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Transcriptome analysis of food habit transition from carnivory to herbivory in a typical vertebrate herbivore, grass carp Ctenopharyngodon idella.

He S, Liang XF, Li L, Sun J, Wen ZY, Cheng XY, Li AX, Cai WJ, He YH, Wang YP, Tao YX, Yuan XC - BMC Genomics (2015)

Bottom Line: Altered expressions of Per, Cry, Clock, Bmal2, Pdp, Dec and Fbxl3 might reset circadian phase of fish after food habit transition.Expression of genes involved in digestion and metabolism were significantly different between fish before and after the transition.We also found extensive alternative splicing and novel transcript accompanying food habit transition.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, College of Fisheries, Huazhong Agricultural University, Hubei Collaborative Innovation Center for Freshwater Aquaculture, 430070, Wuhan, China. laile1985@163.com.

ABSTRACT

Background: Although feeding behavior and food habit are ecologically and economically important properties, little is known about formation and evolution of herbivory. Grass carp (Ctenopharyngodon idella) is an ecologically appealing model of vertebrate herbivore, widely cultivated in the world as edible fish or as biological control agents for aquatic weeds. Grass carp exhibits food habit transition from carnivory to herbivory during development. However, currently little is known about the genes regulating the unique food habit transition and the formation of herbivory, and how they could achieve higher growth rates on plant materials, which have a relatively poor nutritional quality.

Results: We showed that grass carp fed with duckweed (modeling fish after food habit transition) had significantly higher relative length of gut than fish before food habit transition or those fed with chironomid larvae (fish without transition). Using transcriptome sequencing, we identified 10,184 differentially expressed genes between grass carp before and after transition in brain, liver and gut. By eliminating genes potentially involved in development (via comparing fish with or without food habit transition), we identified changes in expression of genes involved in cell proliferation and differentiation, appetite control, circadian rhythm, and digestion and metabolism between fish before and after food habit transition. Up-regulation of GHRb, Egfr, Fgf, Fgfbp1, Insra, Irs2, Jak, STAT, PKC, PI3K expression in fish fed with duckweed, consistent with faster gut growth, could promote the food habit transition. Grass carp after food habit transition had increased appetite signal in brain. Altered expressions of Per, Cry, Clock, Bmal2, Pdp, Dec and Fbxl3 might reset circadian phase of fish after food habit transition. Expression of genes involved in digestion and metabolism were significantly different between fish before and after the transition.

Conclusions: We suggest that the food habit transition from carnivory to herbivory in grass carp might be due to enhanced gut growth, increased appetite, resetting of circadian phase and enhanced digestion and metabolism. We also found extensive alternative splicing and novel transcript accompanying food habit transition. These differences together might account for the food habit transition and the formation of herbivory in grass carp.

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Differentially expressed genes in circadian rhythm pathway between grass carp before and after food habit transition from transcriptome analysis. The colors of ellipses were shaded according to the different expression (red: the mRNA expression levels of fish in Group C were significantly higher than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1); green: the mRNA expression levels of fish in Group C were significantly lower than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1)). All of these genes were not differentially expressed between Groups A and B.
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Fig5: Differentially expressed genes in circadian rhythm pathway between grass carp before and after food habit transition from transcriptome analysis. The colors of ellipses were shaded according to the different expression (red: the mRNA expression levels of fish in Group C were significantly higher than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1); green: the mRNA expression levels of fish in Group C were significantly lower than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1)). All of these genes were not differentially expressed between Groups A and B.

Mentions: We found 10,184 genes to be differentially expressed between Groups A and C, 8,711 genes between Groups A and B, 4,435 genes between Groups B and C; and 40,149 genes to be differentially expressed between brain and gut, 47,849 genes between brain and liver, 35,434 genes between liver and gut (False Discovery Rate (FDR) ≤ 0.001, fold-change ≥ 2, Additional file 4). Genes differentially expressed between Groups A and C, but not differentially expressed between Groups A and B were potentially involved in the food habit transition of grass carp. We mapped the differentially expressed genes to the reference canonical pathways in Kyoto Encyclopedia of Genes and Genomes (KEGG) to identify the biological pathways. The representative pathways with the differentially expressed genes were MAPK signaling, adipocytokine, glutamatergic synapase, calcium signaling, GABAergic synapase, insulin signaling, PPAR signaling, pancreatic secretion, protein digestion and absorption, bile secretion and gastric acid secretion and mammalian circadian rhythm pathways. Analysis of these genes, which were differentially expressed between Groups A and C, but not differentially expressed between Groups A and B, revealed the signaling pathways involved, including cell proliferation and differentiation (growth hormone receptor b (GHRb), epidermal growth factor receptor (Egfr), fibroblast growth factor (Fgf), FGF-binding protein 1 (Fgfbp1), insulin receptor a (Insra), insulin receptor substrate 2 (Irs2), Janus kinase (Jak), signal transducer and activator of transcription 1 (STAT), phosphatidylinositol-4,5-bisphosphate 3-kinase (PI3K), protein kinase C (PKC), suppressor of cytokine signaling 1 (SOCS1)) (Figure 3); appetite control (agouti gene-related protein 2 (Agrp2), neuropeptide Y receptor 2 (Npy y2), dopamine receptor D1 (Drd1), GABA A receptor (GABAra), leptin (Leptin), cholecystokinin (Cck), insulin receptor a (Insra), insulin receptor substrate 2 (Irs2), thyrotropin-releasing hormone receptor 1 (Trhr1)) (Figure 4); circadian rhythm (period 1 (Per1), Per3, cryptochrome 5 (Cry5), Cry2, clock protein (Clock), Bmal2, hepatic leukemia factor (Pdp), class B basic helix-loop-helix protein (Dec), F-box and leucine-rich repeat protein 3 (Fbxl3), nocturnin) (Figure 5).Figure 3


Transcriptome analysis of food habit transition from carnivory to herbivory in a typical vertebrate herbivore, grass carp Ctenopharyngodon idella.

He S, Liang XF, Li L, Sun J, Wen ZY, Cheng XY, Li AX, Cai WJ, He YH, Wang YP, Tao YX, Yuan XC - BMC Genomics (2015)

Differentially expressed genes in circadian rhythm pathway between grass carp before and after food habit transition from transcriptome analysis. The colors of ellipses were shaded according to the different expression (red: the mRNA expression levels of fish in Group C were significantly higher than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1); green: the mRNA expression levels of fish in Group C were significantly lower than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1)). All of these genes were not differentially expressed between Groups A and B.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC4307112&req=5

Fig5: Differentially expressed genes in circadian rhythm pathway between grass carp before and after food habit transition from transcriptome analysis. The colors of ellipses were shaded according to the different expression (red: the mRNA expression levels of fish in Group C were significantly higher than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1); green: the mRNA expression levels of fish in Group C were significantly lower than those in Group A (FDR ≤ 0.001, the absolute value of log2[Ratio] ≥ 1)). All of these genes were not differentially expressed between Groups A and B.
Mentions: We found 10,184 genes to be differentially expressed between Groups A and C, 8,711 genes between Groups A and B, 4,435 genes between Groups B and C; and 40,149 genes to be differentially expressed between brain and gut, 47,849 genes between brain and liver, 35,434 genes between liver and gut (False Discovery Rate (FDR) ≤ 0.001, fold-change ≥ 2, Additional file 4). Genes differentially expressed between Groups A and C, but not differentially expressed between Groups A and B were potentially involved in the food habit transition of grass carp. We mapped the differentially expressed genes to the reference canonical pathways in Kyoto Encyclopedia of Genes and Genomes (KEGG) to identify the biological pathways. The representative pathways with the differentially expressed genes were MAPK signaling, adipocytokine, glutamatergic synapase, calcium signaling, GABAergic synapase, insulin signaling, PPAR signaling, pancreatic secretion, protein digestion and absorption, bile secretion and gastric acid secretion and mammalian circadian rhythm pathways. Analysis of these genes, which were differentially expressed between Groups A and C, but not differentially expressed between Groups A and B, revealed the signaling pathways involved, including cell proliferation and differentiation (growth hormone receptor b (GHRb), epidermal growth factor receptor (Egfr), fibroblast growth factor (Fgf), FGF-binding protein 1 (Fgfbp1), insulin receptor a (Insra), insulin receptor substrate 2 (Irs2), Janus kinase (Jak), signal transducer and activator of transcription 1 (STAT), phosphatidylinositol-4,5-bisphosphate 3-kinase (PI3K), protein kinase C (PKC), suppressor of cytokine signaling 1 (SOCS1)) (Figure 3); appetite control (agouti gene-related protein 2 (Agrp2), neuropeptide Y receptor 2 (Npy y2), dopamine receptor D1 (Drd1), GABA A receptor (GABAra), leptin (Leptin), cholecystokinin (Cck), insulin receptor a (Insra), insulin receptor substrate 2 (Irs2), thyrotropin-releasing hormone receptor 1 (Trhr1)) (Figure 4); circadian rhythm (period 1 (Per1), Per3, cryptochrome 5 (Cry5), Cry2, clock protein (Clock), Bmal2, hepatic leukemia factor (Pdp), class B basic helix-loop-helix protein (Dec), F-box and leucine-rich repeat protein 3 (Fbxl3), nocturnin) (Figure 5).Figure 3

Bottom Line: Altered expressions of Per, Cry, Clock, Bmal2, Pdp, Dec and Fbxl3 might reset circadian phase of fish after food habit transition.Expression of genes involved in digestion and metabolism were significantly different between fish before and after the transition.We also found extensive alternative splicing and novel transcript accompanying food habit transition.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Freshwater Animal Breeding, Ministry of Agriculture, College of Fisheries, Huazhong Agricultural University, Hubei Collaborative Innovation Center for Freshwater Aquaculture, 430070, Wuhan, China. laile1985@163.com.

ABSTRACT

Background: Although feeding behavior and food habit are ecologically and economically important properties, little is known about formation and evolution of herbivory. Grass carp (Ctenopharyngodon idella) is an ecologically appealing model of vertebrate herbivore, widely cultivated in the world as edible fish or as biological control agents for aquatic weeds. Grass carp exhibits food habit transition from carnivory to herbivory during development. However, currently little is known about the genes regulating the unique food habit transition and the formation of herbivory, and how they could achieve higher growth rates on plant materials, which have a relatively poor nutritional quality.

Results: We showed that grass carp fed with duckweed (modeling fish after food habit transition) had significantly higher relative length of gut than fish before food habit transition or those fed with chironomid larvae (fish without transition). Using transcriptome sequencing, we identified 10,184 differentially expressed genes between grass carp before and after transition in brain, liver and gut. By eliminating genes potentially involved in development (via comparing fish with or without food habit transition), we identified changes in expression of genes involved in cell proliferation and differentiation, appetite control, circadian rhythm, and digestion and metabolism between fish before and after food habit transition. Up-regulation of GHRb, Egfr, Fgf, Fgfbp1, Insra, Irs2, Jak, STAT, PKC, PI3K expression in fish fed with duckweed, consistent with faster gut growth, could promote the food habit transition. Grass carp after food habit transition had increased appetite signal in brain. Altered expressions of Per, Cry, Clock, Bmal2, Pdp, Dec and Fbxl3 might reset circadian phase of fish after food habit transition. Expression of genes involved in digestion and metabolism were significantly different between fish before and after the transition.

Conclusions: We suggest that the food habit transition from carnivory to herbivory in grass carp might be due to enhanced gut growth, increased appetite, resetting of circadian phase and enhanced digestion and metabolism. We also found extensive alternative splicing and novel transcript accompanying food habit transition. These differences together might account for the food habit transition and the formation of herbivory in grass carp.

Show MeSH
Related in: MedlinePlus