Modularity of the Angiosperm Female Gametophyte and Its Bearing on the Early Evolution of Endosperm in Flowering Plants

Abstract

Abstract. The monosporic seven-celled/eight-nucleate Polygonum-type female gametophyte has long served as a focal point for discussion of the origin and subsequent evolution of the angiosperm female gametophyte. In Polygonumtype female gametophytes, two haploid female nuclei are incorporated into the central cell, and fusion of a sperm cell with the binucleate central cell produces a triploid endosperm with a complement of two maternal and one paternal genomes, characteristic of most angiosperms. We document the development of a four-celled/four-nucleate female gametophyte in Nuphar polysepala (Engelm.) and infer its presence in many other ancient lineages of angiosperms. The central cell of the female gametophyte in these taxa contains only one haploid nucleus; thus endosperm is diploid and has a ratio of one maternal to one paternal genome. Based on comparisons among flowering plants, we conclude that the angiosperm female gametophyte is constructed of modular developmental subunits. Each module is characterized by a common developmental pattern: (1) positioning of a single nucleus within a cytoplasmic domain (pole) of the female gametophyte; (2) two free-nuclear mitoses to yield four nuclei within that domain; and (3) partitioning of three uninucleate cells adjacent to the pole such that the fourth nucleus is confined to the central region of the female gametophyte (central cell). Within the basal angiosperm lineages Nymphaeales and Illiciales, female gametophytes are characterized by a single developmental module that produces a four-celled/four-nucleate structure with a haploid uninucleate central cell. A second pattern, typical of Amborella and the overwhelming majority of eumagnoliids, monocots, and eudicots, involves the early establishment of two developmental modules that produce a sevencelled/eight-nucleate female gametophyte with two haploid nuclei in the central cell. Comparative analysis of ontogenetic sequences suggests that the seven-celled female gametophyte (two modules) evolved by duplication and ectopic expression of an ancestral Nuphar-like developmental module within the chalazal domain of the female gametophyte. These analyses indicate that the first angiosperm female gametophytes were composed of a single developmental module, which upon double fertilization yielded a diploid endosperm. Early in angiosperm history this basic module was duplicated, and resulted in a seven-celled/eight-nucleate female gametophyte, which yielded a triploid endosperm with the characteristic 2:1 maternal to paternal genome ratio.

Plant and Animal Reproductive Strategies: Lessons from Offspring Size and Number Tradeoffs

“…The endosperm is a specialized embryonourishing tissue and is one of the products of double fertilization, a unique feature of angiosperm reproduction (Baroux et al, 2002;Friedman and Williams, 2003). As a general trend, the endosperm is larger in primitive angiosperm clades and small or absent in younger clades.…”

Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early‐diverging flowering plants

“…For over a century, the key intermediate steps involved in the transition from an embryo‐nourishing female gametophyte (as in gymnosperms) to the embryo‐nourishing triploid endosperm of most flowering plants have remained obscure. With the recent discovery of diploid endosperms in ancient lineages of angiosperms (Williams and Friedman, 2002, 2004; Friedman and Williams, 2003; Friedman et al, 2003, 2008; Friedman, 2008), one of the transitional states appears to have been revealed: the first flowering plants were likely to have had a diploid endosperm, with a subsequent transition to a triploid endosperm in the common ancestor of monocots, eudicots, and magnoliids (Friedman and Williams, 2004).…”

Occurrence of unique three-celled megagametophyte and single fertilization in an aquatic angiosperm-Dalzellia zeylanica (Podostemaceae-Tristichoideae)

“…During the course of evolution, a transition probably occurred from this simple module of the female gametophyte to that of an eightnucleate, seven-celled female gametophyte (by development of a chalazal quartet) with triploid, biparental endosperm prevalent in 70% (Márton and Dresselhaus 2008) of the extant angiosperms (Friedman and Williams 2003). Nevertheless, it is evident that double fertilization occurred both in the simple module of the ancient angiosperms and in the derived module of extant angiosperms and is considered a ubiquitous, defining and ancestral feature of the angiosperms.…”