Reconstructing the ancestral female gametophyte of angiosperms: Insights from Amborella and other ancient lineages of flowering plants

Abstract

For more than a century, the common ancestor of flowering plants was thought to have had a seven-celled, eight-nucleate Polygonum-type female gametophyte. It is now evident that not one, but in fact three, patterns of female gametophyte development and mature structure characterize the common ancestors of the four most ancient clades of extant angiosperms: Amborella-type, Nuphar/Schisandra-type and Polygonum-type. The Amborella-type female gametophyte is restricted to a single extant species, Amborella trichopoda, and at maturity consists of eight cells and nine nuclei. Development of the Amborella-type gametophyte is essentially identical to the Polygonum-type except that there is an additional and asynchronous cell division at the micropylar pole prior to maturation that produces a third synergid and the egg cell. The Nuphar/Schisandra-type female gametophyte is four-nucleate and four-celled and at maturity contains a typical three-celled egg apparatus and a central cell with a single haploid polar nucleus. This type of gametophyte appears to be universal among extant members of the Nymphaeales (including Hydatellaceae) and Austrobaileyales. Based on explicit reconstruction of character distribution and evolution, the Polygonum-type female gametophyte is certain to be representative of the common ancestors of monocots, eudicots, magnoliids, Ceratophyllaceae, and Chloranthaceae. There are compelling biological reasons to suggest that the four-celled, four-nucleate female gametophyte (as found in Nymphaeales and Austrobaileyales) is ancestral among angiosperms, with transitions to Polygonum-type female gametophytes separately in the Amborellales and in the ancient angiosperm clade that includes all angiosperms except Amborella, Nymphaeales, and Austrobaileyales. Subsequent to the evolution of a seven-celled, eight-nucleate Polygonum-type female gametophyte in the Amborellales, we hypothesize that a peramorphic increase in egg apparatus cell number took place and led to the unique situation in which there are three synergids in Amborella trichopoda.

Ancestral traits and specializations in the flowers of the basal grade of living angiosperms

“…-The embryo sac in Nymphaeales and Austrobaileyales is remarkable in being 4 nucleate and 4 celled, so that the endosperm (which is formed by normal double fertilization) is diploid (Williams & Friedman, 2002, 2004Tobe & al., 2007;Friedman & Ryerson, 2009). Thus this embryo sac has only two rounds of mitotic divisions, and not three as in most other angiosperms.…”

“…Tobe & al. (2000) reported that its embryo sac has three rounds of mitotic divisions, leading to a conventional Polygonum type embryo sac, but later it was found to have a 9 nucleate, 8 celled embryo sac, resulting from an additional division of one cell of the egg apparatus (Friedman, 2006;Friedman & Ryerson, 2009). By contrast, an 8 nucleate and 7 celled embryo sac (thus the normal Polygonum type of most other Mesangiospermae) was found in Chloranthaceae (Edwards, 1920;Yoshida, 1957Yoshida, , 1959Yoshida, , 1960Vijayaraghavan, 1964) and Ceratophyllaceae (De Klercker, 1885;Strasburger, 1902;Jędrychowska & Sroczyńska, 1934;Shamrov, 1983Shamrov, , 1997.…”

Ploidy and the Evolution of Endosperm of Flowering Plants

“…In these conditions, we would expect to find both types of endosperm (1m:1p and 2m:1p, see Figure 6). Consistent with this prediction, some angiosperms [in Nympheaceae, Hydatellaceae, Cabombaceae, Illiciaceae, Schisandraceae, Austrobaileyaceae, and Oenothera (Maheshwari 1963;Friedman 2001a;Williams and Friedman 2002;Friedman and Ryerson 2009)] have a 1m:1p endosperm (DF, no MCD) and others a 2m:1p endosperm (other groups, both DF and MCD evolved).…”

“…More specifically, the idea is that DF and MCD increase the endosperm ploidy level, which enhances its postfertilization metabolic efficiency (increased transcription rate, increased cell size, and resource storage). The problem with this view is that endomitosis would achieve the same effect and is very common at the beginning of gametophyte/endosperm development in both angiosperm and gymnosperm (Friedman 2001a,b): DF and MCD seem unnecessary Figure 2.-Possible scenarios for the evolution of the genetic makeup of the embryo nutritive tissue, modified from Friedman and Ryerson (2009). In the left scenario, there are one 1m:0p / 1m:1p transition and two 1m:1p / 2m:1p transitions and thus three steps.…”

Seed evolution: parental conflicts in a multi-generational household

“…The single quartet module giving rise to the four-celled embryo sac and diploid endosperm of the Nymphaeales and Austrobaileyales is possibly the ancestral condition, present in the first flowering plants. If this hypothesis is correct, a duplication of this module appears to have occurred independently at least twice: once in the Amborella lineage (the most basal of living flowering plants, and which has eight-celled embryo sacs) (28) and also in the common ancestor of monocots, eudicots and magnoliids (26,27). Later, in different groups of flowering plants, further duplications of the basic quartet module gave rise to bisporic embryo sacs (which also originate triploid endosperms), and tetrasporic embryo sacs (which originate triploid, pentaploid, nonaploid or decapentaploid endosperms) (8,29).…”