Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Embryological evidence for developmental lability during early angiosperm evolution


Recent advances in angiosperm phylogeny reconstruction1,2,3, palaeobotany4,5 and comparative organismic biology6,7,8 have provided the impetus for a major re-evaluation of the earliest phases of the diversification of flowering plants. We now know that within the first fifteen million years of angiosperm history, three major lineages of flowering plants—monocotyledons, eumagnoliids and eudicotyledons—were established5, and that within this window of time, tremendous variation in vegetative and floral characteristics evolved. Here I report on a novel type of embryo sac (angiosperm female gametophyte or haploid egg-producing structure) in Amborella trichopoda, the sole member of the most ancient extant angiosperm lineage. This is the first new pattern of embryo sac structure to be discovered among angiosperms in well over half a century. This discovery also supports the emerging view9,10,11,12 that the earliest phases of angiosperm evolution were characterized by an extensive degree of developmental experimentation and structural lability, and may provide evidence of a critical link to the gymnospermous ancestors of flowering plants.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: A seven-celled, eight-nucleate female gametophyte (Polygonum-type) that is common to the vast majority of angiosperms.
Figure 2: Transmission electron micrographs of an individual serially sectioned female gametophyte of Amborella.
Figure 3: Three-dimensional reconstructions (from semi-thin serial sections) of the four-celled egg apparatus of Amborella.
Figure 4: Terminal developmental stages of the egg apparatus in the female gametophyte of Amborella.
Figure 5: Development of the female gametophyte of Amborella.

Similar content being viewed by others


  1. Soltis, P. S. & Soltis, D. E. The origin and diversification of angiosperms. Am. J. Bot. 91, 1614–1626 (2004)

    Article  Google Scholar 

  2. Leebens-Mack, J. et al. Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one's way out of the Felsenstein zone. Mol. Biol. Evol. 22, 1948–1963 (2005)

    Article  CAS  Google Scholar 

  3. Qiu, Y.-L. et al. Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes. Int. J. Plant Sci. 166, 815–842 (2005)

    Article  CAS  Google Scholar 

  4. Friis, E. M., Pedersen, K. R. & Crane, P. R. Fossil floral structures of a basal angiosperm with monocolpate, reticulate-acolumellate pollen from the Early Cretaceous of Portugal. Grana 39, 226–239 (2000)

    Article  Google Scholar 

  5. Crane, P. R., Herendeen, P. & Friis, E. M. Fossils and plant phylogeny. Am. J. Bot. 91, 1683–1699 (2004)

    Article  Google Scholar 

  6. Carlquist, S. & Schneider, E. L. The tracheid-vessel element transition in angiosperms involves multiple independent features: Cladistic consequences. Am. J. Bot. 89, 185–195 (2002)

    Article  Google Scholar 

  7. Feild, T. S., Arens, N. C. & Dawson, T. E. The ancestral ecology of angiosperms: Emerging perspectives from extant basal lineages. Int. J. Plant Sci. 164, S129–S142 (2003)

    Article  Google Scholar 

  8. Friedman, W. E. & Williams, J. H. Developmental evolution of the sexual process in ancient flowering plant lineages. Plant Cell 16, S119–S132 (2004)

    Article  CAS  Google Scholar 

  9. 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 

  10. Endress, P. K. Origins of flower morphology. J. Exp. Zool. 291, 105–115 (2001)

    Article  CAS  Google Scholar 

  11. De Craene, L. P. R., Soltis, P. S. & Soltis, D. E. Evolution of floral structures in basal angiosperms. Int. J. Plant Sci. 164, S329–S363 (2003)

    Article  Google Scholar 

  12. Zanis, M. J., Soltis, P. S., Qiu, Y. L., Zimmer, E. & Soltis, D. E. Phylogenetic analyses and perianth evolution in basal angiosperms. Ann. Mo. Bot. Gard. 90, 129–150 (2003)

    Article  Google Scholar 

  13. Stebbins, G. L. Flowering Plants: Evolution Above the Species Level (Harvard Univ. Press, Cambridge, 1974)

    Book  Google Scholar 

  14. Cronquist, A. The Evolution and Classification of Flowering Plants 2nd edn (New York Bot. Gard., Bronx, 1988)

    Google Scholar 

  15. Porsch, O. Versuch einer phylogenetischen erklärung des embryosackes und der doppelten befruchtung der angiospermen (Gustav Fisher, Jena, 1907)

    Google Scholar 

  16. Schnarf, K. Vergleichende embryologie der angiospermen (Borntraeger, Berlin, 1931)

    Google Scholar 

  17. Johri, B. M. in Recent Advances in the Embryology of Angiosperms (ed. Maheshwari, P.) 69–103 (Int. Soc. Plant Morphol., Delhi, 1963)

    Google Scholar 

  18. Davis, G. L. Systematic Embryology of the Angiosperms (John Wiley and Sons, New York, 1966)

    Google Scholar 

  19. Donoghue, M. J. & Scheiner, S. M. in Ecology and Evolution of Plant Reproduction (ed. Wyatt, R.) 356–389 (Chapman & Hall, New York, 1992)

    Google Scholar 

  20. Mathews, S. & Donoghue, M. J. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286, 947–950 (1999)

    Article  CAS  Google Scholar 

  21. Parkinson, C. L., Adams, K. L. & Palmer, J. D. Multigene analyses identify the three earliest lineages of extant flowering plants. Curr. Biol. 9, 1485–1488 (1999)

    Article  CAS  Google Scholar 

  22. Qiu, Y.-L. et al. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404–407 (1999)

    Article  CAS  ADS  Google Scholar 

  23. Soltis, P. S., Soltis, D. E. & Chase, M. W. Angiosperm phylogeny inferred from multiple genes as a research tool for comparative biology. Nature 402, 402–404 (1999)

    Article  CAS  ADS  Google Scholar 

  24. Huang, B.-Q. & Russell, S. D. Female germ unit: Organization, isolation, and function. Int. Rev. Cytol. 140, 233–293 (1992)

    Article  Google Scholar 

  25. Guo, F. L., Huang, B. Q., Han, Y. Z. & Zee, S. Y. Fertilization in maize indeterminate gametophyte1 mutant. Protoplasma 223, 111–120 (2004)

    Article  Google Scholar 

  26. Tobe, H., Jaffre, T. & Raven, P. H. Embryology of Amborella (Amborellaceae): descriptions and polarity of character states. J. Plant Res. 113, 271–280 (2000)

    Article  Google Scholar 

  27. Williams, J. H. & Friedman, W. E. Identification of diploid endosperm in an early angiosperm lineage. Nature 415, 522–526 (2002)

    Article  ADS  Google Scholar 

  28. Friedman, W. E., Gallup, W. N. & Williams, J. H. Female gametophyte development in Kadsura: implications for Schisandraceae, Illiciales, and the early evolution of flowering plants. Int. J. Plant Sci. 164, S293–S305 (2003)

    Article  Google Scholar 

  29. Williams, J. H. & Friedman, W. E. The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. Am. J. Bot. 91, 332–351 (2004)

    Article  Google Scholar 

  30. Gifford, E. M. & Foster, A. S. Morphology and Evolution of Vascular Plants (W.H. Freeman and Co., New York, 1989)

    Google Scholar 

Download references


I thank P. K. Diggle, R. H. Robichaux and L. Hufford for critical comments on the manuscript; K. C. Ryerson for assistance with all aspects of data collection and field work; and A. J. Redford, D. O'Connor, T. J. Lemieux and E. N. Madrid for assistance with various aspects of histology and field work. Field collections of Amborella in New Caledonia were made possible by permission of the Direction des Ressources Naturelles, Province Sud, Nouvelle-Calédonie and facilitated by B. Fogliani. This work was supported by grants from the National Science Foundation. To A.S.F., who read every paper I wrote.

Author information

Authors and Affiliations


Corresponding author

Correspondence to William E. Friedman.

Ethics declarations

Competing interests

Reprints and permissions information is available at The author declares no competing financial interests.

Supplementary information

Supplementary Video 1

This movie shows several rotations of a three-dimensional computer reconstruction of the egg apparatus of the female gametophyte of Amborella. The three synergids cells are outlined in blue, green, and yellow and can be seen to abut the micropylar wall (shaded grey) of the female gametophyte. The egg cell is outlined in pink. When the synergids are removed from the computer image, the pyramidal shape of the egg cell is apparent, as well as the fact that the egg cell does not share a common cell wall with the wall delimiting the female gametophyte. (MOV 1424 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Friedman, W. Embryological evidence for developmental lability during early angiosperm evolution. Nature 441, 337–340 (2006).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing