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

Baalsrud, Helle Tessand, Tørresen, Ole Kristian, Solbakken, Monica Hongrø, Salzburger, Walter, Hanel, Reinhold, Jakobsen, Kjetill S, Jentoft, Sissel·2018·Molecular Biology and Evolution
DOI 10.1093/molbev/msx311PMC PMC5850335
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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.
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.CC BY-NC · PubMed Central
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.
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.CC BY-NC · PubMed Central
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.
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.CC BY-NC · PubMed Central
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.
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.CC BY-NC · PubMed Central
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).
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).CC BY-NC · PubMed Central

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Authors
Baalsrud, H. T., Tørresen, O. K., Solbakken, M. H., Salzburger, W., Hanel, R., Jakobsen, K. S., & Jentoft, S.
Affiliations
  • Department of Biosciences, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway
  • Institute of Fisheries Ecology, Johann Heinrich von Thünen Institute, Federal Research Institute for Rural Areas, Forestry and Fisheries, Hamburg, Germany
ORCID
Solbakken, Monica Hongrø
Venue
Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2017-12-05
Volume
35
Issue
3
Pages
593-606
ISSN
  • 0737-4038
  • 1537-1719
DOI
10.1093/molbev/msx311
PMC
PMC5850335
Cited by
116
References
3
Language
en

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