nuclear-scale epigenome remodeling. Dynamic patterns of DNA methyltransferase expression, DNA methylation, and in the distribution of histone variants and histone modifications have been described at discrete stages of embryo sac and pollen development

INTRODUCTION In sexually reproducing organisms, gametes are generated by a specific lineage derived from somatic cells that undergo a somaticto-reproductive cell fate transition (SRT). In mammals, the primordial germ cells (PGCs) differentiate in the embryo at gastrulation stage (Bendel-Stenzel et al., 1998). By contrast, the spore mother cells (SMCs) of flowering plants are formed in the adult plant during floral organ differentiation (Maheshwari, 1950). The female SMC, or megaspore mother cell (MMC), differentiates from nucellar cells within the ovule primordium. The male SMC, or microspore mother cell, develops from the sporogeneous tissue within the anthers. Unlike in animals, the plant products of meiosis (spores) do not directly give rise to functional gametes. Instead, they undergo mitosis to form multicellular structures called gametophytes, which, in turn, give rise to the gametes. In most flowering plants, such as in Arabidopsis, the gametophytes are reduced to a small number of cells. The male gametophyte, or pollen, is composed of two sperm cells enclosed within a vegetative cell. The female gametophyte, or embryo sac, is composed of two gametes, termed the egg and central cell, accompanied by accessory cells called antipodals and synergids, the latter of which assist in fertilization. Double fertilization encompasses two fertilization events that produce a totipotent zygote and a nourishing tissue termed the endosperm. Plant gametophyte development establishes several cell types with distinct fates over the course of only two to three divisions. For the female gametophyte, which initiates its polarized development as a syncythium, it has been postulated that epigenetic differentiation of the mitotic daughter nuclei might already take place in nuclei before cellularization (Messing and Grossniklaus, 1999; Grant-Downton and Dickinson, 2006). There is a growing body of evidence that gametophyte development is associated with nuclear-scale epigenome remodeling. Dynamic patterns of DNA methyltransferase expression, DNA methylation, and in the distribution of histone variants and histone modifications have been described at discrete stages of embryo sac and pollen development (Ingouff et al., 2007; Schoft et al., 2009; Ingouff et al., 2010; Pillot et al., 2010; Houben et al., 2011; Ibarra et al., 2012; Jullien et al., 2012). Ultimately, an epigenetic dimorphism is established at the level of DNA methylation, histone modifications and their readers, histone variants and transcriptional competence in mature gametophytes, both between the sperm and vegetative cell in the pollen and between the egg and central cell in the embryo sac. This dimorphism is thought to play important functional roles, including the control of transcriptional activity in the egg and early embryo (Pillot et al., 2010) and of transposable elements in the gametes and early embryo, guided by small RNAs (Slotkin et al., 2009; Calarco and Martienssen, 2011; Ibarra et al., 2012). Another wave of reprogramming occurs after fertilization, with the renewal of the repertoire of histone H3 variants in the zygote and the resetting of DNA methylation patterns during the first divisions of the embryo (Ingouff et al., 2010; Jullien et al., 2012). Thus, two windows of reprogramming have been described during plant reproduction to date: first, during postmeiotic gametophyte development and second, after fertilization during seed development. However, whether reprogramming occurs before meiosis in the SMCs is unknown. In animals, epigenetic reprogramming at the equivalent stage of reproduction, in the PGCs, is crucial for subsequent development. In plants, genetic evidence 1Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, Zollikerstrasse 107, 8008 Zürich, Switzerland. 2Institut de Recherche pour le Développement (UMR 232), Centre National de la Recherche Scientifique (URL 5300), Université de Montpellier II, 911 Avenue Agropolis, 34394 Montpellier, France. 3Laboratory of Plant Molecular Biology, Warsaw University and Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawińskiego 5a, 02-106 Warsaw, Poland.