A Genome-Wide mRNA Screen and Functional Analysis Reveal FOXO3 as a Candidate Gene for Chicken Growth

Chicken growth performance provides direct economic benefits to the poultry industry. However, the underlying genetic mechanisms are unclear. The objective of this study was to identify candidate genes associated with chicken growth and investigate their potential mechanisms. We used RNA-Seq to stud...

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Veröffentlicht in:PloS one 2015-09, Vol.10 (9), p.e0137087-e0137087
Hauptverfasser: Chen, Biao, Xu, Jiguo, He, Xiaomei, Xu, Haiping, Li, Guihuan, Du, Hongli, Nie, Qinghua, Zhang, Xiquan
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container_issue 9
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container_title PloS one
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creator Chen, Biao
Xu, Jiguo
He, Xiaomei
Xu, Haiping
Li, Guihuan
Du, Hongli
Nie, Qinghua
Zhang, Xiquan
description Chicken growth performance provides direct economic benefits to the poultry industry. However, the underlying genetic mechanisms are unclear. The objective of this study was to identify candidate genes associated with chicken growth and investigate their potential mechanisms. We used RNA-Seq to study the breast muscle transcriptome in high and low tails of Recessive White Rock (WRRh, WRRl) and Xinghua chickens (XHh, XHl). A total of 60, 23, 153 and 359 differentially expressed genes were detected in WRRh vs. WRRl, XHh vs. XHl, WRRh vs. XHh and WRRl vs. XHl, respectively. GO, KEGG pathway and gene network analyses showed that CEBPB, FBXO32, FOXO3 and MYOD1 played key roles in growth. The functions of FBXO32 and FOXO3 were validated. FBXO32 was predominantly expressed in leg muscle, heart and breast muscle. After decreased FBXO32 expression, growth-related genes such as PDK4, IGF2R and IGF2BP3 were significantly down-regulated (P < 0.05). FBXO32 was significantly (P < 0.05) associated with carcass and meat quality traits, but not growth traits. FOXO3 was predominantly expressed in breast and leg muscle. In both of these tissues, the FOXO3 mRNA level in XH was significantly higher than that in WRR chickens with normal body weight (P < 0.05). In DF-1 cells, siRNA knockdown of FOXO3 significantly (P < 0.01) inhibited the MYOD expression and significantly up-regulated (P < 0.01 or P < 0.05) the expression of growth-related genes including CEBPB, FBXO32, GH, GHR, IGF1R, IGF2R, IGF2BP1, IGF2BP3, INSR, PDK1 and PDK4. Moreover, 18 SNPs were identified in FOXO3. G66716193A was significantly (P < 0.05) associated with growth traits. The sites C66716002T, C66716195T and A66716179G were significantly (P < 0.05) associated with growth or carcass traits. These results demonstrated that FOXO3 is a candidate gene influencing chicken growth. Our observations provide new clues to understand the molecular basis of chicken growth.
doi_str_mv 10.1371/journal.pone.0137087
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However, the underlying genetic mechanisms are unclear. The objective of this study was to identify candidate genes associated with chicken growth and investigate their potential mechanisms. We used RNA-Seq to study the breast muscle transcriptome in high and low tails of Recessive White Rock (WRRh, WRRl) and Xinghua chickens (XHh, XHl). A total of 60, 23, 153 and 359 differentially expressed genes were detected in WRRh vs. WRRl, XHh vs. XHl, WRRh vs. XHh and WRRl vs. XHl, respectively. GO, KEGG pathway and gene network analyses showed that CEBPB, FBXO32, FOXO3 and MYOD1 played key roles in growth. The functions of FBXO32 and FOXO3 were validated. FBXO32 was predominantly expressed in leg muscle, heart and breast muscle. After decreased FBXO32 expression, growth-related genes such as PDK4, IGF2R and IGF2BP3 were significantly down-regulated (P < 0.05). FBXO32 was significantly (P < 0.05) associated with carcass and meat quality traits, but not growth traits. FOXO3 was predominantly expressed in breast and leg muscle. In both of these tissues, the FOXO3 mRNA level in XH was significantly higher than that in WRR chickens with normal body weight (P < 0.05). In DF-1 cells, siRNA knockdown of FOXO3 significantly (P < 0.01) inhibited the MYOD expression and significantly up-regulated (P < 0.01 or P < 0.05) the expression of growth-related genes including CEBPB, FBXO32, GH, GHR, IGF1R, IGF2R, IGF2BP1, IGF2BP3, INSR, PDK1 and PDK4. Moreover, 18 SNPs were identified in FOXO3. G66716193A was significantly (P < 0.05) associated with growth traits. The sites C66716002T, C66716195T and A66716179G were significantly (P < 0.05) associated with growth or carcass traits. These results demonstrated that FOXO3 is a candidate gene influencing chicken growth. Our observations provide new clues to understand the molecular basis of chicken growth.]]></description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0137087</identifier><identifier>PMID: 26366565</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agriculture ; Animal sciences ; Animals ; Avian Proteins - genetics ; Avian Proteins - metabolism ; Body weight ; Breast muscle ; Cell Line ; Chickens ; Chickens - genetics ; Chickens - growth &amp; development ; Chickens - metabolism ; DNA methylation ; Female ; Forkhead Transcription Factors - genetics ; Forkhead Transcription Factors - metabolism ; FOXO3 protein ; Functional analysis ; Gene expression ; Gene Expression Regulation, Developmental ; Genes ; Genetics ; Genome-Wide Association Study ; Genomes ; Genomics ; Growth hormone ; Insulin-like growth factor II receptors ; Leg ; Meat ; Muscle Proteins - genetics ; Muscle Proteins - metabolism ; Muscles ; Musculoskeletal system ; MyoD protein ; Oncorhynchus mykiss ; Polymorphism, Single Nucleotide ; Poultry ; Proteins ; Quantitative Trait Loci ; Ribonucleic acid ; RNA ; RNA, Messenger - analysis ; Sequence Analysis, RNA - methods ; Single-nucleotide polymorphism ; siRNA ; Studies ; Transcription factors ; Zoology</subject><ispartof>PloS one, 2015-09, Vol.10 (9), p.e0137087-e0137087</ispartof><rights>2015 Chen et al. 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However, the underlying genetic mechanisms are unclear. The objective of this study was to identify candidate genes associated with chicken growth and investigate their potential mechanisms. We used RNA-Seq to study the breast muscle transcriptome in high and low tails of Recessive White Rock (WRRh, WRRl) and Xinghua chickens (XHh, XHl). A total of 60, 23, 153 and 359 differentially expressed genes were detected in WRRh vs. WRRl, XHh vs. XHl, WRRh vs. XHh and WRRl vs. XHl, respectively. GO, KEGG pathway and gene network analyses showed that CEBPB, FBXO32, FOXO3 and MYOD1 played key roles in growth. The functions of FBXO32 and FOXO3 were validated. FBXO32 was predominantly expressed in leg muscle, heart and breast muscle. After decreased FBXO32 expression, growth-related genes such as PDK4, IGF2R and IGF2BP3 were significantly down-regulated (P < 0.05). FBXO32 was significantly (P < 0.05) associated with carcass and meat quality traits, but not growth traits. 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Our observations provide new clues to understand the molecular basis of chicken growth.]]></description><subject>Agriculture</subject><subject>Animal sciences</subject><subject>Animals</subject><subject>Avian Proteins - genetics</subject><subject>Avian Proteins - metabolism</subject><subject>Body weight</subject><subject>Breast muscle</subject><subject>Cell Line</subject><subject>Chickens</subject><subject>Chickens - genetics</subject><subject>Chickens - growth &amp; development</subject><subject>Chickens - metabolism</subject><subject>DNA methylation</subject><subject>Female</subject><subject>Forkhead Transcription Factors - genetics</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>FOXO3 protein</subject><subject>Functional analysis</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genes</subject><subject>Genetics</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Growth hormone</subject><subject>Insulin-like growth factor II receptors</subject><subject>Leg</subject><subject>Meat</subject><subject>Muscle Proteins - genetics</subject><subject>Muscle Proteins - metabolism</subject><subject>Muscles</subject><subject>Musculoskeletal system</subject><subject>MyoD protein</subject><subject>Oncorhynchus mykiss</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Poultry</subject><subject>Proteins</subject><subject>Quantitative Trait Loci</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Messenger - analysis</subject><subject>Sequence Analysis, RNA - methods</subject><subject>Single-nucleotide polymorphism</subject><subject>siRNA</subject><subject>Studies</subject><subject>Transcription factors</subject><subject>Zoology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptkl1v0zAUhiMEYmPwDxBY4oabFH87uUGqKlomTVQaILizHPtkdUnjYidD-_e4azZtiBt_HL_nOcf2WxSvCZ4RpsiHbRhjb7rZPvQwwzmEK_WkOCU1o6WkmD19sD4pXqS0xViwSsrnxQmVTEohxWkBc7SCPuyg_OEdoN3llzn6aiNAj0zv0HLs7eBDroPmebhJPqFLuIa8X65_rhkyCRm0yFLvzAAHFqA2RLTYePsrQ1Yx_Bk2L4tnrekSvJrms-L78tO3xefyYr06X8wvSiuoHMoGHFPWkYbSuuZKCQ6ONsQ4yhxuG-IcsxRUzVzV1FhSIYCypjHQWseFceyseHvk7ruQ9PRCSRNFaloJxllWnB8VLpit3ke_M_FGB-P1bSDEK23i4G0HuiUtF7bG0LaCu1oaJa2BhlsgnIM6sD5O1cZmB85CP0TTPYI-Pun9Rl-Fa82FzD9TZcD7CRDD7xHSoHc-Weg600MYb_umqiJY8Sx994_0_7fjR5WNIaUI7X0zBOuDa-6y9ME1enJNTnvz8CL3SXc2YX8B6fLAIA</recordid><startdate>20150914</startdate><enddate>20150914</enddate><creator>Chen, Biao</creator><creator>Xu, Jiguo</creator><creator>He, Xiaomei</creator><creator>Xu, Haiping</creator><creator>Li, Guihuan</creator><creator>Du, Hongli</creator><creator>Nie, Qinghua</creator><creator>Zhang, Xiquan</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150914</creationdate><title>A Genome-Wide mRNA Screen and Functional Analysis Reveal FOXO3 as a Candidate Gene for Chicken Growth</title><author>Chen, Biao ; 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However, the underlying genetic mechanisms are unclear. The objective of this study was to identify candidate genes associated with chicken growth and investigate their potential mechanisms. We used RNA-Seq to study the breast muscle transcriptome in high and low tails of Recessive White Rock (WRRh, WRRl) and Xinghua chickens (XHh, XHl). A total of 60, 23, 153 and 359 differentially expressed genes were detected in WRRh vs. WRRl, XHh vs. XHl, WRRh vs. XHh and WRRl vs. XHl, respectively. GO, KEGG pathway and gene network analyses showed that CEBPB, FBXO32, FOXO3 and MYOD1 played key roles in growth. The functions of FBXO32 and FOXO3 were validated. FBXO32 was predominantly expressed in leg muscle, heart and breast muscle. After decreased FBXO32 expression, growth-related genes such as PDK4, IGF2R and IGF2BP3 were significantly down-regulated (P < 0.05). FBXO32 was significantly (P < 0.05) associated with carcass and meat quality traits, but not growth traits. FOXO3 was predominantly expressed in breast and leg muscle. In both of these tissues, the FOXO3 mRNA level in XH was significantly higher than that in WRR chickens with normal body weight (P < 0.05). In DF-1 cells, siRNA knockdown of FOXO3 significantly (P < 0.01) inhibited the MYOD expression and significantly up-regulated (P < 0.01 or P < 0.05) the expression of growth-related genes including CEBPB, FBXO32, GH, GHR, IGF1R, IGF2R, IGF2BP1, IGF2BP3, INSR, PDK1 and PDK4. Moreover, 18 SNPs were identified in FOXO3. G66716193A was significantly (P < 0.05) associated with growth traits. The sites C66716002T, C66716195T and A66716179G were significantly (P < 0.05) associated with growth or carcass traits. These results demonstrated that FOXO3 is a candidate gene influencing chicken growth. Our observations provide new clues to understand the molecular basis of chicken growth.]]></abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26366565</pmid><doi>10.1371/journal.pone.0137087</doi><oa>free_for_read</oa></addata></record>
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subjects Agriculture
Animal sciences
Animals
Avian Proteins - genetics
Avian Proteins - metabolism
Body weight
Breast muscle
Cell Line
Chickens
Chickens - genetics
Chickens - growth & development
Chickens - metabolism
DNA methylation
Female
Forkhead Transcription Factors - genetics
Forkhead Transcription Factors - metabolism
FOXO3 protein
Functional analysis
Gene expression
Gene Expression Regulation, Developmental
Genes
Genetics
Genome-Wide Association Study
Genomes
Genomics
Growth hormone
Insulin-like growth factor II receptors
Leg
Meat
Muscle Proteins - genetics
Muscle Proteins - metabolism
Muscles
Musculoskeletal system
MyoD protein
Oncorhynchus mykiss
Polymorphism, Single Nucleotide
Poultry
Proteins
Quantitative Trait Loci
Ribonucleic acid
RNA
RNA, Messenger - analysis
Sequence Analysis, RNA - methods
Single-nucleotide polymorphism
siRNA
Studies
Transcription factors
Zoology
title A Genome-Wide mRNA Screen and Functional Analysis Reveal FOXO3 as a Candidate Gene for Chicken Growth
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