The Maternal to Zygotic Transition in Animals and Plants

Abstract

Plants and animals have each evolved different reproductive strategies that determine the extent to which the parents, usually the female, exert control over the developing offspring. Fertilization can be external or internal. In the latter case, the fertilized egg can be laid on a nutritive substrate (e.g., insects) or it develops within a protective and nurturing matrix (the placenta of mammals, the egg of birds and reptiles, the seed of seed plants). The MZT marks the end of maternal control and the onset of zygotic control over embryo development. It is characterized by the simultaneous degradation of stored maternal products and zygotic genome activation (Andéol 1994;Schultz 2002;Tadros et al. 2003;Stitzel and Seydoux 2007). In animals, the MZT occurs several cell cycles after fertilization. As a consequence, the first stages of embryonic development essentially rely on maternally deposited products. Despite divergent reproductive strategies and differences in the parental provisioning for offspring development, current evidence indicates that plants and animals share a marked maternal control of early postfertilization development. We review this evidence and our knowledge regarding the mechanisms controlling the onset of the MZT in both animals and plants. We hypothesize that shared biological constraints on early embryo development explain the existence of convergent mechanisms for maintaining maternal predominance. EARLY EMBRYOGENESIS IN ANIMALS AND HIGHER PLANTSEmbryogenesis in flowering plants and animals has in common the union of a male and a female gamete that produces the zygote and the sequential events of cell proliferation, morphogenesis, and organogenesis that follow ( Fig. 1). In animals, a single female gamete, the oocyte, fuses with a motile sperm to produce the zygote. Cell proliferation generates a multicellular morula of 16-32 cells in mammals, a blastula of approximately 30,000 cells in Xenopus, and a syncytial blastoderm of about 6000 nuclei in Drosophila. Cellularization (for the syncytial blastoderm of insects) and asymmetric divisions define the onset of morphogenesis, and cellular migration marks the beginning of gastrulation and organogenesis (Browder et al. 1991).In flowering plants, two pairs of gametes fuse, a process termed double fertilization. The two female gametes, the egg and central cell, are each fertilized by a sperm to produce the embryo and the endosperm, respectively. The endosperm is a protective and nurturing tissue that has a role similar to that of the placenta in eutherian mammals (Harper et al. 1970). The female gametes are produced together with "accessory" cells (the synergids and antipodals) within the female gametophyte (embryo sac), which is enclosed in the ovule that, after fertilization, forms the seed. Ovule and seed development occurs in the gynoecium in the center of the flower. The two sperms are produced by the male gametophyte (pollen), which germinates and grows through tissues of the gyneocium to deliver the sperm cells to the embryo sac. In pla...

Embryo and Endosperm Inherit Distinct Chromatin and Transcriptional States from the Female Gametes in Arabidopsis

“…How far these deposited products might sustain embryo development is unclear. The stage of developmental arrest in these experiments may indicate the stage at which the embryo functionally requires de novo zygotic transcription, a central event of the maternal-to-zygotic transition (Baroux et al, 2008;Tadros and Lipshitz, 2009). The variability of developmental arrest between siblings of the POLII-RNAi lines may denote an unequal amount of inherited maternal products.…”

“…In animals, both toxicological experiments and RNA interference (RNAi) strategies have been used to inhibit POLII activity (Powell-Coffman et al, 1996; reviewed in Baroux et al, 2008;Tadros and Lipshitz, 2009). Because toxicological approaches are not easily applicable to Arabidopsis seeds, we chose to downregulate the Arabidopsis gene encoding the main subunit of POLII gene by RNAi.…”

“…The maternal-to-zygotic transition defines the period when this maternal influence ends, and the development of the embryo requires de novo activities produced by the zygotic genome. It occurs one to several cell division cycles following fertilization and entails the degradation of the maternal transcript population, the turnover of maternally stored proteins, and the initiation of zygotic transcription (zygotic genome activation; reviewed in Schier, 2007;Baroux et al, 2008;Tadros and Lipshitz, 2009). …”

The influence of parental effects on transcriptomic landscape during early development in brook charr (Salvelinus fontinalis, Mitchill)

“…Moreover, Bai et al (2007) suggested that a high abundance of maternal ribosomes is found in the yolk sac and could have an impact on the translation control of the offspring genome. In addition to these yolk sac components, maternally deposited RNAs are known to degrade relatively slowly and consequently, have been found in embryos up to late developmental stages (Mathavan et al, 2005;Baroux et al, 2008). As a result, these maternal RNAs could act as transcription regulators and interact with the zygote's transcripts to regulate the level of expression of some genes.…”

Identification of genes preferentially expressed in wheat egg cells and zygotes

“…The timing of zygotic gene 14 activation (ZGA) in plants is somewhat controversial (Baroux et al 2008;Zhao et al 2011;15 Nodine and Barte2012). Recent data, however, indicate that it follows fertilization very early 16 and the first steps of embryogenesis are mostly under zygotic control in Arabidopsis and 17 tobacco (Nodine and Bartel 2012;Zhao et al 2011).…”