Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1998 Feb;10(2):171–182. doi: 10.1105/tpc.10.2.171

Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate.

M M Kater 1, L Colombo 1, J Franken 1, M Busscher 1, S Masiero 1, M M Van Lookeren Campagne 1, G C Angenent 1
PMCID: PMC143982  PMID: 9490741

Abstract

The C function in Arabidopsis, which specifies stamen and carpel identity, is represented by a single gene called AGAMOUS (AG). From both petunia and cucumber, two MADS box genes have been isolated. Both share a high degree of amino acid sequence identity with the Arabidopsis AG protein. Their roles in specifying stamen and carpel identity have been studied by ectopic expression in petunia, resulting in plants with different floral phenotypes. Cucumber MADS box gene 1 (CUM1) induced severe homeotic transformations of sepals into carpelloid structures and petals into stamens, which is similar to ectopic AG expression in Arabidopsis plants. Overexpression of the other cucumber AG homolog, CUM10, resulted in plants with partial transformations of the petals into antheroid structures, indicating that CUM10 is also able to promote floral organ identity. From the two petunia AG homologs pMADS3 and Floral Binding Protein gene 6 (FBP6), only pMADS3 was able to induce homeotic transformations of sepals and petals. Ectopic expression of both pMADS3 and FBP6, as occurrs in the petunia homeotic mutant blind, phenocopies the pMADS3 single overexpresser plants, indicating that there is no additive effect of concerted expression. This study demonstrates that in petunia and cucumber, multiple AG homologs exist, although they differ in their ability to induce reproductive organ fate.

Full Text

The Full Text of this article is available as a PDF (708.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Angenent G. C., Busscher M., Franken J., Mol J. N., van Tunen A. J. Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant Cell. 1992 Aug;4(8):983–993. doi: 10.1105/tpc.4.8.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Angenent G. C., Franken J., Busscher M., Colombo L., van Tunen A. J. Petal and stamen formation in petunia is regulated by the homeotic gene fbp1. Plant J. 1993 Jul;4(1):101–112. doi: 10.1046/j.1365-313x.1993.04010101.x. [DOI] [PubMed] [Google Scholar]
  3. Angenent G. C., Franken J., Busscher M., van Dijken A., van Went J. L., Dons H. J., van Tunen A. J. A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell. 1995 Oct;7(10):1569–1582. doi: 10.1105/tpc.7.10.1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bowman J. L., Smyth D. R., Meyerowitz E. M. Genetic interactions among floral homeotic genes of Arabidopsis. Development. 1991 May;112(1):1–20. doi: 10.1242/dev.112.1.1. [DOI] [PubMed] [Google Scholar]
  5. Bradley D., Carpenter R., Sommer H., Hartley N., Coen E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell. 1993 Jan 15;72(1):85–95. doi: 10.1016/0092-8674(93)90052-r. [DOI] [PubMed] [Google Scholar]
  6. Carpenter R., Coen E. S. Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 1990 Sep;4(9):1483–1493. doi: 10.1101/gad.4.9.1483. [DOI] [PubMed] [Google Scholar]
  7. Coen E. S., Meyerowitz E. M. The war of the whorls: genetic interactions controlling flower development. Nature. 1991 Sep 5;353(6339):31–37. doi: 10.1038/353031a0. [DOI] [PubMed] [Google Scholar]
  8. Colombo L., Franken J., Koetje E., van Went J., Dons H. J., Angenent G. C., van Tunen A. J. The petunia MADS box gene FBP11 determines ovule identity. Plant Cell. 1995 Nov;7(11):1859–1868. doi: 10.1105/tpc.7.11.1859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drews G. N., Bowman J. L., Meyerowitz E. M. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell. 1991 Jun 14;65(6):991–1002. doi: 10.1016/0092-8674(91)90551-9. [DOI] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  11. Florack D. E., Dirkse W. G., Visser B., Heidekamp F., Stiekema W. J. Expression of biologically active hordothionins in tobacco. Effects of pre- and pro-sequences at the amino and carboxyl termini of the hordothionin precursor on mature protein expression and sorting. Plant Mol Biol. 1994 Jan;24(1):83–96. doi: 10.1007/BF00040576. [DOI] [PubMed] [Google Scholar]
  12. Huang H., Mizukami Y., Hu Y., Ma H. Isolation and characterization of the binding sequences for the product of the Arabidopsis floral homeotic gene AGAMOUS. Nucleic Acids Res. 1993 Oct 11;21(20):4769–4776. doi: 10.1093/nar/21.20.4769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kang H. G., Noh Y. S., Chung Y. Y., Costa M. A., An K., An G. Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol Biol. 1995 Oct;29(1):1–10. doi: 10.1007/BF00019114. [DOI] [PubMed] [Google Scholar]
  14. Kempin S. A., Mandel M. A., Yanofsky M. F. Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol. 1993 Dec;103(4):1041–1046. doi: 10.1104/pp.103.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Koes R., Souer E., van Houwelingen A., Mur L., Spelt C., Quattrocchio F., Wing J., Oppedijk B., Ahmed S., Maes T. Targeted gene inactivation in petunia by PCR-based selection of transposon insertion mutants. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8149–8153. doi: 10.1073/pnas.92.18.8149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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 Mar;5(3):484–495. doi: 10.1101/gad.5.3.484. [DOI] [PubMed] [Google Scholar]
  17. Mandel M. A., Bowman J. L., Kempin S. A., Ma H., Meyerowitz E. M., Yanofsky M. F. Manipulation of flower structure in transgenic tobacco. Cell. 1992 Oct 2;71(1):133–143. doi: 10.1016/0092-8674(92)90272-e. [DOI] [PubMed] [Google Scholar]
  18. Mena M., Ambrose B. A., Meeley R. B., Briggs S. P., Yanofsky M. F., Schmidt R. J. Diversification of C-function activity in maize flower development. Science. 1996 Nov 29;274(5292):1537–1540. doi: 10.1126/science.274.5292.1537. [DOI] [PubMed] [Google Scholar]
  19. Mizukami Y., Huang H., Tudor M., Hu Y., Ma H. Functional domains of the floral regulator AGAMOUS: characterization of the DNA binding domain and analysis of dominant negative mutations. Plant Cell. 1996 May;8(5):831–845. doi: 10.1105/tpc.8.5.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mizukami Y., Ma H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell. 1992 Oct 2;71(1):119–131. doi: 10.1016/0092-8674(92)90271-d. [DOI] [PubMed] [Google Scholar]
  21. Pnueli L., Abu-Abeid M., Zamir D., Nacken W., Schwarz-Sommer Z., Lifschitz E. The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J. 1991 Sep;1(2):255–266. [PubMed] [Google Scholar]
  22. Pnueli L., Hareven D., Rounsley S. D., Yanofsky M. F., Lifschitz E. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell. 1994 Feb;6(2):163–173. doi: 10.1105/tpc.6.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pollock R., Treisman R. Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev. 1991 Dec;5(12A):2327–2341. doi: 10.1101/gad.5.12a.2327. [DOI] [PubMed] [Google Scholar]
  24. Purugganan M. D., Rounsley S. D., Schmidt R. J., Yanofsky M. F. Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics. 1995 May;140(1):345–356. doi: 10.1093/genetics/140.1.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Saedler H., Huijser P. Molecular biology of flower development in Antirrhinum majus (snapdragon). Gene. 1993 Dec 15;135(1-2):239–243. doi: 10.1016/0378-1119(93)90071-a. [DOI] [PubMed] [Google Scholar]
  26. Savidge B., Rounsley S. D., Yanofsky M. F. Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell. 1995 Jun;7(6):721–733. doi: 10.1105/tpc.7.6.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schwarz-Sommer Z., Huijser P., Nacken W., Saedler H., Sommer H. Genetic Control of Flower Development by Homeotic Genes in Antirrhinum majus. Science. 1990 Nov 16;250(4983):931–936. doi: 10.1126/science.250.4983.931. [DOI] [PubMed] [Google Scholar]
  28. Tsuchimoto S., van der Krol A. R., Chua N. H. Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell. 1993 Aug;5(8):843–853. doi: 10.1105/tpc.5.8.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Verwoerd T. C., Dekker B. M., Hoekema A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989 Mar 25;17(6):2362–2362. doi: 10.1093/nar/17.6.2362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weigel D., Meyerowitz E. M. The ABCs of floral homeotic genes. Cell. 1994 Jul 29;78(2):203–209. doi: 10.1016/0092-8674(94)90291-7. [DOI] [PubMed] [Google Scholar]
  31. Yanofsky M. F., Ma H., Bowman J. L., Drews G. N., Feldmann K. A., Meyerowitz E. M. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990 Jul 5;346(6279):35–39. doi: 10.1038/346035a0. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES