Dataset Information

Methylation dynamics during the maternal-to-zygotic genome transition in dioecious species.

ABSTRACT: The starting point of a new generation in sexually reproducing species is fertilization. In many species, fertilization is followed by cell divisions controlled primarily by maternal transcripts, with little to no zygotic transcription. The activation of the zygotic genome (ZGA) is part of a process called maternal-to-zygotic transition (MZT), during which transcripts from the zygotic genome take control of development, setting the conditions for cellular specialization. While we know that epigenetic processes (e.g. methylation) are involved in the MZT, their roles and interplay in the transition are largely unknown. I developed a model and used simulations to elucidate the interaction between possible epigenetic processes, namely methylation processes, involved in the MZT. The model focuses on the dynamics of global methylation levels and how these interact with factors such as a parental repressor and the nucleocytoplasmic ratio to trigger the ZGA, followed by development from fertilization to adulthood. In addition, I included transgenerational effects transmitted to the zygote from both parents through their gametes to show that these may set the stage for plastic developmental processes. I demonstrate that the rates of maintenance methylation and demethylation, which are important for the achievement of the final methylation levels of an individual, exhibit a certain level of flexibility in terms of parameter values. I find that high final methylation levels require more restricted combinations of parameter values. The model is discussed in the context of the current empirical knowledge and provide suggestions for directions of future empirical and theoretical studies.

SUBMITTER: Silva WTAF

PROVIDER: S-EPMC6039002 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Publications

Methylation dynamics during the maternal-to-zygotic genome transition in dioecious species.

Silva Willian T A F WTAF

PloS one 20180710 7

The starting point of a new generation in sexually reproducing species is fertilization. In many species, fertilization is followed by cell divisions controlled primarily by maternal transcripts, with little to no zygotic transcription. The activation of the zygotic genome (ZGA) is part of a process called maternal-to-zygotic transition (MZT), during which transcripts from the zygotic genome take control of development, setting the conditions for cellular specialization. While we know that epige ...[more]

PMID: 29990374

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Project description:Microarray analysis of zygotic gene expression in 2-to-3 hour wild-type (wt) and smg mutant embryos. Expression is relative to mature, stage 14 oocytes, which contain the full maternal pool of mRNA. Strictly maternal genes that are not transcribed at the MZT contribute approximately 80% of transcripts in early embryos, and are not shown. Class I zygotic genes showed high levels of expression in 2-to-3 hour embryos. 142 of the 166 Class I genes were not expressed in smg mutants. The remaining zygotically expressed genes were also present in oocytes. These genes were divided into two classes, based on analysis of 4-to-6 hour old unfertilized eggs (4-6h unf), which are transcriptionally inactive. Class-II genes produce maternal transcripts that are stable in unfertilized eggs and show significantly increased expression in 2-to-3 hour post-fertilization embryos. 358 of 395 Class-II genes require SMAUG for zygotic expression. Class-III genes produce maternal transcripts that are degraded in unfertilized eggs and show significantly increased expression in 2-to-3 hour post-fertilization embryos. 65 of 408 Class-III genes require SMAUG for expression in 2-to-3 hour embryos. mRNA was extracted from staged fertilized or unfertilized eggs, as well as stage 14 oocytes as described previously (Tadros et al., 2007a). To assay mRNA quality, known stable (rpA1) and unstable (Hsp83) transcripts were probed on Northern blots. Total RNA was then reverse transcribed with random primers (Tadros et al., 2007a) and labeled asÃ?described in the Indirect Labeling of Total RNA for Microarray Hybridization protocol at http://www.flyarrays.com. The fluorescently labeled cDNA probes were hybridized to 12Kv1 microarrays obtained from the Canadian Drosophila Microarray Centre (http://www.flyarrays.com; GEO platform accession number GPL1467: http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GPL1467). Hybridization and scanning were performed using a PerkinElmer/GSI ScanArray 4000 scanner and the ScanArray software as previously described (Neal et al., 2003). The 16 bit TIFF image files were quantified using QuantArray Version 3 (PerkinElmer), using the adaptive quantification algorithm and analyzed using GeneTraffic Duo3.2 (Iobion Informatics/Stratagene). The 12Kv1 arrays were normalized using the rank invariant LOWESS extrapolation method (Schadt et al., 2001).

Project description:Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robustness is achieved in embryos is limited. While much attention has been paid to the role of gene and signaling networks in promoting robust cell fate determination, little has been done to rigorously assay how mechanical processes like morphogenesis are designed to buffer against variable conditions. Here we show that the cell shape changes that drive morphogenesis can be made robust by mechanisms targeting the actin cytoskeleton. We identified two novel members of the Vinculin/?-Catenin Superfamily that work together to promote robustness during Drosophila cellularization, the dramatic tissue-building event that generates the primary epithelium of the embryo. We find that zygotically-expressed Serendipity-? (Sry-?) and maternally-loaded Spitting Image (Spt) share a redundant, actin-regulating activity during cellularization. Spt alone is sufficient for cellularization at an optimal temperature, but both Spt plus Sry-? are required at high temperature and when actin assembly is compromised by genetic perturbation. Our results offer a clear example of how the maternal and zygotic genomes interact to promote the robustness of early developmental events. Specifically, the Spt and Sry-? collaboration is informative when it comes to genes that show both a maternal and zygotic requirement during a given morphogenetic process. For the cellularization of Drosophilids, Sry-? and its expression profile may represent a genetic adaptive trait with the sole purpose of making this extreme event more reliable. Since all morphogenesis depends on cytoskeletal remodeling, both in embryos and adults, we suggest that robustness-promoting mechanisms aimed at actin could be effective at all life stages.

Dataset Information

Methylation dynamics during the maternal-to-zygotic genome transition in dioecious species.

Publications

Methylation dynamics during the maternal-to-zygotic genome transition in dioecious species.

Similar Datasets

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