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. 1996 May 14;93(10):4793–4798. doi: 10.1073/pnas.93.10.4793

Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS.

J L Riechmann 1, B A Krizek 1, E M Meyerowitz 1
PMCID: PMC39358  PMID: 8643482

Abstract

The MADS domain homeotic proteins APETALA1 (AP1), APETALA3 (AP3), PISTILLATA (PI), and AGAMOUS (AG) act in a combinatorial manner to specify the identity of Arabidopsis floral organs. The molecular basis for this combinatorial mode of action was investigated. Immunoprecipitation experiments indicate that all four proteins are capable of interacting with each other. However, these proteins exhibit "partner-specificity" for the formation of DNA-binding dimers; only AP1 homodimers, AG homodimers, and AP3/PI heterodimers are capable of binding to CArG-box sequences. Both the AP3/PI heterodimer and the AP1 or AG homodimers are formed when the three corresponding proteins are present together. The use of chimeric proteins formed by domain swapping indicates that the L region (which follows the MADS box) constitutes a key molecular determinant for the selective formation of DNA-binding dimers. The implications of these results for the ABC genetic model of flower development are discussed.

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Selected References

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  1. 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]
  2. Goto K., Meyerowitz E. M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 1994 Jul 1;8(13):1548–1560. doi: 10.1101/gad.8.13.1548. [DOI] [PubMed] [Google Scholar]
  3. Gustafson-Brown C., Savidge B., Yanofsky M. F. Regulation of the arabidopsis floral homeotic gene APETALA1. Cell. 1994 Jan 14;76(1):131–143. doi: 10.1016/0092-8674(94)90178-3. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Jack T., Brockman L. L., Meyerowitz E. M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell. 1992 Feb 21;68(4):683–697. doi: 10.1016/0092-8674(92)90144-2. [DOI] [PubMed] [Google Scholar]
  6. Jack T., Fox G. L., Meyerowitz E. M. Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell. 1994 Feb 25;76(4):703–716. doi: 10.1016/0092-8674(94)90509-6. [DOI] [PubMed] [Google Scholar]
  7. Jofuku K. D., den Boer B. G., Van Montagu M., Okamuro J. K. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell. 1994 Sep;6(9):1211–1225. doi: 10.1105/tpc.6.9.1211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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 Jan;122(1):11–22. doi: 10.1242/dev.122.1.11. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Mandel M. A., Gustafson-Brown C., Savidge B., Yanofsky M. F. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature. 1992 Nov 19;360(6401):273–277. doi: 10.1038/360273a0. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Mueller C. G., Nordheim A. A protein domain conserved between yeast MCM1 and human SRF directs ternary complex formation. EMBO J. 1991 Dec;10(13):4219–4229. doi: 10.1002/j.1460-2075.1991.tb05000.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Okamoto H., Yano A., Shiraishi H., Okada K., Shimura Y. Genetic complementation of a floral homeotic mutation, apetala3, with an Arabidopsis thaliana gene homologous to DEFICIENS of Antirrhinum majus. Plant Mol Biol. 1994 Oct;26(1):465–472. doi: 10.1007/BF00039556. [DOI] [PubMed] [Google Scholar]
  14. Pellegrini L., Tan S., Richmond T. J. Structure of serum response factor core bound to DNA. Nature. 1995 Aug 10;376(6540):490–498. doi: 10.1038/376490a0. [DOI] [PubMed] [Google Scholar]
  15. Pollock R., Treisman R. A sensitive method for the determination of protein-DNA binding specificities. Nucleic Acids Res. 1990 Nov 11;18(21):6197–6204. doi: 10.1093/nar/18.21.6197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Rounsley S. D., Ditta G. S., Yanofsky M. F. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell. 1995 Aug;7(8):1259–1269. doi: 10.1105/tpc.7.8.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schwarz-Sommer Z., Hue I., Huijser P., Flor P. J., Hansen R., Tetens F., Lönnig W. E., Saedler H., Sommer H. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 1992 Jan;11(1):251–263. doi: 10.1002/j.1460-2075.1992.tb05048.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sharrocks A. D., Gille H., Shaw P. E. Identification of amino acids essential for DNA binding and dimerization in p67SRF: implications for a novel DNA-binding motif. Mol Cell Biol. 1993 Jan;13(1):123–132. doi: 10.1128/mcb.13.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shiraishi H., Okada K., Shimura Y. Nucleotide sequences recognized by the AGAMOUS MADS domain of Arabidopsis thaliana in vitro. Plant J. 1993 Aug;4(2):385–398. doi: 10.1046/j.1365-313x.1993.04020385.x. [DOI] [PubMed] [Google Scholar]
  22. Shore P., Sharrocks A. D. The MADS-box family of transcription factors. Eur J Biochem. 1995 Apr 1;229(1):1–13. doi: 10.1111/j.1432-1033.1995.tb20430.x. [DOI] [PubMed] [Google Scholar]
  23. Tröbner W., Ramirez L., Motte P., Hue I., Huijser P., Lönnig W. E., Saedler H., Sommer H., Schwarz-Sommer Z. GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J. 1992 Dec;11(13):4693–4704. doi: 10.1002/j.1460-2075.1992.tb05574.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Weigel D. The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell. 1995 Apr;7(4):388–389. doi: 10.1105/tpc.7.4.388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wynne J., Treisman R. SRF and MCM1 have related but distinct DNA binding specificities. Nucleic Acids Res. 1992 Jul 11;20(13):3297–3303. doi: 10.1093/nar/20.13.3297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]

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