Zelda and the maternal‐to‐zygotic transition in cockroaches

Ventós-Alfonso, Alba; Ylla, Guillem; Bellés, Xavier

doi:10.1111/febs.14856

Cited by 9 publications

(3 citation statements)

References 49 publications

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“…These levels subsequently decrease and remain low throughout embryogenesis. The pattern suggests that most of the E93 transcripts detected in early embryo are from maternal origin, given that the maternal to zygotic transition (MZT) takes place between ED0 and ED2 in B. germanica ( 14 , 15 ). To study the role of embryonic E93, we used maternal RNA interference (RNAi) by injecting 3 µg double-stranded RNA (dsRNA) targeting the messenger RNA (mRNA) of E93 (dsE93) into 5-d-old females (AdD5).…”

Section: Resultsmentioning

confidence: 99%

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Fernández-Nicolas

Machaj

Ventós-Alfonso

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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The early embryo of the cockroach Blattella germanica exhibits high E93 expression. In general, E93 triggers adult morphogenesis during postembryonic development. Here we show that E93 is also crucial in early embryogenesis in the cockroach, as a significant number of E93-depleted embryos are unable to develop the germ band under maternal RNAi treatment targeting E93 . Moreover, transcriptomic analysis indicates that E93 depletion results in important gene expression changes in the early embryo, and many of the differentially expressed genes are involved in development. Then, using public databases, we gathered E93 expression data in embryo and preadult stages, finding that embryonic expression of E93 is high in hemimetabolan species (whose juveniles, or nymphs, are similar to the adult) and low in holometabolans (whose juveniles, or larvae, are different from the adult). E93 expression is also low in Thysanoptera and in Hemiptera Sternorrhyncha, hemimetabolans with postembryonic quiescent stages, as well as in Odonata, the nymph of which is very different from the adult. In ametabolans, such as the Zygentoma Thermobia domestica , E93 transcript levels are very high in the early embryo, whereas during postembryonic development they are medium and relatively constant. We propose the hypothesis that during evolution, a reduction of E93 expression in the embryo of hemimetabolans facilitated the larval development and the emergence of holometaboly. Independent decreases of E93 transcripts in the embryo of Odonata, Thysanoptera, and different groups of Hemiptera Sternorrhyncha would have allowed the development of modified juvenile stages adapted to specific ecophysiological conditions.

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Section: Resultsmentioning

confidence: 99%

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Fernández-Nicolas

Machaj

Ventós-Alfonso

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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“…Regulation of these important tasks is controlled by mRNAs and proteins, and perhaps unsurprisingly then, mRNA levels in Drosophila are found to be precisely controlled during early embryogenesis [1,2]. This precise control of transcript levels is especially remarkable, however, given that the transcripts at early stages of development come from two different genomes, that of the mother and that of the zygote [3][4][5]. The regulatory mechanisms responsible for this precise control of transcript levels across both genomes are not yet fully understood.…”

Section: Introductionmentioning

confidence: 99%

The conserved regulatory basis of mRNA contributions to the early Drosophila embryo differs between the maternal and zygotic genomes

Omura

Lott

2020

PLoS Genet

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The gene products that drive early development are critical for setting up developmental trajectories in all animals. The earliest stages of development are fueled by maternally provided mRNAs until the zygote can take over transcription of its own genome. In early development, both maternally deposited and zygotically transcribed gene products have been well characterized in model systems. Previously, we demonstrated that across the genus Drosophila, maternal and zygotic mRNAs are largely conserved but also showed a surprising amount of change across species, with more differences evolving at the zygotic stage than the maternal stage. In this study, we use comparative methods to elucidate the regulatory mechanisms underlying maternal deposition and zygotic transcription across species. Through motif analysis, we discovered considerable conservation of regulatory mechanisms associated with maternal transcription, as compared to zygotic transcription. We also found that the regulatory mechanisms active in the maternal and zygotic genomes are quite different. For maternally deposited genes, we uncovered many signals that are consistent with transcriptional regulation at the level of chromatin state through factors enriched in the ovary, rather than precisely controlled gene-specific factors. For genes expressed only by the zygotic genome, we found evidence for previously identified regulators such as Zelda and GAGA-factor, with multiple analyses pointing toward gene-specific regulation. The observed mechanisms of regulation are consistent with what is known about regulation in these two genomes: during oogenesis, the maternal genome is optimized to quickly produce a large volume of transcripts to provide to the oocyte; after zygotic genome activation, mechanisms are employed to activate transcription of specific genes in a spatiotemporally precise manner. Thus the genetic architecture of the maternal and zygotic genomes, and the specific requirements for the transcripts present at each stage of embryogenesis, determine the regulatory mechanisms responsible for transcripts present at these stages.

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“…In the cockroach, Blatella germanica, Dnmt1 RNAi results in embryonic lethality visible both before and after gastrulation 19 . The effects of disrupting the MZT are less well understood in hemimetabolous insects, but strong B. germanica zelda (BgZelda) RNAi knockdown leads to early embryonic lethality similar to that of B. germanica Dnmt1 (BgDnmt1) 57 .…”

Section: Discussionmentioning

confidence: 99%

Dnmt1a is essential for gene body methylation and the regulation of zygotic genome activation in the wasp

Arsala

et al. 2021

Preprint

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Gene body methylation (GBM) is an ancestral form of DNA methylation whose role in development has remained unclear. Unlike vertebrates, DNA methylation is found exclusively in gene bodies in the wasp Nasonia vitripennis, which provides a unique opportunity to interpret the role of GBM in development. We confirmed that parental RNAi (pRNAi) knockdown of DNMT1 (Nv-Dnmt1a) in Nasonia leads to embryonic lethality and failures in cellularization and morphogenesis. Using whole-genome bisulfite sequencing, we found a widespread loss of GBM in Nv-Dnmt1a pRNAi embryos. Using RNAseq, we found that methylated genes that lost GBM in the pRNAi samples were exclusively downregulated during zygotic genome activation. Unexpectedly, nearly all affected unmethylated genes were up-regulated after pRNAi. Lack of proper clearance of mRNAs and abnormal activation drive this up-regulation, indicating critical roles for Nv-Dnmt1a and GBM in the maternal-zygotic transition (MZT) in the wasp, despite their absence in Drosophila.

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Zelda and the maternal‐to‐zygotic transition in cockroaches

Cited by 9 publications

References 49 publications

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

The conserved regulatory basis of mRNA contributions to the early Drosophila embryo differs between the maternal and zygotic genomes

Dnmt1a is essential for gene body methylation and the regulation of zygotic genome activation in the wasp

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