS-box gene expression patterns in the reproductive cones of the gymnosperm Gnetum gnemon. Dev Genes Evol, 2003, 213(11): 567–572

    Article  PubMed  CAS  Google Scholar 

  38. Hsu H-F, Huang C-H, Chou L-T, et al. Ectopic expression of an orchid (Oncidium Gower Ramsey) AGL6-like gene promotes flowering by activating flowering time genes in Arabidopsis thaliana. Plant and Cell Physiol, 2003, 44: 783–794

    Article  CAS  Google Scholar 

  39. Moon Y-H, Kang H-G, Jung J-Y, et al. Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol, 1999, 120: 1193–1204

    Article  PubMed  CAS  Google Scholar 

  40. Bechtold N, Ellis J, Pelletier G. In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci, 1993, 316: 1194–1199

    CAS  Google Scholar 

  41. Mizukami Y, Ma H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell, 1992, 71: 119–131

    Article  PubMed  CAS  Google Scholar 

  42. Mizukami Y, Ma H. Determination of Arabidopsis floral meristem identity by AGAMOUS. Plant Cell, 1997, 9: 393–408

    Article  PubMed  CAS  Google Scholar 

  43. Carlsbecker A, Tandre K, Johanson U, et al. The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). Plant J, 2004, 40(4): 546–557

    Article  PubMed  CAS  Google Scholar 

  44. Preston J C, Kellogg E A. Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics, 2006, 174(1): 421–437.

    Article  PubMed  CAS  Google Scholar 

  45. Kyozuka J, Kobayashi T, Morita M, et al. Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol, 2000, 41: 710–718

    PubMed  CAS  Google Scholar 

  46. Kater M M, Dreni L, Colombo L. Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot, 2006, 57(13): 3433–3444

    Article  PubMed  CAS  Google Scholar 

  47. Rounsley S D, Ditta G S, Yanofsky M F. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell, 1995, 7(8): 1259–1269

    Article  PubMed  CAS  Google Scholar 

  48. Tandre K, Svenson M, Svensson M E, et al. Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J, 1998, 15: 615–623

    Article  PubMed  CAS  Google Scholar 

  49. Lee H, Suh S S, Park E, et al. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev, 2000, 14: 2366–2376

    Article  PubMed  CAS  Google Scholar 

  50. Nilsson O, Lee I, Blázquez M A, et al. Flowering time genes modulate the response to LEAFY activity. Genetics, 1998, 150: 403–410

    PubMed  CAS  Google Scholar 

  51. Wigge P A, Kim M C, Jaeger K E, et al. Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 2005, 309: 1056–1059

    Article  PubMed  CAS  Google Scholar 

  52. Parcy F, Nilsson O, Busch M A, et al. A genetic framework for floral patterning. Nature, 1998, 395: 561–566

    Google Scholar 

  53. Ruiz-Garcia L, Madueno F, Wilkinson M, et al. Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis, Plant Cell, 1997, 9: 1921–1934

    Article  PubMed  CAS  Google Scholar 

  54. Wagner D, Sablowski R W, Meyerowitz E M. Transcriptional activation of APETALA1 by LEAFY. Science, 1999, 285: 582–584

    Article  PubMed  CAS  Google Scholar 

  55. Lamb R S, Hill T A, Tan Q-K, et al. Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development, 2002, 129(9): 2079–2086

    PubMed  CAS  Google Scholar 

  56. Hsu H-F, Yang C-H. An orchid (Oncidium Gower Ramsey) AP3-like MADS gene regulates floral formation and initiation. Plant Cell Physiol, 2002, 43: 1198–1209

    Article  PubMed  CAS  Google Scholar 

  57. Hartmann U, Hohmann S, Nettesheim K, et al. Molecular cloning of SVP: A negative regulator of the floral transition in Arabidopsis. Plant J, 2000, 21: 351–360

    Article  PubMed  CAS  Google Scholar 

  58. Gregis V, Sessa A, Colombo L, et al. AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell, 2006, 18: 1373–1382

    Article  PubMed  CAS  Google Scholar 

  59. Sridhar V V, Surendrarao A, Liu Z. APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development, 2006, 133(16): 3159–3166

    Article  PubMed  CAS  Google Scholar 

  60. Ferrario S, Busscher J, Franken J, et al. Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner. Plant Cell, 2004, 16: 1490–1505

    Article  PubMed  CAS  Google Scholar 

  61. Trevaskis B, Tadege M, Hemming M N, et al. Short Vegetative Phase-like MADS-Box genes inhibit floral meristem identity in barley. Plant Physiol, 2006, 143: 225–235

    Article  PubMed  Google Scholar 

  62. Kim S-Y, Yun P-Y, Fukuda T, et al. Expression of a DEFICIENS-like gene correlates with the differentiation between sepal and petal in the orchid, Habenaria radiata (Orchidaceae). Plant Sci, 2007, 172: 319–326

    Article  CAS  Google Scholar 

  63. Battaglia R, Brambilla V, Colombo L, et al. Functional analysis of MADS-box genes controlling ovule development in Arabidopsis using the ethanol-inducible alc gene-expression system. Mechan Dev, 2006, 123: 267–276

    Article  CAS  Google Scholar 

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Fan, J., Li, W., Dong, X. et al. Ectopic expression of a hyacinth AGL6 homolog caused earlier flowering and homeotic conversion in Arabidopsis . SCI CHINA SER C 50, 676–689 (2007). https://doi.org/10.1007/s11427-007-0083-4

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  • DOI: https://doi.org/10.1007/s11427-007-0083-4

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