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

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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.


Related in: MedlinePlus

Genes related to bone and cartilage. Schematic diagram showing the extracellular matrix of cartilage (adapted from [82]). The figure illustrates collagens (mostly type II collagen), proteoglycans (primarily aggrecan), and other non-collagenous proteins including link protein (yellow circles) and fibronectin. Stars denote fast evolution or positive selection. COMP, cartilage oligomeric matrix protein
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Fig3: Genes related to bone and cartilage. Schematic diagram showing the extracellular matrix of cartilage (adapted from [82]). The figure illustrates collagens (mostly type II collagen), proteoglycans (primarily aggrecan), and other non-collagenous proteins including link protein (yellow circles) and fibronectin. Stars denote fast evolution or positive selection. COMP, cartilage oligomeric matrix protein

Mentions: Another interesting set of fast-evolving genes/genes with positively selected sites are those related to the ECM. The ECM provides the microenvironment of the cell as well as bulk, shape and strength to tissues such as bone and cartilage. In addition, the ECM also contains components required for the conversion of cartilage to bone and its homeostasis [30, 31]. We found a number of genes related to the ECM that exhibit fast evolution or positive selection (Additional file 1: Table S8). The gene COL2A1 encoding type II collagen, which normally represents approximately 80–90 % of the collagen content of the cartilage matrix [32] (Fig. 3), is present in two copies (col2a1a and col2a1b) and contains positively selected sites in the sunfish (Additional file 1: Table S8). Several ECM-related genes (col11a1a, col11a2, bmp1b, fkbp10b, lepre1, serpinf1 and sp7) also exhibit elevated dN/dS values (Additional file 1: Table S8) but as there are no signs of positive selection, these genes might be under relaxed selection.Fig. 3


The genome of the largest bony fish, ocean sunfish ( Mola mola ), provides insights into its fast growth rate
Genes related to bone and cartilage. Schematic diagram showing the extracellular matrix of cartilage (adapted from [82]). The figure illustrates collagens (mostly type II collagen), proteoglycans (primarily aggrecan), and other non-collagenous proteins including link protein (yellow circles) and fibronectin. Stars denote fast evolution or positive selection. COMP, cartilage oligomeric matrix protein
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig3: Genes related to bone and cartilage. Schematic diagram showing the extracellular matrix of cartilage (adapted from [82]). The figure illustrates collagens (mostly type II collagen), proteoglycans (primarily aggrecan), and other non-collagenous proteins including link protein (yellow circles) and fibronectin. Stars denote fast evolution or positive selection. COMP, cartilage oligomeric matrix protein
Mentions: Another interesting set of fast-evolving genes/genes with positively selected sites are those related to the ECM. The ECM provides the microenvironment of the cell as well as bulk, shape and strength to tissues such as bone and cartilage. In addition, the ECM also contains components required for the conversion of cartilage to bone and its homeostasis [30, 31]. We found a number of genes related to the ECM that exhibit fast evolution or positive selection (Additional file 1: Table S8). The gene COL2A1 encoding type II collagen, which normally represents approximately 80–90 % of the collagen content of the cartilage matrix [32] (Fig. 3), is present in two copies (col2a1a and col2a1b) and contains positively selected sites in the sunfish (Additional file 1: Table S8). Several ECM-related genes (col11a1a, col11a2, bmp1b, fkbp10b, lepre1, serpinf1 and sp7) also exhibit elevated dN/dS values (Additional file 1: Table S8) but as there are no signs of positive selection, these genes might be under relaxed selection.Fig. 3

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.


Related in: MedlinePlus