Limits...
The genome of the largest bony fish, ocean sunfish ( Mola mola ), provides insights into its fast growth rate

View Article: PubMed Central - PubMed

ABSTRACT

Background: The ocean sunfish (Mola mola), which can grow up to a length of 2.7 m and weigh 2.3 tons, is the world’s largest bony fish. It has an extremely fast growth rate and its endoskeleton is mainly composed of cartilage. Another unique feature of the sunfish is its lack of a caudal fin, which is replaced by a broad and stiff lobe that results in the characteristic truncated appearance of the fish.

Results: To gain insights into the genomic basis of these phenotypic traits, we sequenced the sunfish genome and performed a comparative analysis with other teleost genomes. Several sunfish genes involved in the growth hormone and insulin-like growth factor 1 (GH/IGF1) axis signalling pathway were found to be under positive selection or accelerated evolution, which might explain its fast growth rate and large body size. A number of genes associated with the extracellular matrix, some of which are involved in the regulation of bone and cartilage development, have also undergone positive selection or accelerated evolution. A comparison of the sunfish genome with that of the pufferfish (fugu), which has a caudal fin, revealed that the sunfish contains more homeobox (Hox) genes although both genomes contain seven Hox clusters. Thus, caudal fin loss in sunfish is not associated with the loss of a specific Hox gene.

Conclusions: Our analyses provide insights into the molecular basis of the fast growth rate and large size of the ocean sunfish. The high-quality genome assembly generated in this study should facilitate further studies of this ‘natural mutant’.

Electronic supplementary material: The online version of this article (doi:10.1186/s13742-016-0144-3) contains supplementary material, which is available to authorized users.

No MeSH data available.


Scpp genes in the ocean sunfish. Upper panel: Comparison of the sunfish sparcl1 locus with those of zebrafish and fugu showing the missing Scpp genes in sunfish (fa93e10, scpp7 and scpp4). The scpp4 pseudogene in the ocean sunfish is shown as a dotted arrow. Lower panel: Alignment of sunfish, fugu and medaka scpp4 sequences showing the single base insertion in exon 2 of this gene in sunfish resulting in a premature termination codon followed by a frameshift in the rest of the open reading frame. This insertion was confirmed by PCR and sequencing of genomic DNA from two other specimens (GenBank accession numbers KF737069 and KF737070). The termination codon in sunfish is underlined in red. The accession numbers for fugu and medaka scpp4 genes used in the alignment are DQ066525.1 and XM_004065875.2, respectively. chr, chromosome; scaf, scaffold
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC5016917&req=5

Fig4: Scpp genes in the ocean sunfish. Upper panel: Comparison of the sunfish sparcl1 locus with those of zebrafish and fugu showing the missing Scpp genes in sunfish (fa93e10, scpp7 and scpp4). The scpp4 pseudogene in the ocean sunfish is shown as a dotted arrow. Lower panel: Alignment of sunfish, fugu and medaka scpp4 sequences showing the single base insertion in exon 2 of this gene in sunfish resulting in a premature termination codon followed by a frameshift in the rest of the open reading frame. This insertion was confirmed by PCR and sequencing of genomic DNA from two other specimens (GenBank accession numbers KF737069 and KF737070). The termination codon in sunfish is underlined in red. The accession numbers for fugu and medaka scpp4 genes used in the alignment are DQ066525.1 and XM_004065875.2, respectively. chr, chromosome; scaf, scaffold

Mentions: We searched for SCPP genes in the sunfish genome to understand the genetic basis of the cartilaginous skeleton of the sunfish. We filled a sequencing gap in this intergenic region by sequencing a genomic PCR product to obtain the complete sequence for spp1. The orthology of the P/Q-rich SCPP genes in sunfish was verified by generating a Maximum Likelihood phylogenetic tree using sequences from sunfish, fugu, medaka and zebrafish (see Additional file 1: Figure S3). Sunfish contains two acidic SCPP genes (spp1 and scpp1) similar to fugu and zebrafish. However, it has lost two P/Q-rich SCPP genes (fa93e10 and scpp7) that are conserved in the other two teleosts (Fig. 4 and Additional file 4). This conclusion was reached after searching the genomic vicinity of the sunfish Sparcl1, the entire genome assembly and the raw reads of the sunfish genome using zebrafish fa93e10 and scpp7 protein sequences by TBLASTN. fa93e10 was first identified as an expressed sequence tag (EST) clone as part of a screen for genes that are expressed in regenerating zebrafish caudal fins [37]. Whole-mount in situ hybridization experiments in zebrafish suggested that fa93e10 is a growth marker that identifies cycles of growth in fin ray segments [37]. Its frequency of expression in fin rays decreases with the age of the fish in tandem with decreased distal mesenchymal cell proliferation [37, 38]. It is not clear whether the absence of fa93e10 in sunfish is somehow related to its unusual fin morphology. In addition to the complete loss of fa93e10 and scpp7, another P/Q-rich SCPP gene, scpp4, that is intact in fugu and medaka has become a pseudogene in the sunfish due to a single nucleotide insertion. This insertion was confirmed by PCR and sequencing of genomic DNA from two other unrelated specimens of sunfish (GenBank accession numbers KF737069 and KF737070), providing further evidence that scpp4 became nonfunctional in the sunfish lineage after it split from the pufferfish lineage (Fig. 4 and Additional files 1 and 4). However, the functional consequence of the loss of this gene in sunfish is not known. Zebrafish does not contain an orthologue of scpp4 but instead contains several other lineage-specific P/Q-rich SCPP genes (Fig. 4 and Additional file 4). Thus, the genetic basis of the cartilaginous skeleton in the sunfish remains unclear. It is possible that this distinctive phenotype is driven by a regulatory change and is therefore not evident in the bone gene repertoire.Fig. 4


The genome of the largest bony fish, ocean sunfish ( Mola mola ), provides insights into its fast growth rate
Scpp genes in the ocean sunfish. Upper panel: Comparison of the sunfish sparcl1 locus with those of zebrafish and fugu showing the missing Scpp genes in sunfish (fa93e10, scpp7 and scpp4). The scpp4 pseudogene in the ocean sunfish is shown as a dotted arrow. Lower panel: Alignment of sunfish, fugu and medaka scpp4 sequences showing the single base insertion in exon 2 of this gene in sunfish resulting in a premature termination codon followed by a frameshift in the rest of the open reading frame. This insertion was confirmed by PCR and sequencing of genomic DNA from two other specimens (GenBank accession numbers KF737069 and KF737070). The termination codon in sunfish is underlined in red. The accession numbers for fugu and medaka scpp4 genes used in the alignment are DQ066525.1 and XM_004065875.2, respectively. chr, chromosome; scaf, scaffold
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5016917&req=5

Fig4: Scpp genes in the ocean sunfish. Upper panel: Comparison of the sunfish sparcl1 locus with those of zebrafish and fugu showing the missing Scpp genes in sunfish (fa93e10, scpp7 and scpp4). The scpp4 pseudogene in the ocean sunfish is shown as a dotted arrow. Lower panel: Alignment of sunfish, fugu and medaka scpp4 sequences showing the single base insertion in exon 2 of this gene in sunfish resulting in a premature termination codon followed by a frameshift in the rest of the open reading frame. This insertion was confirmed by PCR and sequencing of genomic DNA from two other specimens (GenBank accession numbers KF737069 and KF737070). The termination codon in sunfish is underlined in red. The accession numbers for fugu and medaka scpp4 genes used in the alignment are DQ066525.1 and XM_004065875.2, respectively. chr, chromosome; scaf, scaffold
Mentions: We searched for SCPP genes in the sunfish genome to understand the genetic basis of the cartilaginous skeleton of the sunfish. We filled a sequencing gap in this intergenic region by sequencing a genomic PCR product to obtain the complete sequence for spp1. The orthology of the P/Q-rich SCPP genes in sunfish was verified by generating a Maximum Likelihood phylogenetic tree using sequences from sunfish, fugu, medaka and zebrafish (see Additional file 1: Figure S3). Sunfish contains two acidic SCPP genes (spp1 and scpp1) similar to fugu and zebrafish. However, it has lost two P/Q-rich SCPP genes (fa93e10 and scpp7) that are conserved in the other two teleosts (Fig. 4 and Additional file 4). This conclusion was reached after searching the genomic vicinity of the sunfish Sparcl1, the entire genome assembly and the raw reads of the sunfish genome using zebrafish fa93e10 and scpp7 protein sequences by TBLASTN. fa93e10 was first identified as an expressed sequence tag (EST) clone as part of a screen for genes that are expressed in regenerating zebrafish caudal fins [37]. Whole-mount in situ hybridization experiments in zebrafish suggested that fa93e10 is a growth marker that identifies cycles of growth in fin ray segments [37]. Its frequency of expression in fin rays decreases with the age of the fish in tandem with decreased distal mesenchymal cell proliferation [37, 38]. It is not clear whether the absence of fa93e10 in sunfish is somehow related to its unusual fin morphology. In addition to the complete loss of fa93e10 and scpp7, another P/Q-rich SCPP gene, scpp4, that is intact in fugu and medaka has become a pseudogene in the sunfish due to a single nucleotide insertion. This insertion was confirmed by PCR and sequencing of genomic DNA from two other unrelated specimens of sunfish (GenBank accession numbers KF737069 and KF737070), providing further evidence that scpp4 became nonfunctional in the sunfish lineage after it split from the pufferfish lineage (Fig. 4 and Additional files 1 and 4). However, the functional consequence of the loss of this gene in sunfish is not known. Zebrafish does not contain an orthologue of scpp4 but instead contains several other lineage-specific P/Q-rich SCPP genes (Fig. 4 and Additional file 4). Thus, the genetic basis of the cartilaginous skeleton in the sunfish remains unclear. It is possible that this distinctive phenotype is driven by a regulatory change and is therefore not evident in the bone gene repertoire.Fig. 4

View Article: PubMed Central - PubMed

ABSTRACT

Background: The ocean sunfish (Mola mola), which can grow up to a length of 2.7 m and weigh 2.3 tons, is the world’s largest bony fish. It has an extremely fast growth rate and its endoskeleton is mainly composed of cartilage. Another unique feature of the sunfish is its lack of a caudal fin, which is replaced by a broad and stiff lobe that results in the characteristic truncated appearance of the fish.

Results: To gain insights into the genomic basis of these phenotypic traits, we sequenced the sunfish genome and performed a comparative analysis with other teleost genomes. Several sunfish genes involved in the growth hormone and insulin-like growth factor 1 (GH/IGF1) axis signalling pathway were found to be under positive selection or accelerated evolution, which might explain its fast growth rate and large body size. A number of genes associated with the extracellular matrix, some of which are involved in the regulation of bone and cartilage development, have also undergone positive selection or accelerated evolution. A comparison of the sunfish genome with that of the pufferfish (fugu), which has a caudal fin, revealed that the sunfish contains more homeobox (Hox) genes although both genomes contain seven Hox clusters. Thus, caudal fin loss in sunfish is not associated with the loss of a specific Hox gene.

Conclusions: Our analyses provide insights into the molecular basis of the fast growth rate and large size of the ocean sunfish. The high-quality genome assembly generated in this study should facilitate further studies of this ‘natural mutant’.

Electronic supplementary material: The online version of this article (doi:10.1186/s13742-016-0144-3) contains supplementary material, which is available to authorized users.

No MeSH data available.