Abstract

BackgroundGene and genome duplication play important roles in the evolution of gene function. Compared to individual duplicated genes, gene clusters attract particular attention considering their frequent associations with innovation and adaptation. Here, we report for the first time the expansion of the apolipoprotein D (ApoD) ligand-transporter genes in a cluster manner specific to teleost fishes.ResultsBased on comparative genomic and transcriptomic analyses, protein 3D structure comparison, positive selection detection and breakpoints detection, the single ApoD gene in the ancestor expanded into two clusters following a dynamic evolutionary pattern in teleost fishes. Orthologous genes show conserved expression patterns, whereas lineage-specific duplicated genes show tissue-specific expression patterns and even evolve new gene expression profiles. Positive selection occurred in branches before and after gene duplication, especially for lineage-specific duplicated genes. Cluster analyses based on protein 3D structure comparisons, especially comparisons of the four loops at the opening side, show gene duplication-segregating patterns. Duplicated ApoD genes are predicted to be associated with forkhead transcription factors and MAPK genes. ApoD clusters are located next to the breakpoints of genome rearrangements.ConclusionsHere, we report the expansion of ApoD genes specific to teleost fishes in a cluster manner for the first time. Neofunctionalization and subfunctionalization were observed at both the protein and expression levels after duplication. Evidence from different aspects—i.e., abnormal expression-induced disease in humans, fish-specific expansion, predicted associations with forkhead transcription factors and MAPK genes, specific expression patterns in tissues related to sexual selection and adaptation, duplicated genes under positive selection and their location next to the breakpoints of genome rearrangements—suggests the potentially advantageous roles of ApoD genes in teleost fishes. The cluster expansion of ApoD genes specific to teleost fishes provides thus an ideal evo-devo model for studying gene duplication, cluster maintenance and new gene function emergence.

Highlights

  • Gene and genome duplication play important roles in the evolution of gene function

  • The gene copies emerging from duplication events (including whole genome duplications (WGD)) can undergo different evolutionary fates, and a number of models have been proposed as to what can happen after duplication [2]

  • Different numbers of apolipoprotein D (ApoD) genes are located in two clusters in different teleost fishes, i.e., two copies in cavefish (Astyanax mexicanus; A1 and A2) and in tetraodon (Tetraodon nigroviridis; B2a and A2); three copies in zebrafish (Danio rerio; A1, A2 and B2) and in cod (Gadus morhua; A1, A2 and B2b); four copies in platyfish (Xiphophorus maculatus; A1, A2, B2a and B2b); five copies in Amazon molly (Poecilia formosa; A1, A2, B2a, B2ba1, B2ba2) and in fugu (Takifugu rubripes; A1, A2, B1, B2a, B2b); six copies in medaka (Oryzias latipes; A1, A2m1, A2m2, A2m3, B2a, B2b); and eight copies in stickleback (Gasterosteus aculeatus; A1, A2s1, A2s2, B1, B2a, B2bs1, B2bs2, B2bs3) and in tilapia (Oreochromis niloticus; A1, A2t1, A2t2, A2t3, A2t4, B1, B2a, B2b)

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Summary

Introduction

Gene and genome duplication play important roles in the evolution of gene function. Gene and genome duplication play important roles in evolution by providing new genetic materials [1]. One of the duplicates (2019) 19:9 genes is implicated in trichromatic vision in primates [7]. Functional changes after gene duplication can occur at the protein level [6, 11, 12]. Many examples have provided evidence that duplicated genes acquiring new expression domains are linked to neofunctionalization (e.g., dac, a novel leg segment in arachnids [5]; elnb, bulbus arteriosus in teleost fishes [18]; and fhl2b, egg-spots in cichlid fishes [19])

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