Evidence of early zygotic genome activation in development of the annelid Ophelia limacina

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Abstract

A key event in early embryonic development is activation of zygotic gene expression. The mechanisms of this process have been well studied in only a few model organisms, which do not fully reflect the diversity of developmental patterns and cell fate determination strategies. Among bilaterian animals, representatives of the Spiralia clade, which exhibit remarkable conservation and determinative specification of cell lineages, remain largely unexplored in terms of genome activation. In this study, we used transcriptomic analysis to investigate zygotic genome activation in the White Sea annelid Ophelia limacina, which exhibits homoquadrant (equal) spiral cleavage. We demonstrate that zygotic transcription begins as early as the 8-cell stage, leading to the upregulation of thousands of genes, including components of the Wnt and TGF-β signaling pathways, as well as transcription factors such as Sox2—a conserved regulator of pluripotency and genome activation in vertebrates. These findings broaden our understanding of the variability of molecular mechanisms underlying zygotic genome activation and raise new questions regarding the potential evolutionary conservation of key factors involved in this process.

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About the authors

M. G. Grinberg

St. Petersburg State University

Email: greenerkk@gmail.com

Department of Embryology

Russian Federation, Universitetskaya nab. 7/9, St. Petersburg, 199034

I. E. Borisenko

St. Petersburg State University

Email: ilja.borisenko@gmail.com

Department of Embryology

Russian Federation, Universitetskaya nab. 7/9, St. Petersburg, 199034

V. V. Kozin

St. Petersburg State University

Author for correspondence.
Email: v.kozin@spbu.ru

Department of Embryology

Russian Federation, Universitetskaya nab. 7/9, St. Petersburg, 199034

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Supplementary files

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2. Fig. 1. Phylogenetic position of annelids studied for zygotic genome activation using transcriptomics methods. The columns indicate: 1) the type of spiral cleavage (the image of the embryo with a single-color fill is homoquadrant cleavage, the image with a two-color fill is heteroquadrant); 2) the developmental stage with the first signs of ZGA and the number of statistically significantly up-regulated genes (transcripts); 3) the stage of embryogenesis at which the greatest number of up-regulated genes was detected (h.p.o. — hours after fertilization).

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3. Fig. 2. Venn diagram showing the number of unique and common transcripts (with expression level > 1 TPM across all replicates) for the unfertilized egg and 8-cell embryo.

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4. Fig. 3. Volcano plot comparing the 8-cell stage with an unfertilized egg. Genes with the lowest p-value and annotation are marked.

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5. Fig. 4. Histograms of enriched GO terms in the “Biological process” category for up-regulated genes (a) and down-regulated genes (b) obtained from differential expression analysis. Terms are sorted by significance level. Color scale corresponds to the number of transcripts related to the term.

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6. Fig. 5. Multidimensional scaling of GO terms in the “Biological process” category for up-regulated genes clustered by semantic similarity. Key GO terms are marked with labels with a dark background. Each circle represents a specific GO term. The same colors indicate the semantically most similar terms. The size of the circle reflects the level of significance.

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7. Fig. 6. Histograms of changes in the expression level of components of the WNT, TGF-b signaling pathways, and transcription factors detected by differential expression analysis. The height of the bars reflects log2(Fold Change), the number above each bar is the p-value. Genes that are not expressed in the egg (0 TPM in all replicates) are marked in bold.

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