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After a dozen years of progress the origin of angiosperms is still a great mystery

Nature volume 450, pages 1184–1189 (2007)Cite this article

Abstract

Here we discuss recent advances surrounding the origin of angiosperms. Putatively primitive characters are now much better understood because of a vastly improved understanding of angiosperm phylogenetics, and recent discoveries of fossil flowers have provided an increasingly detailed picture of early diversity in the angiosperms. The ‘anthophyte theory’, the dominant concept of the 1980s and 1990s, has been eclipsed; Gnetales, previously thought to be closest to the angiosperms, are related instead to other extant gymnosperms, probably most closely to conifers. Finally, new theories of flower origins have been proposed based on gene function, duplication and loss, as well as on morphology. Further studies of genetic mechanisms that control reproductive development in seed plants provide a most promising avenue for further research, including tests of these recent theories. Identification of fossils with morphologies that convincingly place them close to angiosperms could still revolutionize understanding of angiosperm origins.

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Figure 1
Figure 2: Welwitschia cones.
Figure 3: Fossil gymnosperms.
Figure 4: Steps in the mostly male theory.
Figure 5: Ginkgo leaves bearing ectopic ovules (and showing autumn colour).

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References

  1. Frohlich, M. W. in Developmental Genetics of the Flower (eds Soltis, D. E., Leebens-Mack, J. H. & Soltis, P. S.) 63–127 (Academic, San Diego, CA, 2006)

    Book  Google Scholar 

  2. Crane, P. R., Friis, E. M. & Pedersen, K. R. The origin and early diversification of angiosperms. Nature 374, 27–33 (1995)

    Article  ADS  CAS  Google Scholar 

  3. Soltis, P. S., Endress, P. K., Chase, M. W. & Soltis, D. E. Angiosperm Phylogeny and Evolution (Sinauer, Sunderland, MA, 2005)

    Google Scholar 

  4. Saarela, J. M. et al. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446, 312–315 (2007)

    Article  ADS  CAS  Google Scholar 

  5. Rudall, P. J. et al. Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early-divergent angiosperm lineage. Am. J. Bot. 94, 1073–1092 (2007)

    Article  Google Scholar 

  6. Friis, E. M., Pedersen, K. R. & Crane, P. R. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 251–293 (2006)

    Article  Google Scholar 

  7. Rydin, C., Pedersen, K. R., Crane, P. R. & Friis, E.-M. Former diversity of Ephedra (Gnetales): Evidence from Early Cretaceous seeds from Portugal and North America. Ann. Bot. (Lond.) 98, 123–140 (2006)

    Article  Google Scholar 

  8. Friis, E. M., Doyle, J. A., Endress, P. K. & Leng, Q. Archaefructus—angiosperm precursor or specialized early angiosperm? Trends Plant Sci. 8, 369–373 (2003)

    Article  CAS  Google Scholar 

  9. Ji, Q. et al. Early Cretaceous Archaefructus eoflora sp. nov. with bisexual flowers from Beipiao, Western Liaoning, China. Acta Geol. Sin. Engl. Edn 78, 883–896 (2004)

    Google Scholar 

  10. Anderson, J. M. & Anderson, H. M. Heyday of the Gymnosperms: Systematics and Biodiversity of the late Trassic Molteno Fructifications (National Botanical Institute, Pretoria, 2003)

    Google Scholar 

  11. Crane, P. R. Phylogenetic analysis of seed plants and the origin of angiosperms. Ann. Mo. Bot. Gard. 72, 716–793 (1985)

    Article  Google Scholar 

  12. Doyle, J. A. & Donoghue, M. J. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Bot. Rev. 52, 321–431 (1986)

    Article  Google Scholar 

  13. Doyle, J. A. Seed plant phylogeny and the relationships of Gnetales. Int. J. Plant Sci. 157, S3–S39 (1996)

    Article  Google Scholar 

  14. Burleigh, J. G. & Mathews, S. Assessing among-locus variation in the inference of seed plant phylogeny. Int. J. Plant Sci. 168, 111–124 (2007)

    Article  CAS  Google Scholar 

  15. Hilton, J. & Bateman, R. M. Pteridosperms are the backbone of seed-plant phylogeny. J. Torrey Bot. Soc. 133, 119–168 (2006)

    Article  Google Scholar 

  16. Bateman, R. M., Hilton, J. & Rudall, P. J. Morphological and molecular phylogenetic context of the angiosperms: contrasting the ‘top-down’ and ‘bottom-up’ approaches used to infer the likely characteristics of the first flowers. J. Exp. Bot. 13, 3471–3503 (2006)

    Article  Google Scholar 

  17. Doyle, J. A. Seed ferns and the origin of angiosperms. J. Torrey Bot. Soc. 133, 169–209 (2006)

    Article  Google Scholar 

  18. Doyle, J. A. & Endress, P. K. Morphological phylogenetic analysis of basal angiosperms: Comparison and combination with molecular data. Int. J. Plant Sci. 161, S121–S153 (2000)

    Article  CAS  Google Scholar 

  19. Soltis, D. E. et al. The evolving floral genome: A history of genome-wide duplications and shifting patterns of gene expression. Trends Plant Sci. 12, 358–367 (2007)

    Article  CAS  Google Scholar 

  20. Taylor, D. W. et al. Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils. Paleobiology 32, 179–190 (2006)

    Article  Google Scholar 

  21. Auras, S. et al. Aromatized arborane/fernane hydrocarbons as biomarkers for Cordaites. Naturwissenschaften 93, 616–621 (2006)

    Article  ADS  CAS  Google Scholar 

  22. Stebbins, G. L. Flowering Plants Evolution above the Species Level (Harvard Univ. Press, Cambridge, MA, 1974)

    Book  Google Scholar 

  23. Retallack, G. & Dilcher, D. L. Arguments for a glossopterid ancestry of angiosperms. Paleobiology 71, 54–67 (1981)

    Article  Google Scholar 

  24. Friedman, W. E. & Williams, J. H. Modularity of the angiosperm female gametophyte and its bearing on the early evolution of endosperm in flowering plants. Evolution Int. J. Org. Evolution 57, 216–230 (2003)

    Article  Google Scholar 

  25. Hughes, N. F. 1994. The Enigma of Angiosperm Origins (Cambridge Univ. Press, Cambridge, 1994)

    Google Scholar 

  26. Krassilov, V. A. Angiosperm Origins: Morphological and Ecological Aspects (Pensoft Publishers, Sofia, Bulgaria, 1997)

    Google Scholar 

  27. Litt, A. Evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int. J. Plant Sci. 168, 73–91 (2007)

    Article  CAS  Google Scholar 

  28. Albert, V. A., Gustafsson, M. H. G. & Di Laurenzio, L. in Molecular Systematics of Plants II: DNA Sequencing (eds Soltis, D. E., Soltis, P. S. & Doyle, J. J.) 349–374 (Kluwer Academic, Dordrecht, 1998)

    Book  Google Scholar 

  29. Kramer, E. M., Jaramillo, M. A. & Di Stilio, V. S. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166, 1011–1023 (2004)

    Article  CAS  Google Scholar 

  30. Zahn, L. M. et al. Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol. Dev. 8, 30–45 (2006)

    Article  CAS  Google Scholar 

  31. Skinner, D. J., Hill, T. A. & Gasser, C. S. Regulation of ovule development. Plant Cell 16, S32–S45 (2004)

    Article  CAS  Google Scholar 

  32. Buzgo, M., Soltis, P. S. & Soltis, D. E. Floral developmental morphology of Amborella trichopoda (Amborellaceae). Int. J. Plant Sci. 165, 925–947 (2004)

    Article  Google Scholar 

  33. Theissen, G. et al. in Developmental Genetics and Plant Evolution (eds Cronk, Q. C. B., Bateman, R. M. & Hawkins, J. A.) 173–206 (Taylor & Francis, London, 2002)

    Google Scholar 

  34. Theissen, G. & Becker, A. Gymnosperm orthologues of class B floral homeotic genes and their impact on understanding flower origin. Crit. Rev. Plant Sci. 23, 129–148 (2004)

    Article  CAS  Google Scholar 

  35. Baum, D. A. & Hileman, L. C. in Flowering and its Manipulation (ed. Ainsworth, C.) 3–27 (Blackwell, Oxford, 2006)

    Google Scholar 

  36. Frohlich, M. W. & Parker, D. S. The Mostly Male theory of flower evolutionary origins: from genes to fossils. Syst. Bot. 25, 155–170 (2000)

    Article  Google Scholar 

  37. Frohlich, M. W. in Developmental Genetics and Plant Evolution (eds Cronk, Q. C. B. & Bateman, R. M. & Hawkins, J. A.) 85–108 (Taylor & Francis, London, 2002)

    Book  Google Scholar 

  38. Frohlich, M. W. An evolutionary scenario for the origin of flowers. Nature Rev. Genet. 4, 559–566 (2003)

    Article  CAS  Google Scholar 

  39. Vázquez-Lobo, A. et al. Characterization of the expression patterns of LEAFY/FLORICAULA and NEEDLY orthologs in female and male cones of the conifer genera Picea, Podocarpus and Taxus: implications for current evo-devo hypotheses for gymnosperms. Evol. Dev. 9, 446–459 (2007)

    Article  Google Scholar 

  40. Meyen, S. V. Origin of the angiosperm gynoecium by gametoheterotopy. Bot. J. Linn. Soc. 97, 171–178 (1988)

    Article  Google Scholar 

  41. Kim, S. et al. Sequence and expression studies of A-, B-, and C-class Mads-box homologues in Eupomatia (Eupomatiaceae): support for the bracteate origin of the calyptra. Int. J. Plant Sci. 166, 185–198 (2005)

    Article  CAS  Google Scholar 

  42. Jaramillo, M. A. & Kramer, E. M. The role of developmental genetics in understanding homology and morphological evolution in plants. Int. J. Plant Sci. 168, 61–72 (2007)

    Article  CAS  Google Scholar 

  43. Long, J. & Barton, M. K. Initiation of axillary and floral meristems in Arabidopsis. Dev. Biol. 218, 341–353 (2000)

    Article  CAS  Google Scholar 

  44. Causier, B. et al. Evolution in action: Following function in duplicated floral homeotic genes. Curr. Biol. 15, 1508–1512 (2005)

    Article  CAS  Google Scholar 

  45. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380 (2005)

    Article  ADS  CAS  Google Scholar 

  46. Burch-Smith, T. M., Anderson, J. C., Martin, G. B. & Dinesh-Kumar, S. P. Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 39, 734–746 (2004)

    Article  CAS  Google Scholar 

  47. David-Schwartz, R. & Sinha, N. Evolution and development in plants: bridging the gap. Int. J. Plant Sci. 168, 49–59 (2007)

    Article  CAS  Google Scholar 

  48. De Bodt, S., Theissen, G. & Van de Peer, Y. Promoter analysis of MADS-box genes in eudicots through phylogenetic footprinting. Mol. Biol. Evol. 23, 1293–1303 (2006)

    Article  CAS  Google Scholar 

  49. Boozer, C. et al. Looking towards label-free biomolecular interaction analysis in a high-throughput format: a review of new surface plasmon resonance technologies. Curr. Opin. Biotechnol. 17, 400–405 (2006)

    Article  CAS  Google Scholar 

  50. Nalefski, E. A., Nebelitsky, E., Lloyd, J. A. & Gullans, S. R. Single-molecule detection of transcription factor binding to DNA in real time: Specificity, equilibrium, and kinetic parameters. Biochemistry 45, 13794–13806 (2006)

    Article  CAS  Google Scholar 

  51. Pryer, K. M. et al. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409, 618–622 (2001)

    Article  CAS  Google Scholar 

  52. Klavins, S. D., Taylor, T. N. & Taylor, E. L. Anatomy of Umkomasia (Corystospermales) from the Triassic of Antarctica. Am. J. Bot. 89, 664–676 (2002)

    Article  Google Scholar 

  53. Moore, M. J. et al. Using plastid-genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc. Natl. Acad. Sci. USA 104, 19363–19368 (2007)

    Article  ADS  Google Scholar 

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Acknowledgements

M.W.F. thanks the National Science Foundation (USA) for supporting work in this area. We thank J. A. Doyle, E.-M. Friis, P. S. Soltis, R. M. Bateman, P. Kenrick, D. E. Soltis and J. Hilton for commenting on the manuscript, and J. Trager and Huntington Gardens for Welwitschia materials.

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  1. Royal Botanic Gardens Kew, Richmond, Surrey TW9 3DS, UK,

    Michael W. Frohlich & Mark W. Chase

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Correspondence to Michael W. Frohlich.

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Frohlich, M., Chase, M. After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450, 1184–1189 (2007). https://doi.org/10.1038/nature06393

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