Abstract
Expression patterns from in situ hybridization of four MADS-box genes (GGM7, GGM9, GGM11, and GGM15) from the gymnosperm species Gnetum gnemon are presented. Together with previously published data about putative orthologs of floral homeotic genes from G. gnemon (GGM2, GGM3, GGM13), we describe seven temporally and spatially distinct expression patterns in male, female or both types of reproductive units which very likely reflect the diversity of MADS-box gene function in gymnosperm cones. There is evidence that some aspects of the observed differential expression have been conserved since the last common ancestor of extant angiosperms and gymnosperms about 300 million years ago.
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References
Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phyl Evol (in press)
Becker A, Winter K-U, Meyer B, Saedler H, Theissen G (2000) MADS-box gene diversity in seed plants 300 million years ago. Mol Biol Evol 17:1425–1434
Becker A, Kaufmann K, Freialdenhoven A, Vincent C, Li M-A, Saedler H, Theissen G (2002) A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol Genet Genom 266:942–950
Force A, Lynch M, Pickett FB, Amores A, Yan Y-I, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Goremykin V, Hansmann S, Martin WF (1997) Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: revised molecular estimates of two seed plant divergence times. Plant Syst Evol 206:337–351
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 209:525–529
Hufford L (1996) The morphology and evolution of male reproductive structures of Gnetales. Int J Plant Sci 157:S95-S112
Jack T (2001) Relearning our ABCs: new twists on an old model. Trends Plant Sci 6:310–316
Mouradov A, Glassick T, Hamdorf B, Murphy LC, Marla SS, Yang Y, Teasdale RD (1998) Family of MADS-box genes expressed early in male and female reproductive structures of Monterey pine. Plant Physiol 117:66–61
Mouradov A, Hamdorf B, Teasdale RD, Kim JT, Winter K-U, Theissen G (1999) A DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. Dev Genet 25:245–252
Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195
Pelaz S, Ditta GS, Baumann E, Wissmann E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203
Riechmann JL, Meyerowitz EM (1997) MADS-domain proteins in plant development. Biol Chem 378:1079–1101
Rutledge R, Regan S, Nicolas O, Forbert P, Cote C, Bosnich W, Kauffeldt C, Sunohara G, Seguin A, Stewart D (1998) Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. Plant J 15:625–634
Schwarz-Sommer S, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931–936
Shindo S, Ito M, Ueda M, Hasebe M (1999) Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev 1:180–190
Sundström J, Carlsbecker A, Svensson ME, Svenson M, Johansen U, Theissen G, Engström P (1999) MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. Dev Genet 25:253–266
Tandre K, Albert VA, Sundas A, Engström P (1995) Conifer homologs to genes that control floral development in angiosperms. Plant Mol Biol 27:69–78
Tandre K, Svenson M, Svensson ME, Engström P (1998) Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J 15:615–623
Theissen G (2001a) Flower development, genetics of. In: Brenner S, Miller JH (eds) Encyclopedia of genetics. Academic Press, London, pp 713–717
Theissen G (2001b) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85
Theissen G (2001c) Genetics of identity. Nature 414:491
Theissen G, Saedler H (1995) MADS-box genes in plant ontogeny and phylogeny: Haeckel’s ‘biogenetic law’ revisited. Curr Opin Genet Dev 5:628–639
Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter K-U, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149
Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209
Winter K-U, Becker A, Münster T, Kim JT, Saedler H, Theissen G (1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc Natl Sci USA 96:7342–7347
Winter K-U, Saedler H, Theissen G (2002) On the origin of class B floral homeotic genes: functional substitution and dominant inhibition in Arabidopsis by expression of an orthologue from the gymnosperm Gnetum. Plant J 31:457–475
Acknowledgements
We thank T. Stützel (Botanical Garden Bochum, Germany), A. Piernitzki and M. Weisenseel (Botanical Garden Karlsruhe, Germany) for providing plant material from Gnetum gnemon, W. Martin for providing GAP-DH cDNA from Gnetum gnemon, B. Grosardt for excellent technical assistance, and K.-U. Winter for providing colour photos of the GGM2 and GGM3 in situ hybridization and stimulating discussions. The work was funded by grants from the Deutsche Forschungsgemeinschaft to G.T. (Th 417/3-1 and -2) and to A.B. (Graduiertenkolleg “Molekulare Analyse von Entwicklungsprozessen bei Pflanzen”).
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Becker, A., Saedler, H. & Theissen, G. Distinct MADS-box gene expression patterns in the reproductive cones of the gymnosperm Gnetum gnemon . Dev Genes Evol 213, 567–572 (2003). https://doi.org/10.1007/s00427-003-0358-0
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DOI: https://doi.org/10.1007/s00427-003-0358-0