Evolutionary origins of the endosperm in flowering plants

Abstract

The evolutionary origin of double fertilization and the resultant endosperm tissue in flowering plants remains a puzzle, despite over a century of research. The recent resurgence of approaches to evolutionary developmental biology combining comparative biology with phylogenetics provides new understanding of endosperm origins.

Figure 1

Reconstruction of the evolutionary ontogeny of the endosperm by phylogenetically anchored comparative embryology. A schematic representation of the phylogenetic trees of (a) gymnosperms and (b) angiosperms. Only species relevant for the text or the illustration in (c) are indicated. Trees were drawn according to [15] and [16], respectively. (c) A series of example species illustrating the diversity of embryo sac structures among extant plants and the subsequent diversity of endosperm ploidy. The embryo sac depicted for Amborella and Arabidopsis is of the Polygonum type. The variations in endosperm ploidy for Piperaceae and Plumbaginaceae, the transient presence of endosperm in Orchidaceae and its absence from Podostemonaceae are all only predicted, on the basis of cytological studies [3]. The ploidy number of the endosperm has been precisely measured in some basal angiosperms [1] and is known in Arabidopsis. For comparison to the angiosperm female gametophyte (embryo sac), the female gametophyte of two gymnosperm species is shown with copious cellularized haploid tissue and between one and five archegonia, each harboring one egg cell. In the case of Ephedra, egg cells are binucleate with a normal egg nucleus and a ventral canal nucleus [8]. In gymnosperms a situation of 'simple complex polyembryony' occurs [10] in which several egg cells can be fertilized (by mitotically distinct sperm nuclei), and each zygote then generates four embryo clones. The extent of this polyembryony varies between species, and a simplified form is depicted here. Ultimately, only one embryo will survive while the others degenerate (gray dashed lines in the example of Abies). In the case of Ephedra, both nuclei of the egg cell are fertilized by two sperm nuclei discharged by a single pollen tube (double fertilization) and polyembryony also applies to both fertilization products [2,8]. Embryo sac structures were drawn based on [3], and photographs are courtesy of the Missouri Botanical Garden [17]: Abies balsamea, Ephedra viridis, Amborella trichopoda, Nymphaea odorata, Peperomia argyreia, Orchis mascula, Plumbago europaea and Oenothera macrocarpa. The Polypleurum dichotomum and Arabidopsis thaliana photographs are courtesy of Rolf Rütishauser and John Bowman, respectively.