A High-Quality Assembly of the Nine-Spined Stickleback (Pungitius pungitius) Genome

Srinidhi Varadharajan; Pasi Rastas; Ari Löytynoja; Michael Matschiner; Federico C F Calboli; Baocheng Guo; Alexander J Nederbragt; Kjetill S Jakobsen; Juha Merilä

doi:10.1093/gbe/evz240

A High-Quality Assembly of the Nine-Spined Stickleback (Pungitius pungitius) Genome

Genome Biol Evol. 2019 Nov 1;11(11):3291-3308. doi: 10.1093/gbe/evz240.

Authors

Srinidhi Varadharajan¹, Pasi Rastas², Ari Löytynoja³, Michael Matschiner^{1

4}, Federico C F Calboli^{2

5}, Baocheng Guo^{2

6}, Alexander J Nederbragt^{1

7}, Kjetill S Jakobsen¹, Juha Merilä²

Affiliations

¹ Department of Biology, Centre for Ecological and Evolutionary Synthesis, University of Oslo, Norway.
² Ecological Genetics Research Unit, Research Programme in Organismal and Evolutionary Biology, Faculty of Biological and Environmental Sciences, University of Helsinki, Finland.
³ Institute of Biotechnology, University of Helsinki, Finland.
⁴ Department of Paleontology and Museum, University of Zurich, Switzerland.
⁵ Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, Belgium.
⁶ Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology Chinese Academy of Sciences, Beijing, China.
⁷ Biomedical Informatics Research Group, Department of Informatics, University of Oslo, Norway.

Abstract

The Gasterosteidae fish family hosts several species that are important models for eco-evolutionary, genetic, and genomic research. In particular, a wealth of genetic and genomic data has been generated for the three-spined stickleback (Gasterosteus aculeatus), the "ecology's supermodel," whereas the genomic resources for the nine-spined stickleback (Pungitius pungitius) have remained relatively scarce. Here, we report a high-quality chromosome-level genome assembly of P. pungitius consisting of 5,303 contigs (N50 = 1.2 Mbp) with a total size of 521 Mbp. These contigs were mapped to 21 linkage groups using a high-density linkage map, yielding a final assembly with 98.5% BUSCO completeness. A total of 25,062 protein-coding genes were annotated, and about 23% of the assembly was found to consist of repetitive elements. A comprehensive analysis of repetitive elements uncovered centromere-specific tandem repeats and provided insights into the evolution of retrotransposons. A multigene phylogenetic analysis inferred a divergence time of about 26 million years ago (Ma) between nine- and three-spined sticklebacks, which is far older than the commonly assumed estimate of 13 Ma. Compared with the three-spined stickleback, we identified an additional duplication of several genes in the hemoglobin cluster. Sequencing data from populations adapted to different environments indicated potential copy number variations in hemoglobin genes. Furthermore, genome-wide synteny comparisons between three- and nine-spined sticklebacks identified chromosomal rearrangements underlying the karyotypic differences between the two species. The high-quality chromosome-scale assembly of the nine-spined stickleback genome obtained with long-read sequencing technology provides a crucial resource for comparative and population genomic investigations of stickleback fishes and teleosts.

Keywords: Pungitius pungitius; comparative genomics; genome assembly; stickleback.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
DNA Transposable Elements
Evolution, Molecular
Female
Fish Proteins / genetics
Genome*
Hemoglobins / genetics
Male
Microsatellite Repeats
Molecular Sequence Annotation
Perciformes / classification
Perciformes / genetics*
Phylogeny
Recombination, Genetic

Substances

DNA Transposable Elements
Fish Proteins
Hemoglobins