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. 1996 Jan;8(1):81–94. doi: 10.1105/tpc.8.1.81

DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation.

H Huang 1, M Tudor 1, T Su 1, Y Zhang 1, Y Hu 1, H Ma 1
PMCID: PMC161083  PMID: 8597661

Abstract

MADS domain proteins are members of a highly conserved family found in all eukaryotes. Genetic studies clearly indicate that many plant MADS domain proteins have different regulatory functions in flower development, yet they share a highly conserved DNA binding domain and can bind to very similar sequences. How, then, can these MADS box genes confer their specific functions? Here, we describe results from DNA binding studies of AGL1 and AGL2 (for AGAMOUS-like), two Arabidopsis MADS domain proteins that are preferentially expressed in flowers. We demonstrate that both proteins are sequence-specific DNA binding proteins and show that each binding consensus has distinct features, suggestion a mechanism for specificity. In addition, we show that the proteins with more similar amino acid sequences have more similar binding sequences. We also found that AGL2 binds to DNA in vitro as a dimer and determined the region of AGL2 that is sufficient for DNA binding and dimerization. Finally, we show that several plant MADS domain proteins can bind to DNA either as homodimers or as heterodimers, suggesting that the number of different regulators could be much greater than the number of MADS box genes.

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Selected References

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  1. Bowman J. L., Drews G. N., Meyerowitz E. M. Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell. 1991 Aug;3(8):749–758. doi: 10.1105/tpc.3.8.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bowman J. L., Smyth D. R., Meyerowitz E. M. Genes directing flower development in Arabidopsis. Plant Cell. 1989 Jan;1(1):37–52. doi: 10.1105/tpc.1.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Flanagan C. A., Ma H. Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers. Plant Mol Biol. 1994 Oct;26(2):581–595. doi: 10.1007/BF00013745. [DOI] [PubMed] [Google Scholar]
  6. Gehring W. J. Homeo boxes in the study of development. Science. 1987 Jun 5;236(4806):1245–1252. doi: 10.1126/science.2884726. [DOI] [PubMed] [Google Scholar]
  7. Haran T. E., Kahn J. D., Crothers D. M. Sequence elements responsible for DNA curvature. J Mol Biol. 1994 Nov 25;244(2):135–143. doi: 10.1006/jmbi.1994.1713. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Huang H., Tudor M., Weiss C. A., Hu Y., Ma H. The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol Biol. 1995 Jun;28(3):549–567. doi: 10.1007/BF00020401. [DOI] [PubMed] [Google Scholar]
  10. Huijser P., Klein J., Lönnig W. E., Meijer H., Saedler H., Sommer H. Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J. 1992 Apr;11(4):1239–1249. doi: 10.1002/j.1460-2075.1992.tb05168.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Irish V. F., Sussex I. M. Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell. 1990 Aug;2(8):741–753. doi: 10.1105/tpc.2.8.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Kempin S. A., Savidge B., Yanofsky M. F. Molecular basis of the cauliflower phenotype in Arabidopsis. Science. 1995 Jan 27;267(5197):522–525. doi: 10.1126/science.7824951. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Mizukami Y., Ma H. Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA. Plant Mol Biol. 1995 Aug;28(5):767–784. doi: 10.1007/BF00042064. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Passmore S., Elble R., Tye B. K. A protein involved in minichromosome maintenance in yeast binds a transcriptional enhancer conserved in eukaryotes. Genes Dev. 1989 Jul;3(7):921–935. doi: 10.1101/gad.3.7.921. [DOI] [PubMed] [Google Scholar]
  19. Passmore S., Maine G. T., Elble R., Christ C., Tye B. K. Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MAT alpha cells. J Mol Biol. 1988 Dec 5;204(3):593–606. doi: 10.1016/0022-2836(88)90358-0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. Smyth D. R., Bowman J. L., Meyerowitz E. M. Early flower development in Arabidopsis. Plant Cell. 1990 Aug;2(8):755–767. doi: 10.1105/tpc.2.8.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sommer H., Beltrán J. P., Huijser P., Pape H., Lönnig W. E., Saedler H., Schwarz-Sommer Z. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 1990 Mar;9(3):605–613. doi: 10.1002/j.1460-2075.1990.tb08152.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Struhl K. Helix-turn-helix, zinc-finger, and leucine-zipper motifs for eukaryotic transcriptional regulatory proteins. Trends Biochem Sci. 1989 Apr;14(4):137–140. doi: 10.1016/0968-0004(89)90145-X. [DOI] [PubMed] [Google Scholar]
  28. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]

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