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Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation.

Ao J, Mu Y, Xiang LX, Fan D, Feng M, Zhang S, Shi Q, Zhu LY, Li T, Ding Y, Nie L, Li Q, Dong WR, Jiang L, Sun B, Zhang X, Li M, Zhang HQ, Xie S, Zhu Y, Jiang X, Wang X, Mu P, Chen W, Yue Z, Wang Z, Wang J, Shao JZ, Chen X - PLoS Genet. (2015)

Bottom Line: Gene families underlying adaptive behaviours, such as vision-related crystallins, olfactory receptors, and auditory sense-related genes, were significantly expanded in the genome of L. crocea relative to those of other vertebrates.Proteomics data demonstrate that skin mucus of the air-exposed L. crocea had a complex composition, with an unexpectedly high number of proteins (3,209), suggesting its multiple protective mechanisms involved in antioxidant functions, oxygen transport, immune defence, and osmotic and ionic regulation.The data generated by this study will provide valuable resources for the genetic improvement of stress resistance and yield potential in L. crocea.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Marine Biogenetics and Resources, Third Institute of Oceanography, State Oceanic Administration, Fujian Collaborative Innovation Center for Exploitation and Utilization of Marine Biological Resources, Key Laboratory of Marine Genetic Resources of Fujian Province, Xiamen, P. R. China.

ABSTRACT
The large yellow croaker Larimichthys crocea (L. crocea) is one of the most economically important marine fish in China and East Asian countries. It also exhibits peculiar behavioral and physiological characteristics, especially sensitive to various environmental stresses, such as hypoxia and air exposure. These traits may render L. crocea a good model for investigating the response mechanisms to environmental stress. To understand the molecular and genetic mechanisms underlying the adaptation and response of L. crocea to environmental stress, we sequenced and assembled the genome of L. crocea using a bacterial artificial chromosome and whole-genome shotgun hierarchical strategy. The final genome assembly was 679 Mb, with a contig N50 of 63.11 kb and a scaffold N50 of 1.03 Mb, containing 25,401 protein-coding genes. Gene families underlying adaptive behaviours, such as vision-related crystallins, olfactory receptors, and auditory sense-related genes, were significantly expanded in the genome of L. crocea relative to those of other vertebrates. Transcriptome analyses of the hypoxia-exposed L. crocea brain revealed new aspects of neuro-endocrine-immune/metabolism regulatory networks that may help the fish to avoid cerebral inflammatory injury and maintain energy balance under hypoxia. Proteomics data demonstrate that skin mucus of the air-exposed L. crocea had a complex composition, with an unexpectedly high number of proteins (3,209), suggesting its multiple protective mechanisms involved in antioxidant functions, oxygen transport, immune defence, and osmotic and ionic regulation. Our results reveal the molecular and genetic basis of fish adaptation and response to hypoxia and air exposure. The data generated by this study will provide valuable resources for the genetic improvement of stress resistance and yield potential in L. crocea.

No MeSH data available.


Related in: MedlinePlus

Skin mucus proteins are overexpressed in air-exposed L. crocea.(A) The distribution of mucus proteins in the molecular function class of Gene Ontology is shown. The over-represented functional categories are indicated in the pie chart, of which oxidoreductase activity-, peroxidase activity-, oxygen binding-, and ion binding-related proteins are enriched. (B) A representation of the functional mechanisms of the mucus barrier is shown. The continuously replenished thick mucus layer can retain a large number of antioxidant, immune, oxygen-binding, and ion-binding molecules, which are involved in antioxidant functions, immune defence, oxygen transport, and osmotic and ionic regulation, respectively. Antioxidant, immune, oxygen-binding, and ion-binding molecules are indicated in red, green, blue, and gray, respectively.
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pgen.1005118.g004: Skin mucus proteins are overexpressed in air-exposed L. crocea.(A) The distribution of mucus proteins in the molecular function class of Gene Ontology is shown. The over-represented functional categories are indicated in the pie chart, of which oxidoreductase activity-, peroxidase activity-, oxygen binding-, and ion binding-related proteins are enriched. (B) A representation of the functional mechanisms of the mucus barrier is shown. The continuously replenished thick mucus layer can retain a large number of antioxidant, immune, oxygen-binding, and ion-binding molecules, which are involved in antioxidant functions, immune defence, oxygen transport, and osmotic and ionic regulation, respectively. Antioxidant, immune, oxygen-binding, and ion-binding molecules are indicated in red, green, blue, and gray, respectively.

Mentions: We identified 22,054 peptides belonging to 3,209 genes in the L. crocea skin mucus proteome, and this accounted for more than 12% of the protein-coding genes in the genome (S24 Table). The complexity of the L. crocea mucus presumably relates to the multitude of its biological functions that allow the fish to survive and adapt to environmental changes. The over-represented functional categories were oxidoreductase activity (GO:0016491, P = 1.58×10-35, 223 proteins), peroxidase activity (GO:0004601, P = 0.0075, 9 proteins), oxygen binding (GO:0019825, P = 0.0011, 8 proteins), and ion binding (GO:0043167, P = 2.21×10-6, 347 proteins) (Fig. 4A and S18 Fig.). Two hundred and thirty-two antioxidant proteins that were related to oxidoreductase activity and peroxidase activity were highly enriched in the L. crocea mucus, and they included peroxiredoxins, glutathione peroxidase, and thioredoxin (S25 Table). These proteins intercept and degrade environmental peroxyl and hydroxyl radicals from aqueous environments [53]. Therefore, the presence of high-abundance antioxidant proteins in the skin mucus may have the potential to protect fish against air exposure-induced oxidative damage (Fig. 4B). Eight proteins related to oxygen transport, including hemoglobin subunits α1, αA, αD, β, and β1, and cytoglobin-1, were identified in the L. crocea skin mucus (S26 Table). The abundant expression of hemoglobin may contribute to the binding and holding of oxygen for respiration. Various immune molecules that provide immediate protection to fish from potential pathogens, such as lectins, lysozymes, C-reactive proteins, complement components, immunoglobulins, and chemokines, were also found in the L. crocea skin mucus (S27 Table). To date, the mechanisms of osmotic and ionic regulation of the skin mucus have not been confirmed [49]. In this study, a large number of ion-binding proteins were identified in the L. crocea mucus (S28 Table). These proteins and the layer of mucus may have a role in limiting the diffusion of ions on the surface of the fish (Fig. 4B). However, a substantial proportion of the proteins, which are highly present in the skin mucus of fish under air exposure, play an unknown role in the mucus response.


Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation.

Ao J, Mu Y, Xiang LX, Fan D, Feng M, Zhang S, Shi Q, Zhu LY, Li T, Ding Y, Nie L, Li Q, Dong WR, Jiang L, Sun B, Zhang X, Li M, Zhang HQ, Xie S, Zhu Y, Jiang X, Wang X, Mu P, Chen W, Yue Z, Wang Z, Wang J, Shao JZ, Chen X - PLoS Genet. (2015)

Skin mucus proteins are overexpressed in air-exposed L. crocea.(A) The distribution of mucus proteins in the molecular function class of Gene Ontology is shown. The over-represented functional categories are indicated in the pie chart, of which oxidoreductase activity-, peroxidase activity-, oxygen binding-, and ion binding-related proteins are enriched. (B) A representation of the functional mechanisms of the mucus barrier is shown. The continuously replenished thick mucus layer can retain a large number of antioxidant, immune, oxygen-binding, and ion-binding molecules, which are involved in antioxidant functions, immune defence, oxygen transport, and osmotic and ionic regulation, respectively. Antioxidant, immune, oxygen-binding, and ion-binding molecules are indicated in red, green, blue, and gray, respectively.
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4383535&req=5

pgen.1005118.g004: Skin mucus proteins are overexpressed in air-exposed L. crocea.(A) The distribution of mucus proteins in the molecular function class of Gene Ontology is shown. The over-represented functional categories are indicated in the pie chart, of which oxidoreductase activity-, peroxidase activity-, oxygen binding-, and ion binding-related proteins are enriched. (B) A representation of the functional mechanisms of the mucus barrier is shown. The continuously replenished thick mucus layer can retain a large number of antioxidant, immune, oxygen-binding, and ion-binding molecules, which are involved in antioxidant functions, immune defence, oxygen transport, and osmotic and ionic regulation, respectively. Antioxidant, immune, oxygen-binding, and ion-binding molecules are indicated in red, green, blue, and gray, respectively.
Mentions: We identified 22,054 peptides belonging to 3,209 genes in the L. crocea skin mucus proteome, and this accounted for more than 12% of the protein-coding genes in the genome (S24 Table). The complexity of the L. crocea mucus presumably relates to the multitude of its biological functions that allow the fish to survive and adapt to environmental changes. The over-represented functional categories were oxidoreductase activity (GO:0016491, P = 1.58×10-35, 223 proteins), peroxidase activity (GO:0004601, P = 0.0075, 9 proteins), oxygen binding (GO:0019825, P = 0.0011, 8 proteins), and ion binding (GO:0043167, P = 2.21×10-6, 347 proteins) (Fig. 4A and S18 Fig.). Two hundred and thirty-two antioxidant proteins that were related to oxidoreductase activity and peroxidase activity were highly enriched in the L. crocea mucus, and they included peroxiredoxins, glutathione peroxidase, and thioredoxin (S25 Table). These proteins intercept and degrade environmental peroxyl and hydroxyl radicals from aqueous environments [53]. Therefore, the presence of high-abundance antioxidant proteins in the skin mucus may have the potential to protect fish against air exposure-induced oxidative damage (Fig. 4B). Eight proteins related to oxygen transport, including hemoglobin subunits α1, αA, αD, β, and β1, and cytoglobin-1, were identified in the L. crocea skin mucus (S26 Table). The abundant expression of hemoglobin may contribute to the binding and holding of oxygen for respiration. Various immune molecules that provide immediate protection to fish from potential pathogens, such as lectins, lysozymes, C-reactive proteins, complement components, immunoglobulins, and chemokines, were also found in the L. crocea skin mucus (S27 Table). To date, the mechanisms of osmotic and ionic regulation of the skin mucus have not been confirmed [49]. In this study, a large number of ion-binding proteins were identified in the L. crocea mucus (S28 Table). These proteins and the layer of mucus may have a role in limiting the diffusion of ions on the surface of the fish (Fig. 4B). However, a substantial proportion of the proteins, which are highly present in the skin mucus of fish under air exposure, play an unknown role in the mucus response.

Bottom Line: Gene families underlying adaptive behaviours, such as vision-related crystallins, olfactory receptors, and auditory sense-related genes, were significantly expanded in the genome of L. crocea relative to those of other vertebrates.Proteomics data demonstrate that skin mucus of the air-exposed L. crocea had a complex composition, with an unexpectedly high number of proteins (3,209), suggesting its multiple protective mechanisms involved in antioxidant functions, oxygen transport, immune defence, and osmotic and ionic regulation.The data generated by this study will provide valuable resources for the genetic improvement of stress resistance and yield potential in L. crocea.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Marine Biogenetics and Resources, Third Institute of Oceanography, State Oceanic Administration, Fujian Collaborative Innovation Center for Exploitation and Utilization of Marine Biological Resources, Key Laboratory of Marine Genetic Resources of Fujian Province, Xiamen, P. R. China.

ABSTRACT
The large yellow croaker Larimichthys crocea (L. crocea) is one of the most economically important marine fish in China and East Asian countries. It also exhibits peculiar behavioral and physiological characteristics, especially sensitive to various environmental stresses, such as hypoxia and air exposure. These traits may render L. crocea a good model for investigating the response mechanisms to environmental stress. To understand the molecular and genetic mechanisms underlying the adaptation and response of L. crocea to environmental stress, we sequenced and assembled the genome of L. crocea using a bacterial artificial chromosome and whole-genome shotgun hierarchical strategy. The final genome assembly was 679 Mb, with a contig N50 of 63.11 kb and a scaffold N50 of 1.03 Mb, containing 25,401 protein-coding genes. Gene families underlying adaptive behaviours, such as vision-related crystallins, olfactory receptors, and auditory sense-related genes, were significantly expanded in the genome of L. crocea relative to those of other vertebrates. Transcriptome analyses of the hypoxia-exposed L. crocea brain revealed new aspects of neuro-endocrine-immune/metabolism regulatory networks that may help the fish to avoid cerebral inflammatory injury and maintain energy balance under hypoxia. Proteomics data demonstrate that skin mucus of the air-exposed L. crocea had a complex composition, with an unexpectedly high number of proteins (3,209), suggesting its multiple protective mechanisms involved in antioxidant functions, oxygen transport, immune defence, and osmotic and ionic regulation. Our results reveal the molecular and genetic basis of fish adaptation and response to hypoxia and air exposure. The data generated by this study will provide valuable resources for the genetic improvement of stress resistance and yield potential in L. crocea.

No MeSH data available.


Related in: MedlinePlus