The Earliest Transcribed Zygotic Genes Are Short, Newly Evolved, and Different across Species

• Published in: Cell reports (Cambridge) 2014-01, Vol.6 (2), p.285-292
• Main Authors: Heyn, Patricia, Kircher, Martin, Dahl, Andreas, Kelso, Janet, Tomancak, Pavel, Kalinka, Alex T., Neugebauer, Karla M.
• Format: Article
• Language: English
• Subjects: Animals; Danio rerio; Evolution, Molecular; Gene Expression Regulation, Developmental; Genes, Mitochondrial; RNA, Messenger - genetics; RNA, Messenger - metabolism; Species Specificity; Transcription, Genetic; Zebrafish; Zygote - metabolism
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2013.12.030

The transition from maternal to zygotic control is fundamental to the life cycle of all multicellular organisms. It is widely believed that genomes are transcriptionally inactive from fertilization until zygotic genome activation (ZGA). Thus, the earliest genes expressed probably support the rapid cell divisions that precede morphogenesis and, if so, might be evolutionarily conserved. Here, we identify the earliest zygotic transcripts in the zebrafish, Danio rerio, through metabolic labeling and purification of RNA from staged embryos. Surprisingly, the mitochondrial genome was highly active from the one-cell stage onwards, showing that significant transcriptional activity exists at fertilization. We show that 592 nuclear genes become active when cell cycles are still only 15 min long, confining expression to relatively short genes. Furthermore, these zygotic genes are evolutionarily younger than those expressed at other developmental stages. Comparison of fish, fly, and mouse data revealed different sets of genes expressed at ZGA. This species specificity uncovers an evolutionary plasticity in early embryogenesis that probably confers substantial adaptive potential. [Display omitted] •Metabolic labeling with 4-thio-UTP identifies earliest zygotic transcripts•Mitochondrial transcription is active from fertilization onward•Earliest transcripts are short, enabling transcription during short cell cycles•The set of genes of the first transcribed genes is different among species The development of all metazoans is initially controlled by maternal factors, and transcription of the zygotic genome starts only later. In this study, Tomancak, Neugebauer, and colleagues identify the first zygotic transcripts in zebrafish with a 4-sUTP metabolic labeling approach. Using this data set, they find that the first zygotic transcripts in different species are not shared, whereas the maternally deposited RNAs are highly enriched for shared orthologs. These results highlight the striking flexibility of early development.