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Parallels and contrasts between the cnidarian and bilaterian maternal-to-zygotic transition are revealed in Hydractinia embryos

ABSTRACT: Embryogenesis requires coordinated gene regulatory activities early on that establish the trajectory of subsequent development, during a period called the maternal-to-zygotic transition (MZT). The MZT comprises transcriptional activation of the embryonic genome and post-transcriptional regulation of egg-inherited maternal mRNA. Investigation into the MZT in animals has focused almost exclusively on bilaterians, which include all classical models such as flies, worms, sea urchin, and vertebrates, thus limiting our capacity to understand the gene regulatory paradigms uniting the MZT across all animals. Here, we elucidate the MZT of a non-bilaterian, the cnidarian Hydractinia symbiolongicarpus. Using parallel poly(A)-selected and non poly(A)-dependent RNA-seq approaches, we find that the Hydractinia MZT is composed of regulatory activities analogous to many bilaterians, including cytoplasmic readenylation of maternally contributed mRNA, delayed genome activation, and separate phases of maternal mRNA deadenylation and degradation that likely depend on both maternally and zygotically encoded clearance factors, including microRNAs. But we also observe massive upregulation of histone genes and an expanded repertoire of predicted H4K20 methyltransferases, aspects thus far unique to the Hydractinia MZT and potentially underlying a novel mode of early embryonic chromatin regulation. Thus, similar regulatory strategies with taxon-specific elaboration underlie the MZT in both bilaterian and non-bilaterian embryos, providing insight into how an essential developmental transition may have arisen in ancestral animals.

ORGANISM(S): Hydractinia symbiolongicarpus

PROVIDER: GSE232065 | GEO | 2023/05/09

REPOSITORIES: GEO

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Project description:During early stages of embryonic development the genome is transcriptionally inactive and cells are under the control of maternally provided mRNA and proteins. At a key point in development, known as the maternal to zygotic transition (MZT), the genome becomes activated and the maternally provided mRNAs begin to degrade. In the early zebrafish embryo, when under maternal control, cells divide rapidly and synchronously with cell cycles that lack gap phases. At cell cycle ten the introduction of gap phases lengthens the cell cycle and synchronised division is lost. During the MZT, zygotic activation of microRNAs leads to the targeted degradation of a number of maternally provided mRNAs, thus linking genome activation to maternal mRNA degredation.While the MZT has been studied in several different organisms the molecular mechanisms that coordinate genome activity and mRNA degradation remain largely unknown. For example, while the bulk of zygotic transcription occurs at cell cycle ten we do not understand why there is a minor wave of transcription before this time point. Similarly maternal mRNAs degrade at different rates, with only a percentage undergoing microRNA-mediated degredation. The aparant different rates of maternal mRNA degredation may be obscured by zygotic transcription.In order to gain an understanding of the MZT I intend to establish a precise understanding of transcription in the early embryo by using solexa sequencing to perform transcript counting at five different developmental stages that span the MZT. Specifically I intend to use crosses from two different zebrafish strains SAT (Sequenced AB and Tbingen, Zv9) and WIK. This project will allow one to understand the overall transcription profiles of genes in the early embryo, but importantly, the SNPs between the two different strains will determine if transcripts are maternal or zygotic (paternal). As a proof of principle we will first use one lane of sequencing to identify transcripts from a cross of an SAT and a WIK fish. This will allow us to observe SNPs between the two different strains. This will be run over one solexa lane. We will then sequence from five different time points on four different crosses SAT male and WIK female, WIK male and SAT female, WIK male and WIK female and SAT male with SAT female. We will prepare the libraries, which will be sequenced paired-end 54 bp over a total of seven lanes of solexa.. This data is part of a pre-publication release. For information on the proper use of pre-publication data shared by the Wellcome Trust Sanger Institute (including details of any publication moratoria), please see http://www.sanger.ac.uk/datasharing/

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Parallels and contrasts between the cnidarian and bilaterian maternal-to-zygotic transition are revealed in Hydractinia embryos

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