Plant Molecular Biology

, Volume 58, Issue 3, pp 435–445 | Cite as

The modified ABC model explains the development of the petaloid perianth of Agapanthus praecox ssp. orientalis (Agapanthaceae) flowers

  • Toru Nakamura
  • Tatsuya Fukuda
  • Masaru Nakano
  • Mitsuyasu Hasebe
  • Toshiaki Kameya
  • Akira Kanno
Article

Abstract

The class B genes, which belong to the MADS-box gene family, play important roles in regulating the development of petals and stamens in flowering plants. To understand the molecular mechanisms of floral development in Agapanthus praecox ssp. orientalis (Agapanthaceae), we isolated and characterized the homologs of the Antirrhinum majus genes GLOBOSA and DEFICIENS in this plant. These were designated as ApGLO and ApDEF, respectively. ApGLO and ApDEF contain open reading frames that encode deduced protein with 210 and 214 amino acid residues, respectively. Phylogenetic analysis indicated that ApGLO and ApDEF belong to the monocot class B gene family. In situ hybridization experiments revealed that hybridization signals of ApGLO and ApDEF were observed in whorl 1 as well as in whorls 2 and 3. Moreover, the flowers of transgenic Arabidopsis plants that ectopically expressed ApGLO formed petal-like organs in whorl 1. These observations indicate that the flower developmental mechanism of Agapanthus follows the modified ABC model.

Keywords

Agapanthus praecox class B gene flower development MADS-box gene modified ABC model 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bowman, J.L., Smyth, D.R., Meyerowitz, E.M. 1991Genetic interactions among floral homeotic genes of ArabidopsisDevelopment112120Google Scholar
  2. Carpenter, R., Coen, E.S. 1990Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majusGene. Dev414831493Google Scholar
  3. Chase, M.W., Soltis, D.E., Soltis, P.S., Rudall, P.J., Fay, M.F., Hahn, W.H., Sullivan, S., Joseph, J., Molvray, M., Kores, P.J., Givnish, T.J., Sytsma, K.J., Pires, J.C. 2000

    Higher-level systematics of the monocotyledons: an assessment of current knowledge and a new classification

    Wilson, K.L.Morrison, D.A. eds. MonocotsIII: Systematics and EvolutionCRISO publishingMelbourne316
    Google Scholar
  4. Cho, S., Jang, D., Chae, S., Chung, K.M., Moon, Y.H., An, G., Jang, S.K. 1999Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domainPlant Mol. Biol40419429Google Scholar
  5. Clough, S.J., Bent, A.F. 1998Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thalianaPlant J16735743Google Scholar
  6. Coen, E.S., Meyerowitz, E.M. 1991The war of the whorls: genetic interactions controlling flower developmentNature3533137Google Scholar
  7. Cronk, Q.C.B. 2002

    Perspective and paradigms in plant evo-devo

    Cronk, Q.C.B.Bateman, R.M.Hawkins, J.A. eds. Developmental Genetics and Plant EvolutionTaylor & FrancisLondon114
    Google Scholar
  8. Cseke, L.J., Zheng, J., Podila, G.K. 2003Characterization of PTM5 is aspen trees: a MADS-box gene expressed during woody vascular developmentGene3185567Google Scholar
  9. Drews, G.N., Bowman, J.L., Meyerowitz, E.M. 1991Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 productCell659911002Google Scholar
  10. Egea-Cortines, M., Saedler, H., Sommer, H. 1999Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majusEMBO J1853705379Google Scholar
  11. Frohman, M.A., Dush, M.K., Martin, G.R. 1988Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primerProc. Natl. Acad. Sci. USA8589989002Google Scholar
  12. Goto, K., Meyerowitz, E.M. 1994Function and regulation of the Arabidopsis floral homeotic gene PISTILLATAGene. Dev815481560Google Scholar
  13. Honma, T., Goto, K. 2001Complexes of MADS-box proteins are sufficient to convert leaves into floral organsNature409525529Google Scholar
  14. Hsu, H.F., Yang, C.H. 2002An Orchid (Oncidium ‘Gower Ramsey’) AP3-like MADS gene regulates floral formation and initiationPlant Cell Physiol4311981209Google Scholar
  15. Jack, T., Brockman, L.L., Meyerowitz, E.M. 1992The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamensCell68683687Google Scholar
  16. Jack, T., Fox, G.L., Meyerowitz, E.M. 1994Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identityCell76703716Google Scholar
  17. Kanno, A., Saeki, H., Kameya, T., Saedler, H., Theissen, G. 2003Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana)Plant Mol. Biol52831841Google Scholar
  18. Kramer, E.M., Dorit, R.L., Irish, V.F. 1998Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALLA3 and PISTILLATA MADS-box gene lineagesGenetics149765783Google Scholar
  19. Kramer, E.M., Stilio, V.S., Schluter, P.M. 2003Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the RununculaceaeInt. J. Plant Sci164111Google Scholar
  20. Krizek, B.A., Meyerowitz, E.M. 1996The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity functionDevelopment1221122Google Scholar
  21. Lamb, R.S., Irish, V.F. 2003Function divergence within the APETALA3 / PISTILLATA floral homeotic gene lineagesProc. Natl. Acad. Sci. USA10065586563Google Scholar
  22. Lim, J., Moon, Y.H., An, G., Jang, S.K. 2000Two rice MADS domain proteins interact with OsMADS1Plant Mol. Biol44513527Google Scholar
  23. Martin, C., Bhatt, K., Baumann, K., Jin, H., Zachgo, S., Roberts, K., Schwarz-Sommer, Z., Glover, B., Parez-Rodrigues, M. 2002The mechanics of cell fate determination in petalsPhil. Trans. R. Soc. Lond. B Biol. Sci357809813Google Scholar
  24. Mathews, S., Donoghue, M.J. 1999The root of angiosperm phylogeny inferred from duplicate phytochrome genesScience286947950Google Scholar
  25. Moon, Y.H., Jung, J.Y., Kang, H.G., An, G. 1999Identification of a rice APETALA3 homologue by yeast two-hybrid screeningPlant Mol. Biol40167177Google Scholar
  26. Noda, K., Glover, B.J., Linstead, P., Martin, C. 1994Flower color intensity depends on specialized cell shape controlled by a Myb-related transcription factorNature369661664Google Scholar
  27. Park, J.H., Ishikawa, Y., Yoshida, R., Kanno, A., Kameya, T. 2003Expression of AODEF, a B-functional MADS-box gene, in stamens and inner tepals of the dioecious species Asparagus officinalis LPlant Mol. Biol51867875Google Scholar
  28. Park, J.H., Ishikawa, Y., Ochiai, T., Kanno, A., Kameya, T. 2004Two GLOBOSA-like genes are expressed in second and third whorls of homochlamydeous flowers in Asparagus officinalis LPlant Cell Physiol45325332Google Scholar
  29. Perrière, G., Gouy, M. 1996WWW-Query: an on-line retrieval system for biological sequence banksBiochemie78364369Google Scholar
  30. Qiu, Y.L., Lee, J., Bernasconi-Quadroni, F., Soltis, D.E., Soltis, P.S., Zanis, M., Zimmer, E.A., Chen, Z., Savolainen, V., Chase, M.W. 1999The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomesNature402404407Google Scholar
  31. Schwartz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H., Sommer, H. 1990Genetic control of flower development by homeotic genes in Antirrhinum majusScience250931936Google Scholar
  32. Soltis, P.S., Soltis, D.E., Chase, M.W. 1999Angiosperm phylogeny inferred from multiple genes as a tool for comparative biologyNature402402404Google Scholar
  33. Stellari, G.M., Alejandra Jaramillo, M., Kramer, E.M. 2004Evolution of the APETALA3 and PISTILLATA lineages of MADS-box-containing genes in the basal angiospermsMol. Biol. Evol21506519Google Scholar
  34. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Münster, T., Winter, K.-U., Saedler, H. 2000A short history of MADS-box genes in plantsPlant Mol. Biol42115149Google Scholar
  35. Theissen, G. 2001Development of floral organ identity: stories from the MADS houseCurr. Opin. Plant Biol47585Google Scholar
  36. Thompson, J.D., Higgins, D.G., Gibson, T.J. 1994CLUSTAL W: improving the sensitivity multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choiceNucleic Acids Res2246734680Google Scholar
  37. Tröbner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lönnig, W., Saedler, H., Sommer, H., Schwarz-Sommer, Z. 1992GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesisEMBO J1146934704Google Scholar
  38. Tunen, A.J., Eikelboom, W., Angenent, G.C. 1993Floral organogenesis in TulipaFlowering Newsl163337Google Scholar
  39. Weigel, D., Meyerowitz, E.M. 1994The ABCs of floral homeotic genesCell78203209Google Scholar
  40. Wilkinson, M.D., Haughn, G.W. 1995UNUSUAL FLORAL ORGANS controls meristem identity and organ primordial fate in ArabidopsisPlant Cell714851499Google Scholar
  41. Winter, K.U., Weiser, C., Kaufmann, K., Bohne, A., Kirchner, C., Kanno, A., Saedler, H., Theissen, G. 2002Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerizationMol. Biol. Evol19587596Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Toru Nakamura
    • 1
  • Tatsuya Fukuda
    • 1
  • Masaru Nakano
    • 2
  • Mitsuyasu Hasebe
    • 3
  • Toshiaki Kameya
    • 1
  • Akira Kanno
    • 1
  1. 1.Graduate School of Life SciencesTohoku UniversityAoba-ku SendaiJapan
  2. 2.Faculty of AgricultureNiigata UniversityNiigataJapan
  3. 3.National Institute for Basic Biology, Department of Molecular BiomechanicsThe Graduate University for Advanced StudiesMyodaiji-cho OkazakiJapan

Personalised recommendations