Abstract
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.
Highlights
The life cycle of flowering plants alternates between a dominant, diploid, sporophytic generation and a short-lived, haploid, gametophytic generation in specialized reproductive organs
Selected Ecotypes of Arabidopsis Show Natural Variation in Cell Differentiation during Megasporogenesis, Which Is Influenced by Intraspecific Hybridization and Ploidy
Previous reports showed that in most cases of megasporogenesis in Arabidopsis, a single subepidermal cell in the ovule primordium is specified as the megaspore mother cell (MMC) (Vandendries, 1909; Schneitz et al, 1995)
Summary
The life cycle of flowering plants alternates between a dominant, diploid, sporophytic generation and a short-lived, haploid, gametophytic generation in specialized reproductive organs. Integration between environmental signals and developmental programs that control flowering initiates development of the female reproductive lineage within the gynoecium. The MMC subsequently divides by meiosis to produce four haploid cells, one of which is specified as the functional megaspore (FM), the first cell of the female gametophytic phase. The FM develops by three rounds of mitosis into a female gametophyte, containing three antipodal cells, two synergids, the egg, and a binucleated central cell. The egg and the central cell will develop into the embryo and the endosperm, respectively (Reiser and Fischer, 1993; Grossniklaus and Schneitz, 1998; Drews and Koltunow, 2011)
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