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De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data - PubMed

  • ️Mon Jan 01 2018

De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data

Helle Tessand Baalsrud et al. Mol Biol Evol. 2018.

Abstract

New genes can arise through duplication of a pre-existing gene or de novo from non-coding DNA, providing raw material for evolution of new functions in response to a changing environment. A prime example is the independent evolution of antifreeze glycoprotein genes (afgps) in the Arctic codfishes and Antarctic notothenioids to prevent freezing. However, the highly repetitive nature of these genes complicates studies of their organization. In notothenioids, afgps evolved from an extant gene, yet the evolutionary origin of afgps in codfishes is unknown. Here, we demonstrate that afgps in codfishes have evolved de novo from non-coding DNA 13-18 Ma, coinciding with the cooling of the Northern Hemisphere. Using whole-genome sequence data from several codfishes and notothenioids, we find higher copy number of afgp in species exposed to more severe freezing suggesting a gene dosage effect. Notably, antifreeze function is lost in one lineage of codfishes analogous to the afgp losses in non-Antarctic notothenioids. This indicates that selection can eliminate the antifreeze function when freezing is no longer imminent. In addition, we show that evolution of afgp-assisting antifreeze potentiating protein genes (afpps) in notothenioids coincides with origin and lineage-specific losses of afgp. The origin of afgps in codfishes is one of the first examples of an essential gene born from non-coding DNA in a non-model species. Our study underlines the power of comparative genomics to uncover past molecular signatures of genome evolution, and further highlights the impact of de novo gene origin in response to a changing selection regime.

Keywords: molecular adaptation; orphan genes; teleost fishes.

© The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.

afgps in codfishes. (A) Gene organization of afgps in G. morhua and M. aeglefinus. The afgp genes have been divided up in promoter, 5′UTR, signal peptide, intron, afgp repeat and 3′UTR and colored according to legend. The hatched yellow indicates a truncated 3′UTR. The sequences are labeled with species name, a scaffold (scf) or linkage group (LG) identifier, name of afgps with Ψ signifying a pseudogene, and the length of each gene given as number of amino acids (aa). The organization of a complete, functional afgp gene is shown with triangles indicating cleavage sites of the polyprotein peptide. (B) Presence of afgp in a selection of codfishes in a phylogenetic context, showing copy numbers of different parts of afgps mapped on a time-calibrated species tree modified from (Malmstrøm et al. 2016) with time given in millions of years (Ma). The time period when freezing temperatures appeared in the Northern Hemisphere is shaded in blue (Eastman 1997). Species shown to have functional AFGP and thermal hysteresis are denoted with (+): A. glacilis, B. saida (Praebel 2005), G. chalcogrammus (Tsuda and Miura 2005), and G. morhua (Hew et al. 1981). Species shown not to have functional AFGPs or thermal hysteresis are denoted with (–): M. aeglefinus (Ewart et al. 2000) and P. virens (Denstad et al. 1987). The numbers of putative promoters, ex2, and beginning of ex3 (containing afgp repeat) and 3′UTR are given in the colored boxes. The branches where afgps originated and pseudogenized according to the most parsimonious explanation are indicated in the tree according to the legend along with the first appearance of an afgp 5′UTR sequence.

<sc>Fig</sc>. 2.
Fig. 2.

Phylogeny of afgps and afgp-like sequences in codfishes. Sequences from the genomes of G. morhua, M. aeglefinus, G. chalcogrammus, B. saida, A. glacilis, M. merlangius, P. virens, T. minutus, and G. argenteus are included. The sequences from G. morhua and M. aeglefinus have a scaffold (scf) or linkage group (LG) identifier and sequence annotation (either afgp or afgp-like). Ψ is signifying a pseudogene. The remaining sequences have an assigned letter following the species name (details regarding content and genomic position of each sequence is given in supplementary table S3, Supplementary Material online). The tree topology was constructed with MrBayes. Posterior probabilities are shown for the main branching patterns in addition to bootstrap support for a maximum likelihood topology (using MEGA 7). Putatively functional afgps and afgp-like sequences are highlighted in blue and green, respectively, according to legend.

<sc>Fig</sc>. 3.
Fig. 3.

Synteny of genes flanking afgp and tryps in codfishes and notothenioids. Scaffold (scf), linkage group (LG), or chromosome (chr) is specified under each species, orientation of genes is indicated as arrows, grey triangles denote unidentified ORFs and truncated lines indicate regions containing genes not shown for practical purposes. (A) Synteny of the afgp genomic region in G. morhua (gadMor2) and M. aeglefinus (melAeg) compared with the following teleosts lacking afgps: G. aculeatus, T. nigroviridis, T. rubripes, O. niloticus, X. maculates, and E. lucius. Scf9468 in G. morhua has been placed in a gap in LG06 based on syntenic context and overlap at the afgp locus. (B) Genomic organization of the afgp locus in N. coriiceps. (C) Synteny of the trypsinogen locus in N. coriiceps and G. aculeatus, T. nigroviridis, T. rubripes, O. niloticus, and E. lucius.

<sc>Fig</sc>. 4.
Fig. 4.

ISD for all genes in the G. morhua genome assembly. A histograms of the distribution of mean ISD for all annotated genes in G. morhua with the average mean ISD for afgp is shown. Average mean ISD for all genes in the G. morhua genome assembly was 0.36. ISD was calculated using IUPred for each amino acid position in each annotated gene in G. morhua.

<sc>Fig</sc>. 5.
Fig. 5.

afgp, afpp, tlp, tryps1, and tryps3 in notothenioids. Copy numbers of the different genes mapped on a phylogeny modified from (Colombo et al. 2015) and reprinted with permission. Time is given in millions of years (Ma). Species shown to have functional AFGP and thermal hysteresis are signified by (+): P. antarctica (Wöhrmann 1995), D. mawsoni, G. acuticeps (Cheng et al. 2006), T. newnesi (Fields and Devries 2015), N. coriiceps, C. aceratus (DeVries 1971), Harpagifer spp., A. skottsbergi (Miya et al. 2016) and species shown not to have functional AFGPs or thermal hysteresis are signified by (–): E. maclovinus (Cheng 2003), P. guntheri (Miya et al. 2016). The branches with origin and losses of afgp and afpp, that gives the most parsimonious explanation of the occurrence of the events, are indicated as shown in legend, together with the onset of the Antarctic circumpolar current (ACC) and freezing temperatures in the Antarctic (Eastman 1997). Presence of afpp in D. mawsoni is unknown. Copy numbers in D. mawsoni are taken from Nicodemus-Johnson et al. (2011) and N. coriiceps genome assembly was generated by Shin et al. (2014). H. kerguelensis is inserted in the place of its sister species Harpagifer antarcticus (Derome et al. 2002).

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