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

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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 datasets. Analysis of this highly contiguous (chromosome-scale) assembly reveals 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 repressive/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.

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Most cited references 42

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The zebrafish reference genome sequence and its relationship to the human genome.

Kerstin Howe, Matthew D. Clark, Carlos F Torroja … (2013)

Zebrafish have become a popular organism for the study of vertebrate gene function. The virtually transparent embryos of this species, and the ability to accelerate genetic studies by gene knockdown or overexpression, have led to the widespread use of zebrafish in the detailed investigation of vertebrate gene function and increasingly, the study of human genetic disease. However, for effective modelling of human genetic disease it is important to understand the extent to which zebrafish genes and gene structures are related to orthologous human genes. To examine this, we generated a high-quality sequence assembly of the zebrafish genome, made up of an overlapping set of completely sequenced large-insert clones that were ordered and oriented using a high-resolution high-density meiotic map. Detailed automatic and manual annotation provides evidence of more than 26,000 protein-coding genes, the largest gene set of any vertebrate so far sequenced. Comparison to the human reference genome shows that approximately 70% of human genes have at least one obvious zebrafish orthologue. In addition, the high quality of this genome assembly provides a clearer understanding of key genomic features such as a unique repeat content, a scarcity of pseudogenes, an enrichment of zebrafish-specific genes on chromosome 4 and chromosomal regions that influence sex determination.

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Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.

N. H. Putnam, M Srivastava, U Hellsten … (2007)

Sea anemones are seemingly primitive animals that, along with corals, jellyfish, and hydras, constitute the oldest eumetazoan phylum, the Cnidaria. Here, we report a comparative analysis of the draft genome of an emerging cnidarian model, the starlet sea anemone Nematostella vectensis. The sea anemone genome is complex, with a gene repertoire, exon-intron structure, and large-scale gene linkage more similar to vertebrates than to flies or nematodes, implying that the genome of the eumetazoan ancestor was similarly complex. Nearly one-fifth of the inferred genes of the ancestor are eumetazoan novelties, which are enriched for animal functions like cell signaling, adhesion, and synaptic transmission. Analysis of diverse pathways suggests that these gene "inventions" along the lineage leading to animals were likely already well integrated with preexisting eukaryotic genes in the eumetazoan progenitor.

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The amphioxus genome and the evolution of the chordate karyotype.

Nicholas Putnam, Thomas Butts, David Ferrier … (2008)

Lancelets ('amphioxus') are the modern survivors of an ancient chordate lineage, with a fossil record dating back to the Cambrian period. Here we describe the structure and gene content of the highly polymorphic approximately 520-megabase genome of the Florida lancelet Branchiostoma floridae, and analyse it in the context of chordate evolution. Whole-genome comparisons illuminate the murky relationships among the three chordate groups (tunicates, lancelets and vertebrates), and allow not only reconstruction of the gene complement of the last common chordate ancestor but also partial reconstruction of its genomic organization, as well as a description of two genome-wide duplications and subsequent reorganizations in the vertebrate lineage. These genome-scale events shaped the vertebrate genome and provided additional genetic variation for exploitation during vertebrate evolution.

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Journal

Journal ID (nlm-journal-id): 9216904

Journal ID (pubmed-jr-id): 2419

Journal ID (nlm-ta): Nat Genet

Journal ID (iso-abbrev): Nat. Genet.

Title: Nature genetics

ISSN (Print): 1061-4036

ISSN (Electronic): 1546-1718

Publication date Nihms-submitted: 16 December 2017

Publication date (Electronic): 22 January 2018

Publication date (Print): February 2018

Publication date PMC-release: 22 July 2018

Volume: 50

Issue: 2

Pages: 270-277

Affiliations

[1 ]Department of Biology, University of Kentucky, Lexington, KY, USA

[2 ]Department of Computer Science, University of Maryland, College Park, MD, USA

[3 ]Department of Human Genetics, University of Utah, Salt Lake City, UT, USA

[4 ]Stowers Institute for Medical Research, Kansas City, MO, USA

[5 ]Department of Anatomy & Cell Biology, The University of Kansas School of Medicine, Kansas City, KS, USA

[6 ]Columbia River Inter-Tribal Fish Commission, Portland, OR, USA

[7 ]Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany

[8 ]Department of Pathology and Laboratory Medicine, University of Kansas School of Medicine, Kansas City, KS, USA

[9 ]Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA 98195, USA

[10 ]Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195, USA

[11 ]Radcliffe Department of Medicine, University of Oxford, Oxford, England

[13 ]The Francis Crick Institute, London, England

[14 ]Benaroya Research Institute, Seattle, WA, USA

Author notes

[* ]Corresponding Author: jjsmit3@ 123456uky.edu

[12]

Present Address: Division of Cell Biology, Department of Anatomy, Faculty of Health Sciences, University of Cape Town, Cape Town, RSA.

[15]

Present Address: School of Natural Sciences, University of California Merced, Merced, CA, USA.

[†]

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Article

Manuscript ID: NIHMS928434

DOI: 10.1038/s41588-017-0036-1

PMC ID: 5805609

PubMed ID: 29358652

SO-VID: caa69d1c-ed35-4241-91b9-a7ee1ada076b

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

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Genome Integrity

Most cited references 42

The zebrafish reference genome sequence and its relationship to the human genome.

Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.

The amphioxus genome and the evolution of the chordate karyotype.

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