Atlantic cod (Gadus morhua) is a large, cold-adapted teleost that sustains long-standing commercial fisheries and incipient aquaculture1,2. Here we present the genome sequence of Atlantic cod, showing evidence for complex thermal adaptations in its haemoglobin gene cluster and an unusual immune architecture compared to other sequenced vertebrates. The genome assembly was obtained exclusively by 454 sequencing of shotgun and paired-end libraries, and automated annotation identified 22,154 genes. The major histocompatibility complex (MHC) II is a conserved feature of the adaptive immune system of jawed vertebrates3,4, but we show that Atlantic cod has lost the genes for MHCII, CD4 and Ii that are essential for the function of this pathway. Nevertheless, Atlantic cod is not exceptionally susceptible to disease under natural conditions5. We find a highly expanded number of MHCI genes and a unique composition of its Toll-like receptor (TLR) families. This suggests how the Atlantic cod immune system has evolved compensatory mechanisms within both adaptive and innate immunity in the absence of MHCII. These observations affect fundamental assumptions about the evolution of the adaptive immune system and its components in vertebrates.
Wild and domesticated Atlantic salmon males display large variation for sea age at sexual maturation, which varies between 1–5 years. Previous studies have uncovered a genetic predisposition for variation of age at maturity with moderate heritability, thus suggesting a polygenic or complex nature of this trait. The aim of this study was to identify associated genetic loci, genes and ultimately specific sequence variants conferring sea age at maturity in salmon. We performed a genome wide association study (GWAS) using a pool sequencing approach (20 individuals per river and phenotype) of male salmon returning to rivers as sexually mature either after one sea winter (2009) or three sea winters (2011) in six rivers in Norway. The study revealed one major selective sweep, which covered 76 significant SNPs in which 74 were found in a 370 kb region of chromosome 25. Genotyping other smolt year classes of wild and domesticated salmon confirmed this finding. Genotyping domesticated fish narrowed the haplotype region to four SNPs covering 2386 bp, containing the vgll3 gene, including two missense mutations explaining 33–36% phenotypic variation. A single locus was found to have a highly significant role in governing sea age at maturation in this species. The SNPs identified may be both used as markers to guide breeding for late maturity in salmon aquaculture and in monitoring programs of wild salmon. Interestingly, a SNP in proximity of the VGLL3 gene in humans (Homo sapiens), has previously been linked to age at puberty suggesting a conserved mechanism for timing of puberty in vertebrates.
Tunicate embryos and larvae have small cell numbers and simple anatomical features in comparison with other chordates, including vertebrates. Although they branch near the base of chordate phylogenetic trees, their degree of divergence from the common chordate ancestor remains difficult to evaluate. Here we show that the tunicate Oikopleura dioica has a complement of nine Hox genes in which all central genes are lacking but a full vertebrate-like set of posterior genes is present. In contrast to all bilaterians studied so far, Hox genes are not clustered in the Oikopleura genome. Their expression occurs mostly in the tail, with some tissue preference, and a strong partition of expression domains in the nerve cord, in the notochord and in the muscle. In each tissue of the tail, the anteroposterior order of Hox gene expression evokes spatial collinearity, with several alterations. We propose a relationship between the Hox cluster breakdown, the separation of Hox expression domains, and a transition to a determinative mode of development.
Recent molecular phylogenies support that the non-bilaterian Cnidaria is the sister group to bilaterians (4,5) and are therefore informative to reconstruct the early history of bilaterian homeobox gene complements. Earlier searches for cnidarian homeobox genes have revealed the presence of anterior-like Hox genes as well as Gsx, so that the ProtoHox cluster must have been duplicated prior to the cnidarian-bilaterian split. Earlier reports (6-13) have proposed that posterior Hox genes but not central genes or Hox3 are also present in cnidarians. We used publicly available high coverage genome shotgun sequence to identify the complete set of homeobox genes of two distantly related cnidarians, the freshwater polyp Hydra magnipapillata (Hydrozoa) and the sea anemone Nematostella vectensis (Anthozoa).Nematostella is particularly informative as it is considered to represent the basal group within the Cnidaria (14,15 (Fig. 1b and SOM). Instead, they formed an independent and strongly supported branch. Finally, one of the two divergent genes showed conflicting affinities in network analyses with Cdx and Xlox (Fig. 1b) and is therefore most likely a ParaHox gene. (Fig. 2c), and Gsx was the only ParaHox gene detected.As lineage-specific duplications in the Hox cluster are rare within bilaterians, we wanted to know whether or not those found in Nematostella are limited to the Hox genes. For this we examined potential linkages between all other homeobox genes. Including the nine Hox-like genes mentioned above, we found a total of 139 homeobox genes, a surprisingly high number compared to other invertebrates (Table 1 and SOM). Phylogenetic analyses allowed placing at least 87 of those into 58 known groups of homeobox genes, out of 76 groups known for 5 bilaterians. They also suggested that 42 unclassified genes have arisen through recent amplifications of maximally ten genes. By comparison, Hydra has a considerably smaller number of homeobox genes and gene groups. Since all Hydra homeobox gene groups have representatives in the Nematostella genome, we assume that the homeobox complement has been dramatically reduced in the Hydra lineage (Table 1). Comparisons between the extended homeobox sequences of Nematostella allowed the detection of an additional 13 physical clusters ( Fig. 2b and SOM). Four of these clusters may have a more ancient origin, either because they have been identified in the genomes of bilaterians or because they associate distantly related genes. The other nine clusters are undoubtedly the result of recent tandem duplications. We also did not detect obvious synteny conservation between the environments of well related but unlinked homeobox genes, as might be expected after whole genome duplication (not shown). Hence, the gene duplications observed among the Nematostella Hox genes represent a general phenomenon for the homeobox gene complement.From our data, the most parsimonious scenario for the evolution of Hox/ParaHox clusters is as follows (Fig. 3): two ProtoHox genes (P1/2 and P3) gave rise to the ...
Introgression of farmed salmon escapees into wild stocks is a major threat to the genetic integrity of wild populations. Using germ cell-free fish in aquaculture may mitigate this problem. Our study investigated whether it is possible to produce germ cell-free salmon in F0 by using CRISPR-Cas9 to knock out dnd, a factor required for germ cell survival in vertebrates. To avoid studying mosaic animals, sgRNA targeting alb was simultaneously used as a visual tracer since the phenotype of alb KO is complete loss of pigmentation. Induced mutations for the tracer (alb) and the target (dnd) genes were highly correlated and produced germ cell-less fish lacking pigmentation, underlining the suitability of alb KO to serve as tracer for targeted double allelic mutations in F0 animals in species with prohibitively long generation times. This is also the first report describing dnd knockout in any fish species. Analyzing gene expression and histology of dnd KO fish revealed that sex differentiation of the somatic compartment does not depend on the presence of germ cells. However, the organization of the ovarian somatic compartment seems compromised in mutant fish.
BackgroundThe first Atlantic cod (Gadus morhua) genome assembly published in 2011 was one of the early genome assemblies exclusively based on high-throughput 454 pyrosequencing. Since then, rapid advances in sequencing technologies have led to a multitude of assemblies generated for complex genomes, although many of these are of a fragmented nature with a significant fraction of bases in gaps. The development of long-read sequencing and improved software now enable the generation of more contiguous genome assemblies.ResultsBy combining data from Illumina, 454 and the longer PacBio sequencing technologies, as well as integrating the results of multiple assembly programs, we have created a substantially improved version of the Atlantic cod genome assembly. The sequence contiguity of this assembly is increased fifty-fold and the proportion of gap-bases has been reduced fifteen-fold. Compared to other vertebrates, the assembly contains an unusual high density of tandem repeats (TRs). Indeed, retrospective analyses reveal that gaps in the first genome assembly were largely associated with these TRs. We show that 21% of the TRs across the assembly, 19% in the promoter regions and 12% in the coding sequences are heterozygous in the sequenced individual.ConclusionsThe inclusion of PacBio reads combined with the use of multiple assembly programs drastically improved the Atlantic cod genome assembly by successfully resolving long TRs. The high frequency of heterozygous TRs within or in the vicinity of genes in the genome indicate a considerable standing genomic variation in Atlantic cod populations, which is likely of evolutionary importance.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3448-x) contains supplementary material, which is available to authorized users.
Understanding the biological function behind key proteins is of great concern in Atlantic salmon, both due to a high commercial importance and an interesting life history. Until recently, functional studies in salmonids appeared to be difficult. However, the recent discovery of targeted mutagenesis using the CRISPR/Cas9 (clustered regularly interspaced palindromic repeats/CRISPR-associated) system enables performing functional studies in Atlantic salmon to a great extent. We used the CRISPR/Cas9 system to target two genes involved in pigmentation, tyrosinase (tyr) and solute carrier family 45, member 2 (slc45a2). Embryos were assayed for mutation rates at the 17 somite stage, where 40 and 22% of all injected embryos showed a high degree of mutation induction for slc45a2 and tyr, respectively. At hatching this mutation frequency was also visible for both targeted genes, displaying a graded phenotype ranging from complete lack of pigmentation to partial loss and normal pigmentation. CRISPRslc45a2/Cas9 injected embryos showing a complete lack of pigmentation or just a few spots of pigments also lacked wild type sequences when assaying more than 80 (slc45a2) sequence clones from whole embryos. This indicates that CRISPR/Cas9 can induce double-allelic knockout in the F0 generation. However, types and frequency of indels might affect the phenotype. Therefore, the variation of indels was assayed in the graded pigmentation phenotypes produced by CRISPR/Cas9-slc45a2. The results show a tendency for fewer types of indels formed in juveniles completely lacking pigmentation compared to juveniles displaying partial pigmentation. Another interesting observation was a high degree of the same indel type in different juveniles. This study shows for the first time successful use of the CRISPR/Cas9 technology in a marine cold water species. Targeted double-allelic mutations were obtained and, though the level of mosaicism has to be considered, we demonstrate that F0 fish can be used for functional studies in Atlantic salmon.
BackgroundThe salmon louse, Lepeophtheirus salmonis, is an ectoparasite of salmonids that causes huge economic losses in salmon farming, and has also been causatively linked with declines of wild salmonid populations. Lice control on farms is reliant upon a few groups of pesticides that have all shown time-limited efficiency due to resistance development. However, to date, this example of human-induced evolution is poorly documented at the population level due to the lack of molecular tools. As such, important evolutionary and management questions, linked to the development and dispersal of pesticide resistance in this parasite, remain unanswered. Here, we introduce the first Single Nucleotide Polymorphism (SNP) array for the salmon louse, which includes 6000 markers, and present a population genomic scan using this array on 576 lice from twelve farms distributed across the North Atlantic.ResultsOur results support the hypothesis of a single panmictic population of lice in the Atlantic, and importantly, revealed very strong selective sweeps on linkage groups 1 and 5. These sweeps included candidate genes potentially connected to pesticide resistance. After genotyping a further 576 lice from 12 full sibling families, a genome-wide association analysis established a highly significant association between the major sweep on linkage group 5 and resistance to emamectin benzoate, the most widely used pesticide in salmonid aquaculture for more than a decade.ConclusionsThe analysis of conserved haplotypes across samples from the Atlantic strongly suggests that emamectin benzoate resistance developed at a single source, and rapidly spread across the Atlantic within the period 1999 when the chemical was first introduced, to 2010 when samples for the present study were obtained. These results provide unique insights into the development and spread of pesticide resistance in the marine environment, and identify a small genomic region strongly linked to emamectin benzoate resistance. Finally, these results have highly significant implications for the way pesticide resistance is considered and managed within the aquaculture industry.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-937) contains supplementary material, which is available to authorized users.
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