Abstract
Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that—in vertebrates—over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.
Highlights
Eggs 32 cells Blastula 7 hpf 8 hpf 10 hpf 11 hpf 15 hpf 18 hpf 21 hpf 24 hpf 27 hpf 36 hpf 50 hpf 60 hpf Premet. larvae Hepatic div
The effect of vertebrate whole genome duplication (WGD) on gene regulation have remained poorly understood—both in terms of the fates of duplicate genes and the acquisition of the unique genomic traits that are characteristic of vertebrates
We lack comprehensive functional genomic data from a slow-evolving, closely related outgroup that would enable an in-depth investigation of the origins of the vertebrate regulatory genome and of the effect of WGDs on gene regulation
Summary
The effect of vertebrate WGDs on gene regulation have remained poorly understood—both in terms of the fates of duplicate genes and the acquisition of the unique genomic traits that are characteristic of vertebrates These traits include numerous features that are often associated with gene regulation, such as unusually large intergenic and intronic regions[5,6], high global 5-methylcytosine (5mC) content and 5mC-dependent regulation of embryonic transcriptional enhancers[7]. We lack comprehensive functional genomic data from a slow-evolving, closely related outgroup that would enable an in-depth investigation of the origins of the vertebrate regulatory genome and of the effect of WGDs on gene regulation. Functional genome annotation of amphioxus We generated an exhaustive resource of genomic, epigenomic and transcriptomic data for the Mediterranean amphioxus (B. lanceolatum), comprising a total of 52 sample types (Fig. 1a and Supplementary Data 2, datasets 1–5). A significantly larger global TSS distance in APREs was observed for all vertebrates compared to amphioxus (Fig. 1d), even after correcting for differences in average intergenic
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