In angiosperms, the transition to the female gametophytic phase relies on the specification of premeiotic gamete precursors from sporophytic cells in the ovule. In Arabidopsis thaliana, a single diploid cell is specified as the premeiotic female gamete precursor. Here, we show that ecotypes of Arabidopsis exhibit differences in megasporogenesis leading to phenotypes reminiscent of defects in dominant mutations that epigenetically affect the specification of female gamete precursors. Intraspecific hybridization and polyploidy exacerbate these defects, which segregate quantitatively in F2 populations derived from ecotypic hybrids, suggesting that multiple loci control cell specification at the onset of female meiosis. This variation in cell differentiation is influenced by the activity of ARGONAUTE9 (AGO9) and RNA-DEPENDENT RNA POLYMERASE6 (RDR6), two genes involved in epigenetic silencing that control the specification of female gamete precursors. The pattern of transcriptional regulation and localization of AGO9 varies among ecotypes, and abnormal gamete precursors in ovules defective for RDR6 share identity with ectopic gamete precursors found in selected ecotypes. Our results indicate that differences in the epigenetic control of cell specification lead to natural phenotypic variation during megasporogenesis. We propose that this mechanism could be implicated in the emergence and evolution of the reproductive alternatives that prevail in flowering plants.

Each year, plants and animals perform the task of repopulating the planet through patterns of courtship and mating that have a unifying and compelling logic: the production of offspring. Although life of nearly all organisms is organized around sex and breeding, Darwinian thinking focused more on the struggle for existence than on evolutionary significance of this frantic race to reproduce. In Darwin's own words, "We do not know the final cause of sexuality; why new beings should be produced by the union of the two sexual elements. The whole subject is hidden in darkness. . ." (Darwin 1862). In plants, a major consequence of this search for survival is the evolution of a multitude of reproductive alternatives that have intrigued botanists, geneticists, and evolutionary biologists for more than 100 years. Because sexually derived genetic diversity is interpreted as essential for adaptation, it is often thought that sex is necessary for the perpetuation of a species; however, many organismsincluding several hundred families of flowering plants-are going efficiently about propagating their kind without bothering with meiosis and mating. Whereas many plants can undergo vegetative propagation, through the production of stolons, bulbs, or rhizomes, for example, many others have developed methods to produce an embryo from a single cell whose nucleus is not formed by the fusion of two gametes, offering a direct developmental and evolutionary challenge to sexual reproduction. Recent evidence suggests that epigenetic mechanisms that control transcriptional silencing of DNA repetitive elements and heterochromatin are crucial for the acquisition of cell identity in the ovule, opening the possibility that the developmental distinction between sexual development and apomixis might have evolved as an adaptive response to evolutionary forces that modulate structural variation and reproductive versatility in flowering plants.The emergence of all plants is derived from a common ancestor that endosymbiotically acquired a photosynthetic bacterium capable of transforming light into energy, an evolutionary event that changed the surface of the planet by progressively transforming an environment dominated by cyanobacteria (blue-green bacteria) into a habitat predominantly occupied by photosynthetic multicellular organisms. Although fossilized spores suggest that land plants appeared more than 450 million years ago, the establishment of their life cycle through the alternation of haploid and diploid generations remains an unsolved mystery. In contrast to green algae and mosses, in which the gametophytic (haploid) phase is free-living and temporally dominant, flowering plants have a reduced and ephemeral gametophyte that forms male and female gametes and is necessary to ensure sexual reproduction.Plants have evolved a characteristic life strategy with alternating diploid and haploid phases (or generations), continuous postembryonic development that derives in the formation of aerial and underground meristems, and the absence of a germli...