The earliest transcribed zygotic genes are short, newly evolved, and different across species.
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.
Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
Patricia
P
Heyn
Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany; Department of Genome Sciences, University of Washington, 3720 15th Avenue NE, Seattle, WA 98195, USA.
Martin
M
Kircher
Deep Sequencing Group SFB 655, DFG Research Center for Regenerative Therapies (CRTD), Biotechnology Center (Biotec), Technische Universität Dresden, Fetscherstrasse 105, 01307 Dresden, Germany.
Andreas
A
Dahl
Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany.
Janet
J
Kelso
Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany. Electronic address: tomancak@mpi-cbg.de.
Pavel
P
Tomancak
Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
Alex T
AT
Kalinka
Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany. Electronic address: karla.neugebauer@yale.edu.
Karla M
KM
Neugebauer
D000818:Animals; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D050259:Genes, Mitochondrial; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D013045:Species Specificity; D014158:Transcription, Genetic; D015027:Zebrafish; D015053:Zygote / Q000378:metabolism*
D012333:RNA, Messenger