Skip to main content
Genetics logoLink to Genetics
. 1998 Jun;149(2):765–783. doi: 10.1093/genetics/149.2.765

Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages.

E M Kramer 1, R L Dorit 1, V F Irish 1
PMCID: PMC1460198  PMID: 9611190

Abstract

The specification of floral organ identity in the higher dicots depends on the function of a limited set of homeotic genes, many of them members of the MADS-box gene family. Two such genes, APETALA3 (AP3) and PISTILLATA (PI), are required for petal and stamen identity in Arabidopsis; their orthologs in Antirrhinum exhibit similar functions. To understand how changes in these genes may have influenced the morphological evolution of petals and stamens, we have cloned twenty-six homologs of the AP3 and PI genes from two higher eudicot and eleven lower eudicot and magnolid dicot species. The sequences of these genes reveal the presence of characteristic PI- and AP3-specific motifs. While the PI-specific motif is found in all of the PI genes characterized to date, the lower eudicot and magnolid dicot AP3 homologs contain distinctly different motifs from those seen in the higher eudicots. An analysis of all the available AP3 and PI sequences uncovers multiple duplication events within each of the two gene lineages. A major duplication event in the AP3 lineage coincides with the base of the higher eudicot radiation and may reflect the evolution of a petal-specific AP3 function in the higher eudicot lineage.

Full Text

The Full Text of this article is available as a PDF (831.5 KB).

Selected References

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

  1. Ainsworth C., Crossley S., Buchanan-Wollaston V., Thangavelu M., Parker J. Male and female flowers of the dioecious plant sorrel show different patterns of MADS box gene expression. Plant Cell. 1995 Oct;7(10):1583–1598. doi: 10.1105/tpc.7.10.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Bennett M. D., Smith J. B. Nuclear dna amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci. 1976 May 27;274(933):227–274. doi: 10.1098/rstb.1976.0044. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. Carr S. M., Irish V. F. Floral homeotic gene expression defines developmental arrest stages in Brassica oleracea L. vars. botrytis and italica. Planta. 1997;201(2):179–188. doi: 10.1007/BF01007702. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Davies B., Di Rosa A., Eneva T., Saedler H., Sommer H. Alteration of tobacco floral organ identity by expression of combinations of Antirrhinum MADS-box genes. Plant J. 1996 Oct;10(4):663–677. doi: 10.1046/j.1365-313x.1996.10040663.x. [DOI] [PubMed] [Google Scholar]
  11. Davies B., Schwarz-Sommer Z. Control of floral organ identity by homeotic MADS-box transcription factors. Results Probl Cell Differ. 1994;20:235–258. doi: 10.1007/978-3-540-48037-2_11. [DOI] [PubMed] [Google Scholar]
  12. Garcia-Maroto F., Salamini F., Rohde W. Molecular cloning and expression patterns of three alleles of the Deficiens-homologous gene St-Deficiens from Solanum tuberosum. Plant J. 1993 Nov;4(5):771–780. doi: 10.1046/j.1365-313x.1993.04050771.x. [DOI] [PubMed] [Google Scholar]
  13. Hansen G., Estruch J. J., Sommer H., Spena A. NTGLO: a tobacco homologue of the GLOBOSA floral homeotic gene of Antirrhinum majus: cDNA sequence and expression pattern. Mol Gen Genet. 1993 May;239(1-2):310–312. doi: 10.1007/BF00281633. [DOI] [PubMed] [Google Scholar]
  14. Hardenack S., Ye D., Saedler H., Grant S. Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion. Plant Cell. 1994 Dec;6(12):1775–1787. doi: 10.1105/tpc.6.12.1775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hill T. A., Day C. D., Zondlo S. C., Thackeray A. G., Irish V. F. Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development. 1998 May;125(9):1711–1721. doi: 10.1242/dev.125.9.1711. [DOI] [PubMed] [Google Scholar]
  16. Krizek B. A., Meyerowitz E. M. Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4063–4070. doi: 10.1073/pnas.93.9.4063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kush A., Brunelle A., Shevell D., Chua N. H. The cDNA sequence of two MADS box proteins in Petunia. Plant Physiol. 1993 Jul;102(3):1051–1052. doi: 10.1104/pp.102.3.1051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. McGonigle B., Bouhidel K., Irish V. F. Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev. 1996 Jul 15;10(14):1812–1821. doi: 10.1101/gad.10.14.1812. [DOI] [PubMed] [Google Scholar]
  20. Münster T., Pahnke J., Di Rosa A., Kim J. T., Martin W., Saedler H., Theissen G. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2415–2420. doi: 10.1073/pnas.94.6.2415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Norman C., Runswick M., Pollock R., Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell. 1988 Dec 23;55(6):989–1003. doi: 10.1016/0092-8674(88)90244-9. [DOI] [PubMed] [Google Scholar]
  22. Purugganan M. D. The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J Mol Evol. 1997 Oct;45(4):392–396. doi: 10.1007/pl00006244. [DOI] [PubMed] [Google Scholar]
  23. Riechmann J. L., Krizek B. A., Meyerowitz E. M. Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci U S A. 1996 May 14;93(10):4793–4798. doi: 10.1073/pnas.93.10.4793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Riechmann J. L., Meyerowitz E. M. MADS domain proteins in plant development. Biol Chem. 1997 Oct;378(10):1079–1101. [PubMed] [Google Scholar]
  25. Riechmann J. L., Wang M., Meyerowitz E. M. DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 1996 Aug 15;24(16):3134–3141. doi: 10.1093/nar/24.16.3134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Samach A., Kohalmi S. E., Motte P., Datla R., Haughn G. W. Divergence of function and regulation of class B floral organ identity genes. Plant Cell. 1997 Apr;9(4):559–570. doi: 10.1105/tpc.9.4.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. 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]
  30. Theissen G., Kim J. T., Saedler H. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol. 1996 Nov;43(5):484–516. doi: 10.1007/BF02337521. [DOI] [PubMed] [Google Scholar]
  31. Theissen G., Saedler H. MADS-box genes in plant ontogeny and phylogeny: Haeckel's 'biogenetic law' revisited. Curr Opin Genet Dev. 1995 Oct;5(5):628–639. doi: 10.1016/0959-437x(95)80032-8. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. van der Krol A. R., Brunelle A., Tsuchimoto S., Chua N. H. Functional analysis of petunia floral homeotic MADS box gene pMADS1. Genes Dev. 1993 Jul;7(7A):1214–1228. doi: 10.1101/gad.7.7a.1214. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES