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Cited by 46

The DOI matches its Crossref record; 120 of the 120 references it cites were found in a registry or an index.

Genomic architecture of haddock (Melanogrammus aeglefinus) shows expansions of innate immune genes and short tandem repeats

Tørresen, Ole K., Brieuc, Marine S. O., Solbakken, Monica H., Sørhus, Elin, Nederbragt, Alexander J., Jakobsen, Kjetill S., Meier, Sonnich, Edvardsen, Rolf B., Jentoft, Sissel·2018·BMC Genomics
DOI 10.1186/s12864-018-4616-yPMC PMC5894186

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Abstract

BACKGROUND: Increased availability of genome assemblies for non-model organisms has resulted in invaluable biological and genomic insight into numerous vertebrates, including teleosts. Sequencing of the Atlantic cod (Gadus morhua) genome and the genomes of many of its relatives (Gadiformes) demonstrated a shared loss of the major histocompatibility complex (MHC) II genes 100 million years ago. An improved version of the Atlantic cod genome assembly shows an extreme density of tandem repeats compared to other vertebrate genome assemblies. Highly contiguous assemblies are therefore needed to further investigate the unusual immune system of the Gadiformes, and whether the high density of tandem repeats found in Atlantic cod is a shared trait in this group. RESULTS: Here, we have sequenced and assembled the genome of haddock (Melanogrammus aeglefinus) - a relative of Atlantic cod - using a combination of PacBio and Illumina reads. Comparative analyses reveal that the haddock genome contains an even higher density of tandem repeats outside and within protein coding sequences than Atlantic cod. Further, both species show an elevated number of tandem repeats in genes mainly involved in signal transduction compared to other teleosts. A characterization of the immune gene repertoire demonstrates a substantial expansion of MCHI in Atlantic cod compared to haddock. In contrast, the Toll-like receptors show a similar pattern of gene losses and expansions. For the NOD-like receptors (NLRs), another gene family associated with the innate immune system, we find a large expansion common to all teleosts, with possible lineage-specific expansions in zebrafish, stickleback and the codfishes. CONCLUSIONS: The generation of a highly contiguous genome assembly of haddock revealed that the high density of short tandem repeats as well as expanded immune gene families is not unique to Atlantic cod - but possibly a feature common to all, or most, codfishes. A shared expansion of NLR genes in teleosts suggests that the NLRs have a more substantial role in the innate immunity of teleosts than other vertebrates. Moreover, we find that high copy number genes combined with variable genome assembly qualities may impede complete characterization of these genes, i.e. the number of NLRs in different teleost species might be underestimates.

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Figures

Fig. 1 The historic effective population sizes in cod and haddock. The analysis also includes the time before the two species split, as inferred by PSMC. Haddock is marked in red and cod in blue. Each analysis has been run with 100 bootstrap replicates, shown as pale versions of the main color. The time-span ranges from approximately 20 million to 20,000 years ago
Fig. 1 The historic effective population sizes in cod and haddock. The analysis also includes the time before the two species split, as inferred by PSMC. Haddock is marked in red and cod in blue. Each analysis has been run with 100 bootstrap replicates, shown as pale versions of the main color. The time-span ranges from approximately 20 million to 20,000 years agoCC BY · PubMed Central
Fig. 2 NACHT and FISNA domains content in predicted proteins and genome assemblies for the different species. HMMER hits had to be > 75% of the length of the domain to be reported here. Some species have scaffolds ordered and organized into chromosomes/linkage groups, i.e., placed. For these species the number of domains found in placed scaffolds are also reported. The phylogenetic relationship between the species is based on Malmstrøm et al. [9]. NA: Not applicable
Fig. 2 NACHT and FISNA domains content in predicted proteins and genome assemblies for the different species. HMMER hits had to be > 75% of the length of the domain to be reported here. Some species have scaffolds ordered and organized into chromosomes/linkage groups, i.e., placed. For these species the number of domains found in placed scaffolds are also reported. The phylogenetic relationship between the species is based on Malmstrøm et al. [9]. NA: Not applicableCC BY · PubMed Central
Fig. 3 Relationship between length and coverage of reads for sequences harboring the FISNA domain. Coverage has been normalized for each species by dividing the coverage for each sequence with the average for that species. The average lengths of genes with the FISNA domain is 17 kbp in cod and 14 kbp in haddock, and the increased coverage in sequences about this length might indicate that there are multiple, very similar regions with these genes in the two species. The cod sequences larger than 10 Mbp represent the linkage groups. Cod is plotted with red and haddock in blue. The x-axis is log(10)-transformed since the sequences span from 700 bp to more than 20 Mbp
Fig. 3 Relationship between length and coverage of reads for sequences harboring the FISNA domain. Coverage has been normalized for each species by dividing the coverage for each sequence with the average for that species. The average lengths of genes with the FISNA domain is 17 kbp in cod and 14 kbp in haddock, and the increased coverage in sequences about this length might indicate that there are multiple, very similar regions with these genes in the two species. The cod sequences larger than 10 Mbp represent the linkage groups. Cod is plotted with red and haddock in blue. The x-axis is log(10)-transformed since the sequences span from 700 bp to more than 20 MbpCC BY · PubMed Central
Fig. 4 Cumulative plot of the density (bp/Mbp) and frequency (loci/Mbp) of short tandem repeats (STRs). Shown is the STR content per unit size in the whole assembly and CDS for different teleosts. Most of the STR contents in the whole assembly in cod and haddock are dinucleotide repeats, but there are about equal amounts of dinucleotide and trinucleotide repeats in coding sequence. a Density of STRs in the genome assembly (bp/Mbp). b Density of STRs in protein-coding regions (bp/Mbp). c Frequency of STRs in the genome assembly (loci/Mbp). d Frequency of STRs in the protein-coding regions (loci/Mbp)
Fig. 4 Cumulative plot of the density (bp/Mbp) and frequency (loci/Mbp) of short tandem repeats (STRs). Shown is the STR content per unit size in the whole assembly and CDS for different teleosts. Most of the STR contents in the whole assembly in cod and haddock are dinucleotide repeats, but there are about equal amounts of dinucleotide and trinucleotide repeats in coding sequence. a Density of STRs in the genome assembly (bp/Mbp). b Density of STRs in protein-coding regions (bp/Mbp). c Frequency of STRs in the genome assembly (loci/Mbp). d Frequency of STRs in the protein-coding regions (loci/Mbp)CC BY · PubMed Central
Fig. 5 Pairwise Fisher’s exact test for some gene ontology groups and for some unit sizes. See Additional file 2: Figure S1 for the entire figure with 74 GO groups and unit sizes 1–10 bp, and Additional file 1: Table S4 for the GO groups where haddock and cod differ significantly from the other species. Shown here are GO:0007165 (signal transduction), GO:0007186 (G-protein coupled receptor signaling pathway) and GO:0007264 (small GTPase mediated signal transduction) for tandem repeats in 1–3 bp unit sizes. In the white panels and the white and light blue areas there are no significant differences, but in the dark blue areas there are significant differences between two species. For GO:0007165 and GO:0007186 there is a significant difference (P < 0.05) between cod and haddock and the other species, but not between cod and haddock, nor between cod and cave fish. For GO:0007264, this pattern is less apparent
Fig. 5 Pairwise Fisher’s exact test for some gene ontology groups and for some unit sizes. See Additional file 2: Figure S1 for the entire figure with 74 GO groups and unit sizes 1–10 bp, and Additional file 1: Table S4 for the GO groups where haddock and cod differ significantly from the other species. Shown here are GO:0007165 (signal transduction), GO:0007186 (G-protein coupled receptor signaling pathway) and GO:0007264 (small GTPase mediated signal transduction) for tandem repeats in 1–3 bp unit sizes. In the white panels and the white and light blue areas there are no significant differences, but in the dark blue areas there are significant differences between two species. For GO:0007165 and GO:0007186 there is a significant difference (P < 0.05) between cod and haddock and the other species, but not between cod and haddock, nor between cod and cave fish. For GO:0007264, this pattern is less apparentCC BY · PubMed Central
Fig. 6 An example of gene ontology terms significantly enriched for genes with trinucleotide tandem repeats in different species. Trinucleotide tandem repeats are repeats that can vary in number of repeat units without causing frameshifts in the protein. Only tests with P < 0.01 are colored. Red signifies enrichment, i.e. more trinucleotide repeats than expected, and blue purification, i.e. less than expected, while the P-value is signified with color intensity with more bland color being less significant. White areas have no significant differences. See Additional file 3: Figure S2 for the complete analysis
Fig. 6 An example of gene ontology terms significantly enriched for genes with trinucleotide tandem repeats in different species. Trinucleotide tandem repeats are repeats that can vary in number of repeat units without causing frameshifts in the protein. Only tests with P < 0.01 are colored. Red signifies enrichment, i.e. more trinucleotide repeats than expected, and blue purification, i.e. less than expected, while the P-value is signified with color intensity with more bland color being less significant. White areas have no significant differences. See Additional file 3: Figure S2 for the complete analysisCC BY · PubMed Central

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Authors
Tørresen, O. K., Brieuc, M. S. O., Solbakken, M. H., Sørhus, E., Nederbragt, A. J., Jakobsen, K. S., Meier, S., Edvardsen, R. B., & Jentoft, S.
Venue
BMC Genomics
Publisher
Springer Science and Business Media LLC
Published
2018-04-10
Volume
19
Issue
1
ISSN
1471-2164
DOI
10.1186/s12864-018-4616-y
PMC
PMC5894186
Cited by
46
References
120
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (tdm)
Funders
Norges Forskningsråd (#222378/F20, #234367/E40)

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