Abstract

BackgroundGene duplication has had a major impact on genome evolution. Localized (or tandem) duplication resulting from unequal crossing over and whole genome duplication are believed to be the two dominant mechanisms contributing to vertebrate genome evolution. While much scrutiny has been directed toward discerning patterns indicative of whole-genome duplication events in teleost species, less attention has been paid to the continuous nature of gene duplications and their impact on the size, gene content, functional diversity, and overall architecture of teleost genomes.ResultsHere, using a Markov clustering algorithm directed approach we catalogue and analyze patterns of gene duplication in the four model teleost species with chromosomal coordinates: zebrafish, medaka, stickleback, and Tetraodon. Our analyses based on set size, duplication type, synonymous substitution rate (Ks), and gene ontology emphasize shared and lineage-specific patterns of genome evolution via gene duplication. Most strikingly, our analyses highlight the extraordinary duplication and retention rate of recent duplicates in zebrafish and their likely role in the structural and functional expansion of the zebrafish genome. We find that the zebrafish genome is remarkable in its large number of duplicated genes, small duplicate set size, biased Ks distribution toward minimal mutational divergence, and proportion of tandem and intra-chromosomal duplicates when compared with the other teleost model genomes. The observed gene duplication patterns have played significant roles in shaping the architecture of teleost genomes and appear to have contributed to the recent functional diversification and divergence of important physiological processes in zebrafish.ConclusionsWe have analyzed gene duplication patterns and duplication types among the available teleost genomes and found that a large number of genes were tandemly and intrachromosomally duplicated, suggesting their origin of independent and continuous duplication. This is particularly true for the zebrafish genome. Further analysis of the duplicated gene sets indicated that a significant portion of duplicated genes in the zebrafish genome were of recent, lineage-specific duplication events. Most strikingly, a subset of duplicated genes is enriched among the recently duplicated genes involved in immune or sensory response pathways. Such findings demonstrated the significance of continuous gene duplication as well as that of whole genome duplication in the course of genome evolution.

Highlights

  • Gene duplication has had a major impact on genome evolution

  • Duplicated gene sets among four model teleost species Unigene sets gathered from the Ensembl databases of the four teleost fish were used for self-BLAST followed by Markov clustering dynamic programming utilizing chromosomal coordinates as implemented in the program MCScan [33]

  • Definitions for the duplication types were as follows: 1) tandem duplication: duplicated gene copies located within 10 kb of one another; 2) Intrachromosomal duplication (Non-tandem): duplicated gene copies located on the same chromosome with a distance of greater than 10 kb between all members; and 3) Inter-chromosomal duplication (Non-tandem): duplicated gene copies located on different chromosomes

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Summary

Introduction

Gene duplication has had a major impact on genome evolution. Localized (or tandem) duplication resulting from unequal crossing over and whole genome duplication are believed to be the two dominant mechanisms contributing to vertebrate genome evolution. Sequencing analysis of Hox gene clusters from a spectrum of vertebrate species provided critical evidence in support of Ohno’s hypothesis [5,6,7,8] and indicated, in turn, an additional round of fish-specific genome duplication (FSGD) prior to the divergence of most teleost species [9,10,11,12,13]. Additional evidence supporting FSGD has been garnered from studies of pufferfish, Takifugu rubripes and Tetraodon nigroviridis In these studies, hundreds of genes and gene clusters are present in duplicate in teleost fish but possessing only single copy in other vertebrates, illustrating fish-specific duplication of syntenic regions between humans and fish [14,15,16]. Ongoing examination of gene families across vertebrate evolution continues to provide general support for the three rounds of genome duplication (3R) hypothesis [17,18,19,20,21,22] in teleost fish

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