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

Abstract

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.

Transcription organizes euchromatin similar to an active microemulsion

“…Transcription of these sites preceded the nucleus-wide transcription onset after mitosis (Figure 6 C). Previous work revealed that the miR-430 gene cluster is very highly transcribed in late blastula zebrafish embryos (Heyn et al, 2014). We detected primary miR-430 transcripts at the prominent transcription sites, suggesting a role for miR-430 transcription in their formation (SI Figure 11).…”

“…4 Rate of Pol II escape from promoter-paused state (Stasevich, Hayashi-Takanaka, et al, 2014). 5 Average time of 10 minutes for transcript completion estimated based on a typical length of genes transcribed at late blastula stage of 10 kb (Heyn et al, 2014) and a typical Pol II transcription rate of 1 kb/min (Wada et al, 2009;Jonkers, Kwak and Lis, 2014;Stasevich, Hayashi-Takanaka, et al, 2014). 6 Within the range of typical nuclear retention times of completed transcripts (Bahar Halpern et al, 2015;Battich, Stoeger and Pelkmans, 2015).…”

DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation

“…4D). Recently, it was demonstrated that a small number of genes are transcribed prior to the zebrafish MBT, so we assessed the replication timing of those genes (Heyn et al 2014). The pre-MBT-expressed gene set was significantly earlier replicating than genes overall, consistent with a relationship between their transcription and early replication (Fig.…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…(b) Many of the genes that were differentially regulated had a short predicted protein product (~100 amino acids long, Figure 4a, Supplementary Figure S3). Recent studies in eukaryotes have shown that short genes are transcribed and translated rapidly compared with longer genes, perhaps providing a mechanism for fast response to changes in conditions or during development (Shah et al, 2013;Heyn et al, 2014). Such genes also evolve rapidly and may be important in shaping genomic novelty and evolutionary plasticity (Grishkevich and Yanai, 2014;Heyn et al, 2014).…”

“…Recent studies in eukaryotes have shown that short genes are transcribed and translated rapidly compared with longer genes, perhaps providing a mechanism for fast response to changes in conditions or during development (Shah et al, 2013;Heyn et al, 2014). Such genes also evolve rapidly and may be important in shaping genomic novelty and evolutionary plasticity (Grishkevich and Yanai, 2014;Heyn et al, 2014). Genes encoding for short proteins are common in Prochlorococcus (Figure 4c) yet, for the most part, their roles are still unknown (Zhaxybayeva et al, 2007;Whidden et al, 2014).…”