Depletion of Maternal Cyclin B3 Contributes to Zygotic Genome Activation in the Ciona Embryo

Treen, Nicholas; Heist, Tyler; Wang, Wei; Levine, Michael

doi:10.1016/j.cub.2018.02.046

Cited by 25 publications

(24 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The delayed detection in our analysis may result from a combination of our stringent cutoffs and the lack of sensitivity in scRNA-seq. These results are in line with a recent study in C. intestinalis (23). Nine genes can be considered overlapping, with zygotic transcription detected in both species despite the different cutoffs.…”

Section: Insights On Differential Gene Regulation In Early Ascidian Esupporting

confidence: 92%

A single-cell analysis of the molecular lineage of chordate embryogenesis

Zhang

Imai

et al. 2020

Sci. Adv.

View full text Add to dashboard Cite

Progressive unfolding of gene expression cascades underlies diverse embryonic lineage development. Here, we report a single-cell RNA sequencing analysis of the complete and invariant embryonic cell lineage of the tunicate Ciona savignyi from fertilization to the onset of gastrulation. We reconstructed a developmental landscape of 47 cell types over eight cell cycles in the wild-type embryo and identified eight fate transformations upon fibroblast growth factor (FGF) inhibition. For most FGF-dependent asymmetric cell divisions, the bipotent mother cell displays the gene signature of the default daughter fate. In convergent differentiation of the two notochord lineages, we identified additional gene pathways parallel to the master regulator T/Brachyury. Last, we showed that the defined Ciona cell types can be matched to E6.5-E8.5 stage mouse cell types and display conserved expression of limited number of transcription factors. This study provides a high-resolution single-cell dataset to understand chordate early embryogenesis and cell lineage differentiation.

show abstract

Section: Insights On Differential Gene Regulation In Early Ascidian Esupporting

confidence: 92%

A single-cell analysis of the molecular lineage of chordate embryogenesis

Zhang

Imai

et al. 2020

Sci. Adv.

View full text Add to dashboard Cite

show abstract

“…We conclude that the early expression patterns of a majority of our ten test genes are well conserved between Ciona and Phallusia, some of the observed differences possibly reflecting limitations of the colorimetric in situ hybridisation protocol we used. Future work based on single-cell RNA seq in ascidians (Horie et al, 2018;Sharma et al, 2018;Treen et al, 2018;Wang et al, 2017) may be required to discriminate technical issues from bona fide evolutionary changes. In the following sections, we used our extensive ATAC-seq dataset to identify the cis-regulatory sequences driving the conserved expression of these genes and to compare their activity in both species.…”

Section: Conservation Of Early Regulatory Gene Expression Between Ciomentioning

confidence: 99%

Evolution of the embryonic cis-regulatory landscapes between divergent Phallusia and Ciona ascidians.

Madgwick

Magri

Dantec

et al. 2018

Preprint

View full text Add to dashboard Cite

Open chromatin regions are highly enriched for cis-regulatory elements in ascidian early embryos.• Ascidian Clusters of Open Regulatory Elements (COREs) are found next to regulatory genes.• The spatio-temporal dynamics of chromatin accessibility and closest-gene expression are correlated.• Regulatory gene expression, the trans-regulatory code, is conserved between distantly-related Ciona and Phallusia ascidians. • Ascidians show pervasive use of "shadow" enhancers • The position of homologous enhancers can be conserved, despite extensive genome divergence. ABSTRACT Ascidian species of the Phallusia and Ciona genera are distantly related, their last common ancestor dating several hundred million years ago. Although their genome sequences have extensively diverged since this radiation, Phallusia and Ciona species share almost identical early morphogenesis and stereotyped cell lineages.Here, we explored the evolution of transcriptional control between P. mammillata and C. robusta. We combined genome-wide mapping of open chromatin regions in both species with a comparative analysis of the regulatory sequences of a test set of 10 pairs of orthologous early regulatory genes with conserved expression patterns. We find that ascidian chromatin accessibility landscapes obey similar rules as in other metazoa. Openchromatin regions are short, highly conserved within each genus and cluster around regulatory genes. The dynamics of chromatin accessibility and closest-gene expression are strongly correlated during early embryogenesis. Open-chromatin regions are highly enriched in cis-regulatory elements: 73% of 49 open chromatin regions around our test genes behaved as either distal enhancers or proximal enhancer/promoters following electroporation in Phallusia eggs.Analysis of this datasets suggests a pervasive use in ascidians of "shadow" enhancers with partially overlapping activities. Cross-species electroporations point to a deep conservation of both the transregulatory logic between these distantly-related ascidians and the cis-regulatory activities of individual enhancers. Finally, we found that the relative order and approximate distance to the transcription start site of open chromatin regions can be conserved between Ciona and Phallusia species despite extensive sequence divergence, a property that can be used to identify orthologous enhancers, whose regulatory activity can partially diverge. of chromatin accessibility landscapes and cis-regulatory logic between these species despite extreme sequence divergence.

show abstract

“…Mitotic divisions do not require cyclin B3 and this is reflected by the fact that cyclin B3 knock-out mice are viable without any apparent phenotype, except female sterility (Bouftas and Wassmann, 2019; Karasu et al ., 2019; Karasu and Keeney, 2019; Li et al ., 2019). There are exceptions in non- vertebrates, for example the ascidian Ciona intestinalis , where cyclin B3 acts as a repressor of zygotic genome activation in embryos and contributes to the timing when the transcription machinery switches from maternal to zygotic mRNAs (Treen et al, 2018). In Drosophila, cyclin B3 was shown to promote anaphase onset during early embryonic mitotic divisions and female meiosis, but is dispensable later in development.…”

Section: Discussionmentioning

confidence: 99%

Cyclin B3 implements timely vertebrate oocyte arrest for fertilization

Bouftas

Schneider

Halder

et al. 2022

Preprint

View full text Add to dashboard Cite

To ensure successful offspring ploidy, vertebrate oocytes must halt the cell cycle in meiosis II until sperm entry. Emi2 is essential to keep oocytes arrested until fertilization. Yet, how this arrest is implemented exclusively in meiosis II and not prematurely in meiosis I remained enigmatic. Using mouse and frog oocytes, we show here that cyclin B3, an understudied B-type cyclin, is essential to keep Emi2 levels low in meiosis I. Direct phosphorylation of Emi2 at an evolutionarily highly conserved site by Cdk1/cyclin B3 targets Emi2 for degradation. In contrast, Cdk1/cyclin B1 is inefficient in Emi2 phosphorylation providing a molecular explanation for the requirement of different B-type cyclins for oocyte maturation. Cyclin B3 degradation at exit from meiosis I enables Emi2 accumulation and thus, timely arrest in meiosis II. Our findings illuminate the evolutionarily conserved mechanisms controlling oocyte arrest for fertilization at the correct cell cycle stage, essential for embryo viability.

show abstract

Depletion of Maternal Cyclin B3 Contributes to Zygotic Genome Activation in the Ciona Embryo

Cited by 25 publications

References 44 publications

A single-cell analysis of the molecular lineage of chordate embryogenesis

A single-cell analysis of the molecular lineage of chordate embryogenesis

Evolution of the embryonic cis-regulatory landscapes between divergent Phallusia and Ciona ascidians.

Cyclin B3 implements timely vertebrate oocyte arrest for fertilization

Contact Info

Product

Resources

About