The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution

Jeramiah J Smith,Malcolm Cook ,Dorit Hockman,Courtney K M Waterbury,Tatjana Sauka‐Spengler ,Melissa C Keinath,Cody Saraceno,Nataliya Timoshevskaya,Jon E Hess,Shawn R Narum,Hugo J Parker,Evan E Eichler,Robb Krumlauf,Leanne M Wiedemann,Carson Holt,Henrik Kaessmann,Greg Elgar,Mark Yandell,Carl Baker,Vladimir A Timoshevskiy,Francesco Lamanna,Sofia Robb ,Chengxi Ye,Chris T Amemiya

doi:10.1038/s41588-017-0036-1

Abstract

The sea lamprey (Petromyzon marinus) serves as a comparative model for reconstructing vertebrate evolution. To enable more informed analyses, we developed a new assembly of the lamprey germline genome that integrates several complementary data sets. Analysis of this highly contiguous (chromosome-scale) assembly shows that both chromosomal and whole-genome duplications have played significant roles in the evolution of ancestral vertebrate and lamprey genomes, including chromosomes that carry the six lamprey HOX clusters. The assembly also contains several hundred genes that are reproducibly eliminated from somatic cells during early development in lamprey. Comparative analyses show that gnathostome (mouse) homologs of these genes are frequently marked by polycomb repressive complexes (PRCs) in embryonic stem cells, suggesting overlaps in the regulatory logic of somatic DNA elimination and bivalent states that are regulated by early embryonic PRCs. This new assembly will enhance diverse studies that are informed by lampreys’ unique biology and evolutionary/comparative perspective.

Highlights

PGR results in the physical elimination of ~0.5 Gb of DNA from the organism’s ~2.3-Gb genome[8–10]
Several shotgun-sequencing and scaffolding data sets were generated in order to permit assembly of the sea lamprey germline genome (> 100×sequence coverage in Illumina paired-end reads, >300×physical coverage in 4-kb Illumina mate pairs and >600×physical coverage in 40-kb Illumina mate pairs)
Previous analyses demonstrated that the lamprey genome is highly repetitive, and initial analysis of Illumina shotgun sequence data confirmed that the repeat content of lamprey (~60% high-identity repeats) is substantially higher than that of human (Fig. 1)

Summary

Introduction

PGR results in the physical elimination of ~0.5 Gb of DNA from the organism’s ~2.3-Gb genome[8–10]. In contrast to the germline genome, the somatically retained portions of the genome are relatively well characterized Because it was not known until 2009 that lampreys were subject to PGR8, sequencing efforts focused on somatic tissues from which DNA or intact nuclei could be readily obtained (e.g., blood and liver)[13]. Because of the abundance of highly identical interspersed repetitive elements and moderately high levels of polymorphism (approaching 1%), assembly of the somatic genome resulted in a consensus sequence that was substantially more fragmentary than other Sanger-based vertebrate assemblies[14]. This initial assembly yielded significant improvements in our understanding of the evolution of vertebrate genomes and fundamental aspects of vertebrate neurobiology, immunity and development[1–7]. Analysis of the resulting assembly identifies several hundred genes that are eliminated from somatic tissues by PGR and sheds new light on the evolution of genes and functional elements in the wake of ancient large-scale duplication events

Methods

Results

Conclusion