Limits...
Messenger RNA sequencing and pathway analysis provide novel insights into the biological basis of chickens' feed efficiency.

Zhou N, Lee WR, Abasht B - BMC Genomics (2015)

Bottom Line: Differential expression analysis identified 1,059 genes (FDR < 0.05) that significantly divergently expressed in breast muscle between the high- and low-FE chickens.This study provides novel insights into transcriptional differences in breast muscle between high- and low-FE broiler chickens.Our results show that feed efficiency is associated with breast muscle growth in these birds; furthermore, some physiological changes, e.g., inflammatory response and oxidative stress, may occur in the breast muscle of the high-FE chickens, which may be of concern for continued selection for both of these traits together in modern broiler chickens.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal and Food Sciences, University of Delaware, Newark, DE, 19716, USA. nanzhou@udel.edu.

ABSTRACT

Background: Advanced selection technologies have been developed and continually optimized to improve traits of agricultural importance; however, these methods have been primarily applied without knowledge of underlying biological changes that may be induced by selection. This study aims to characterize the biological basis of differences between chickens with low and high feed efficiency (FE) with a long-term goal of improving the ability to select for FE.

Results: High-throughput RNA sequencing was performed on 23 breast muscle samples from commercial broiler chickens with extremely high (n = 10) and low (n = 13) FE. An average of 34 million paired-end reads (75 bp) were produced for each sample, 80% of which were properly mapped to the chicken reference genome (Ensembl Galgal4). Differential expression analysis identified 1,059 genes (FDR < 0.05) that significantly divergently expressed in breast muscle between the high- and low-FE chickens. Gene function analysis revealed that genes involved in muscle remodeling, inflammatory response and free radical scavenging were mostly up-regulated in the high-FE birds. Additionally, growth hormone and IGFs/PI3K/Akt signaling pathways were enriched in differentially expressed genes, which might contribute to the high breast muscle yield in high-FE birds and partly explain the FE advantage of high-FE chickens.

Conclusions: This study provides novel insights into transcriptional differences in breast muscle between high- and low-FE broiler chickens. Our results show that feed efficiency is associated with breast muscle growth in these birds; furthermore, some physiological changes, e.g., inflammatory response and oxidative stress, may occur in the breast muscle of the high-FE chickens, which may be of concern for continued selection for both of these traits together in modern broiler chickens.

No MeSH data available.


Related in: MedlinePlus

NRF2-mediated oxidative stress response. A. The Keap1-NRF2 pathway from IPA software. Canonical pathway analysis identified that the Keap1-NRF2 pathway was statistically significant with P-value = 6.96E-04. Red and green symbols indicate genes up- and down-regulated in the high-FE chickens, respectively. The color intensity is proportional to the degree of fold change. B. NRF2 (NFE2L2) is predicted to be activated in the high-FE chickens by Ingenuity Upstream Regulator Analysis.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4414306&req=5

Fig7: NRF2-mediated oxidative stress response. A. The Keap1-NRF2 pathway from IPA software. Canonical pathway analysis identified that the Keap1-NRF2 pathway was statistically significant with P-value = 6.96E-04. Red and green symbols indicate genes up- and down-regulated in the high-FE chickens, respectively. The color intensity is proportional to the degree of fold change. B. NRF2 (NFE2L2) is predicted to be activated in the high-FE chickens by Ingenuity Upstream Regulator Analysis.

Mentions: The IPA downstream effect analysis supports our hypothesis regarding increased ROS production in the breast muscle of high FE-chickens. Processes, including metabolism of reactive oxygen species (P-value = 5.77E-07), synthesis of reactive oxygen species (P-value = 1.75E-06), production of reactive oxygen species (P-value = 4.92E-06) and production of superoxide (P-value = 2.05E-03), are predicted to be increased in the high-FE chickens. In addition, the NRF2-mediated oxidative stress response pathway is over-represented among the differentially expressed genes, with 17 genes (P-value = 6.96E-04; ratio = 0.089) mapped to this pathway (Figure 7A). Nuclear factor (erythroid-derived 2)-like 2 (NRF2), also known as NFE2L2, is a key transcription factor in cells that responds to a range of oxidative and xenobiotic stresses [91]. Upon exposure of cells to various stimuli such as ROS and electrophilic compounds, quiescent NRF2 in cytoplasm is activated through phosphatidylinositol 3-kinase (PI3K), RAS and PKC signaling pathways [92]. By phosphorylation or binding to actin, activated NRF2 translocates into the nucleus and binds to the antioxidant response elements, initiating the transcription of a number of genes encoding for antioxidants and ROS detoxifying enzymes [93]. A group of NRF2 downstream genes, including v-maf musculoaponeurotic fibrosarcoma oncogene homolog F (avian) (MAFF) [fold-change = 1.61], glutathione S-transferase A3 (GSTA3) [fold-change = 2.03], glutathione S-transferase omega 1 (GSTO1) [fold-change = 1.50], heme oxygenase (decycling) 1 (HMOX1) [fold-change = 1.36], microsomal glutathione S-transferase 1 (MGST1) [fold-change = 1.39], superoxide dismutase 3 (SOD3) [fold-change = 1.85], thioredoxin (TXN) [fold-change = 1.50], peptidylprolyl isomerase B (PPIB) [fold-change = 1.43], aldehyde oxidase 1 (AOX1) [fold-change = -1.63], DnaJ (Hsp40) homolog, subfamily A, member 1 (DNAJA1) [fold-change = -1.39] and DnaJ (Hsp40) homolog, subfamily C, member 1 (DNAJC1) [fold-change = -1.35], are differentially expressed in the current study. Genes encoding for antioxidant proteins, such as SOD3, HMOX1 and TXN, are up-regulated in the high-FE birds. Protein encoded by SOD3 is an extracellular protective enzyme against not only ROS but also inflammation, thus playing a role in tissue recovery [94]. HMOX1 is increased in the condition of oxidative stress and has an effect on protecting cells against ROS and inflammation [95]. The TXN-encoded protein is involved in a range of redox reactions and can decrease the quantity of ROS [96]. The up-regulation of TXN, SOD3 and HMOX1 indicates that an NRF2-mediated antioxidant response is activated in the breast muscle of the high-FE chickens. Additionally, three members from the glutathione s-transferase (GST) group, encoded by GSTO1, GSTA1 and MGST1, are all up-regulated in the high-FE birds. GST is known for its function in detoxification of xenobiotics as well as endogenous metabolites [97]. The increased expression of the GST superfamily also suggests that responses to oxidative stress are elevated in the breast muscle of the high-FE chickens. Although few genes in the NRF2 signaling pathway, including AOX1, DNAJA1 and DNAJC1, are down-regulated in the high-FE chickens, overall there are 14 up-regulated genes mapped to this pathway, indicating that NRF2-mediated oxidative stress response is augmented in the breast muscle of the high-FE birds. Moreover, NRF2 (NFE2L2), a transcription factor, is predicted to be activated in the high-FE chickens (P-value = 1.94E-05; z-score = 2.036) (Figure 7B). Taken together, our results suggest a higher level of ROS generated in the breast muscle of high-FE chickens.Figure 7


Messenger RNA sequencing and pathway analysis provide novel insights into the biological basis of chickens' feed efficiency.

Zhou N, Lee WR, Abasht B - BMC Genomics (2015)

NRF2-mediated oxidative stress response. A. The Keap1-NRF2 pathway from IPA software. Canonical pathway analysis identified that the Keap1-NRF2 pathway was statistically significant with P-value = 6.96E-04. Red and green symbols indicate genes up- and down-regulated in the high-FE chickens, respectively. The color intensity is proportional to the degree of fold change. B. NRF2 (NFE2L2) is predicted to be activated in the high-FE chickens by Ingenuity Upstream Regulator Analysis.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4414306&req=5

Fig7: NRF2-mediated oxidative stress response. A. The Keap1-NRF2 pathway from IPA software. Canonical pathway analysis identified that the Keap1-NRF2 pathway was statistically significant with P-value = 6.96E-04. Red and green symbols indicate genes up- and down-regulated in the high-FE chickens, respectively. The color intensity is proportional to the degree of fold change. B. NRF2 (NFE2L2) is predicted to be activated in the high-FE chickens by Ingenuity Upstream Regulator Analysis.
Mentions: The IPA downstream effect analysis supports our hypothesis regarding increased ROS production in the breast muscle of high FE-chickens. Processes, including metabolism of reactive oxygen species (P-value = 5.77E-07), synthesis of reactive oxygen species (P-value = 1.75E-06), production of reactive oxygen species (P-value = 4.92E-06) and production of superoxide (P-value = 2.05E-03), are predicted to be increased in the high-FE chickens. In addition, the NRF2-mediated oxidative stress response pathway is over-represented among the differentially expressed genes, with 17 genes (P-value = 6.96E-04; ratio = 0.089) mapped to this pathway (Figure 7A). Nuclear factor (erythroid-derived 2)-like 2 (NRF2), also known as NFE2L2, is a key transcription factor in cells that responds to a range of oxidative and xenobiotic stresses [91]. Upon exposure of cells to various stimuli such as ROS and electrophilic compounds, quiescent NRF2 in cytoplasm is activated through phosphatidylinositol 3-kinase (PI3K), RAS and PKC signaling pathways [92]. By phosphorylation or binding to actin, activated NRF2 translocates into the nucleus and binds to the antioxidant response elements, initiating the transcription of a number of genes encoding for antioxidants and ROS detoxifying enzymes [93]. A group of NRF2 downstream genes, including v-maf musculoaponeurotic fibrosarcoma oncogene homolog F (avian) (MAFF) [fold-change = 1.61], glutathione S-transferase A3 (GSTA3) [fold-change = 2.03], glutathione S-transferase omega 1 (GSTO1) [fold-change = 1.50], heme oxygenase (decycling) 1 (HMOX1) [fold-change = 1.36], microsomal glutathione S-transferase 1 (MGST1) [fold-change = 1.39], superoxide dismutase 3 (SOD3) [fold-change = 1.85], thioredoxin (TXN) [fold-change = 1.50], peptidylprolyl isomerase B (PPIB) [fold-change = 1.43], aldehyde oxidase 1 (AOX1) [fold-change = -1.63], DnaJ (Hsp40) homolog, subfamily A, member 1 (DNAJA1) [fold-change = -1.39] and DnaJ (Hsp40) homolog, subfamily C, member 1 (DNAJC1) [fold-change = -1.35], are differentially expressed in the current study. Genes encoding for antioxidant proteins, such as SOD3, HMOX1 and TXN, are up-regulated in the high-FE birds. Protein encoded by SOD3 is an extracellular protective enzyme against not only ROS but also inflammation, thus playing a role in tissue recovery [94]. HMOX1 is increased in the condition of oxidative stress and has an effect on protecting cells against ROS and inflammation [95]. The TXN-encoded protein is involved in a range of redox reactions and can decrease the quantity of ROS [96]. The up-regulation of TXN, SOD3 and HMOX1 indicates that an NRF2-mediated antioxidant response is activated in the breast muscle of the high-FE chickens. Additionally, three members from the glutathione s-transferase (GST) group, encoded by GSTO1, GSTA1 and MGST1, are all up-regulated in the high-FE birds. GST is known for its function in detoxification of xenobiotics as well as endogenous metabolites [97]. The increased expression of the GST superfamily also suggests that responses to oxidative stress are elevated in the breast muscle of the high-FE chickens. Although few genes in the NRF2 signaling pathway, including AOX1, DNAJA1 and DNAJC1, are down-regulated in the high-FE chickens, overall there are 14 up-regulated genes mapped to this pathway, indicating that NRF2-mediated oxidative stress response is augmented in the breast muscle of the high-FE birds. Moreover, NRF2 (NFE2L2), a transcription factor, is predicted to be activated in the high-FE chickens (P-value = 1.94E-05; z-score = 2.036) (Figure 7B). Taken together, our results suggest a higher level of ROS generated in the breast muscle of high-FE chickens.Figure 7

Bottom Line: Differential expression analysis identified 1,059 genes (FDR < 0.05) that significantly divergently expressed in breast muscle between the high- and low-FE chickens.This study provides novel insights into transcriptional differences in breast muscle between high- and low-FE broiler chickens.Our results show that feed efficiency is associated with breast muscle growth in these birds; furthermore, some physiological changes, e.g., inflammatory response and oxidative stress, may occur in the breast muscle of the high-FE chickens, which may be of concern for continued selection for both of these traits together in modern broiler chickens.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal and Food Sciences, University of Delaware, Newark, DE, 19716, USA. nanzhou@udel.edu.

ABSTRACT

Background: Advanced selection technologies have been developed and continually optimized to improve traits of agricultural importance; however, these methods have been primarily applied without knowledge of underlying biological changes that may be induced by selection. This study aims to characterize the biological basis of differences between chickens with low and high feed efficiency (FE) with a long-term goal of improving the ability to select for FE.

Results: High-throughput RNA sequencing was performed on 23 breast muscle samples from commercial broiler chickens with extremely high (n = 10) and low (n = 13) FE. An average of 34 million paired-end reads (75 bp) were produced for each sample, 80% of which were properly mapped to the chicken reference genome (Ensembl Galgal4). Differential expression analysis identified 1,059 genes (FDR < 0.05) that significantly divergently expressed in breast muscle between the high- and low-FE chickens. Gene function analysis revealed that genes involved in muscle remodeling, inflammatory response and free radical scavenging were mostly up-regulated in the high-FE birds. Additionally, growth hormone and IGFs/PI3K/Akt signaling pathways were enriched in differentially expressed genes, which might contribute to the high breast muscle yield in high-FE birds and partly explain the FE advantage of high-FE chickens.

Conclusions: This study provides novel insights into transcriptional differences in breast muscle between high- and low-FE broiler chickens. Our results show that feed efficiency is associated with breast muscle growth in these birds; furthermore, some physiological changes, e.g., inflammatory response and oxidative stress, may occur in the breast muscle of the high-FE chickens, which may be of concern for continued selection for both of these traits together in modern broiler chickens.

No MeSH data available.


Related in: MedlinePlus