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Embryological evidence for developmental lability during early angiosperm evolution

Nature volume 441, pages 337–340 (2006)Cite this article

Abstract

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.

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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.

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Acknowledgements

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.

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  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, 80309, USA

    William E. Friedman

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  1. William E. Friedman
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Correspondence to William E. Friedman.

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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)

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Friedman, W. Embryological evidence for developmental lability during early angiosperm evolution. Nature 441, 337–340 (2006). https://doi.org/10.1038/nature04690

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