Integrating Single-Step GWAS and Bipartite Networks Reconstruction Provides Novel Insights into Yearling Weight and Carcass Traits in Hanwoo Beef Cattle
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Phenotypic and Pedigree Data
2.3. Genotypic Data
2.4. Analysis of the Single-Step Genomic Association
2.5. Selection of Relevant SNP Windows and Putative Candidate Genes Identification
2.6. Functional Gene Set Annotation and Enrichment
2.7. Target Gene Prediction and Validation of Candidate miRNAs
2.8. Gene-Traits and miRNA–Gene Network Reconstruction
3. Results
3.1. Summary Statistics
3.2. Association Analysis
3.3. Functional Gene Set Annotation and Enrichment
3.4. Prediction of miRNA-Target Genes
3.5. Gene-Traits and miRNA–Gene Network Reconstruction
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Trait (Units) | Number of Animals with Record (and Genotype) | Mean (SE) | Min. | Max. | SD | CV% |
---|---|---|---|---|---|---|
BT (mm) | 5824 (1151) | 8.71 (0.05) | 1.00 | 30.00 | 3.71 | 42.61 |
CW (kg) | 5824 (1151) | 343.96 (0.60) | 158.00 | 519.00 | 45.61 | 13.26 |
EMA (cm2) | 5821 (1151) | 78.90 (0.12) | 40.00 | 123.00 | 9.12 | 11.56 |
MS (score) | 3991 (1151) | 3.33 (0.03) | 1.00 | 9.00 | 1.61 | 48.46 |
YW (kg) | 15,279 (1540) | 342.06 (0.38) | 133.86 | 535.90 | 47.48 | 13.88 |
Trait a | Chr b | QTL Region (Mb) c | GV% d | Candidate Genes e |
---|---|---|---|---|
BT | 2 | 0.35–1.28 | 2.16 | LOC104971094, LOC107132231, LOC107132232, LOC784948, LGSN, OCA2, LOC783772, LOC100301143, HERC2, LOC104971093, TRNAE-CUC, NIPA1, NIPA2, LOC107132230, CYFIP1, TUBGCP5, TRNAE-UUC, CCDC115, IMP4, PTPN18 |
BT | 2 | 72.46–73.83 | 1.11 | INHBB, LOC781979, LOC104971258, GLI2, LOC104971259, LOC100335292, TRNAL-CAA, TFCP2L1, CLASP1, NIFK, TSN |
BT | 7 | 39.69–40.83 | 2.59 | HK3, UIMC1, LOC510252, LOC100141185, LOC101905975, LOC784341, LOC533921, LOC782447, TRNAR-CCU, ZNF346, FGFR4, LOC100336707, LOC540197, RAB24, PRELID1, MXD3, LMAN2, RGS14, SLC34A1, PFN3, F12, GRK6, PRR7, DBN1, PDLIM7, DOK3, LOC104969157, DDX41, FAM193B, LOC509184, LOC100139419, TMED9, B4GALT7, LOC107132625, N4BP3, RMND5B, LOC101905866, NHP2, HNRNPAB, PHYKPL, COL23A1 |
BT | 11 | 60.34–61.55 | 1.69 | FAM161A, CCT4, COMMD1, B3GNT2, TMEM17, EHBP1, OTX1 |
BT | 13 | 40.02–41.40 | 1.08 | CFAP61, INSM1, RALGAPA2, LOC104973781, LOC104973782, KIZ, LOC100140493, XRN2, NKX2-4, NKX2-2, LOC614124, PAX1 |
BT | 16 | 34.80–35.91 | 1.08 | LOC100297170, PLD5, LOC104974409, LOC104974410, BECN2, MAP1LC3C, EXO1, WDR64, LOC101907876 |
CW | 7 | 58.66–60.49 | 1.91 | PRELID2, LOC107132647, LOC100138092, LOC788619, GRXCR2, SH3RF2, PLAC8L1, LARS, RBM27, POU4F3, TCERG1, GPR151, PPP2R2B, TRNAC-GCA, STK32A |
CW | 9 | 62.93–64.58 | 1.98 | TRNAE-UUC, LOC100336843, AKIRIN2, ORC3, RARS2, SLC35A1, CFAP206, C9H6orf163, SMIM8, LOC104969583, GJB7, LOC107132774, ZNF292, LOC509829, CGA, HTR1E |
CW | 14 | 11.23–12.26 | 1.04 | ASAP1, FAM49B, GSDMC |
CW | 14 | 16.55–17.80 | 4.46 | NSMCE2, KIAA0196, SQLE, ZNF572, MTSS1, NDUFB9, TATDN1, LOC104968469, RNF139, TRMT12, LOC531462, TMEM65, FER1L6, LOC101907615, FAM91A1, ANXA13 |
CW | 14 | 17.85–19.46 | 2.00 | LOC100848930, FBXO32, WDYHV1, ATAD2, ZHX1, C14H8orf76, FAM83A, TRNAM-CAU, LOC104974006, TBC1D31, DERL1, ZHX2, LOC104974007, LOC100139328 |
CW | 14 | 22.09–23.61 | 4.31 | SNTG1, LOC614437, PCMTD1, LOC101906226, LOC104974020, ST18, LOC100141260, LOC101906592, FAM150A, RB1CC1, LOC104974017, NPBWR1, OPRK1, ATP6V1H, RGS20 |
CW | 14 | 24.58–25.33 | 17.66 | XKR4, TMEM68, TGS1, LYN, RPS20, MOS, PLAG1, CHCHD7, SDR16C5, SDR16C6, PENK, LOC101907667 |
CW | 14 | 25.36–26.15 | 2.43 | LOC101907667, IMPAD1, FAM110B |
CW | 14 | 29.43–30.44 | 3.75 | NKAIN3, LOC107133118, GGH, TTPA, YTHDF3, LOC101907975 |
CW | 14 | 30.54–32.16 | 1.30 | MIR124A-2, BHLHE22, CYP7B1, LOC104974032, ARMC1, MTFR1, LOC104974034, PDE7A, LOC101902754, LOC100299601, LOC104974036, DNAJC5B, TRNAY-GUA, TRNAA-AGC, TRIM55 |
CW | 14 | 32.25–33.90 | 1.43 | CRH, LOC790324, ZSCAN5B, RRS1, ADHFE1, C14H8orf46, MYBL1, VCPIP1, SGK3, LOC104974037, MCMDC2, LOC784087, LOC100847363, TCF24, PPP1R42, COPS5, CSPP1, ARFGEF1, TRNAC-GCA, CPA6, LOC101902584 |
EMA | 1 | 127.77–128.74 | 2.27 | GK5, TFDP2, LOC101903974, LOC511302, ATP1B3, GRK7, RNF7, LOC104968752, RASA2, LOC100294923, ZBTB38, LOC107131348, LOC104971030, LOC104971031, PXYLP1, LOC104971032 |
EMA | 6 | 0.1–1.03 | 1.00 | APELA, LOC101905490, LOC513842, LOC101907917 |
EMA | 6 | 54.52–55.64 | 1.11 | NOT_FOUND |
EMA | 9 | 57.18–58.10 | 2.22 | TRNAC-ACA, LOC782527, EPHA7 |
EMA | 14 | 22.09–23.61 | 1.75 | SNTG1, LOC614437, PCMTD1, LOC101906226, LOC104974020, ST18, LOC100141260, LOC101906592, FAM150A, RB1CC1, LOC104974017, NPBWR1, OPRK1, ATP6V1H, RGS20 |
EMA | 14 | 24.58–25.33 | 7.98 | XKR4, TMEM68, TGS1, LYN, RPS20, MOS, PLAG1, CHCHD7, SDR16C5, SDR16C6, PENK, LOC101907667 |
EMA | 19 | 48.90–50.02 | 1.00 | LOC100140873, TEX2, TRNAG-UCC, LOC104975109, LOC101902037, PECAM1, MILR1, POLG2, DDX5, MIR3064, CEP95, SMURF2, TRNAE-CUC, KPNA2, TRNAR-CCG, C19H17orf58, BPTF, TRNAE-UUC, NOL11, TRNAS-AGA, PITPNC1, LOC101905668 |
MS | 5 | 95.87–97.74 | 2.24 | ATF7IP, LOC100139060, GRIN2B, EMP1, GSG1, FAM234B, HEBP1, GPRC5D, GPRC5A, DDX47, APOLD1, CDKN1B, LOC101901926, GPR19, CREBL2, LOC101902028, LOC107132517, DUSP16 |
MS | 14 | 5.01–5.69 | 1.00 | LOC100850800, COL22A1, FAM135B |
MS | 23 | 30.27–31.28 | 2.03 | ZNF389, ZSCAN16, ZNF165, OR2B6, HIST1H2BB, HIST1H2AG, bta-mir-2379, ZNF184, ZNF391, POM121L2, PRSS16, HIST1H2BN, ZNF322, ABT1 |
MS | 27 | 16.11–17.15 | 1.28 | LOC101905556, LOC101905700, ZFP42, TRNAG-UCC, TRIML2, TRNAF-AAA, TRIML1, LOC507011 |
MS | 27 | 19.17–20.48 | 1.46 | MICU3, FGF20, LOC104976064, TRNAC-ACA, MSR1, LOC104976066, TUSC3 |
YW | 2 | 42.77–43.75 | 1.71 | LOC785568, LOC615401, ARL6IP6, TRNAY-GUA, PRPF40A, FMNL2, LOC101902790 |
YW | 6 | 37.26–38.45 | 1.36 | FAM13A, LOC104972724, LOC100847719, HERC3, NAP1L5, PYURF, PIGY, HERC5, HERC6, PPM1K, ABCG2, LOC781421, PKD2, SPP1, MEPE, IBSP, LOC104972726 |
YW | 6 | 39.50–40.67 | 2.68 | LOC782905 |
YW | 6 | 44.67–45.42 | 1.14 | PPARGC1A |
YW | 6 | 48.80–49.97 | 2.30 | LOC107132565 |
YW | 10 | 50.75–51.96 | 1.56 | LOC107132854, FAM81A, MYO1E, CCNB2, RNF111, SLTM, FAM63B, LOC533308, ADAM10, LIPC, LOC101904602, LOC101903685, TRNAE-UUC |
YW | 14 | 16.55–17.80 | 1.70 | NSMCE2, KIAA0196, SQLE, ZNF572, MTSS1, NDUFB9, TATDN1, LOC104968469, RNF139, TRMT12, LOC531462, TMEM65, FER1L6, LOC101907615, FAM91A1, ANXA13 |
YW | 14 | 22.09–23.61 | 2.54 | SNTG1, LOC614437, PCMTD1, LOC101906226, LOC104974020, ST18, LOC100141260, LOC101906592, FAM150A, RB1CC1, LOC104974017, NPBWR1, OPRK1, ATP6V1H, RGS20 |
YW | 14 | 24.58–25.33 | 9.96 | XKR4, TMEM68, TGS1, LYN, RPS20, MOS, PLAG1, CHCHD7, SDR16C5, SDR16C6, PENK, LOC101907667 |
YW | 14 | 25.36–26.15 | 1.74 | LOC101907667, IMPAD1, FAM110B |
YW | 14 | 29.43–30.44 | 2.64 | NKAIN3, LOC107133118, GGH, TTPA, YTHDF3, LOC101907975 |
YW | 14 | 30.54–32.16 | 2.62 | MIR124A-2, BHLHE22, CYP7B1, LOC104974032, ARMC1, MTFR1, LOC104974034, PDE7A, LOC101902754, LOC100299601, LOC104974036, DNAJC5B, TRNAY-GUA, TRNAA-AGC, TRIM55 |
YW | 14 | 32.25–33.90 | 1.43 | CRH, LOC790324, ZSCAN5B, RRS1, ADHFE1, C14H8orf46, MYBL1, VCPIP1, SGK3, LOC104974037, MCMDC2, LOC784087, LOC100847363, TCF24, PPP1R42, COPS5, CSPP1, ARFGEF1, TRNAC-GCA, CPA6, LOC101902584 |
Traits a | Term ID | Term Name | Genes | p-Value |
---|---|---|---|---|
BT | GO:0006869 | lipid transport | PRELID1 | 0.010233961 |
GO:0010876 | lipid localization | PRELID1 | 0.014172362 | |
GO:0005319 | lipid transporter activity | PRELID1 | 0.019846208 | |
GO:0006629 | lipid metabolic process | FGFR4 | 0.025006995 | |
GO:0008289 | lipid binding | COMMD1, PFN3 | 0.047311441 | |
GO:0008610 | lipid biosynthetic process | FGFR4 | 0.035303187 | |
KEGG:04015 | Rap1 signaling pathway | RGS14 | 0.047961872 | |
CW | GO:0001558 | regulation of cell growth | SGK3 | 0.044446017 |
GO:0007173 | epidermal growth factor receptor signaling pathway | FAM83A | 0.039752933 | |
GO:0016049 | cell growth | POU4F3 | 0.035059849 | |
GO:0035264 | multicellular organism growth | PLAG1 | 0.030366765 | |
GO:0035265 | organ growth | PLAG1, CGA | 0.025673681 | |
GO:0040007 | growth | PLAG1, POU4F3, CGA, SGK3 | 0.020980597 | |
GO:0048589 | developmental growth | PLAG1, POU4F3, CGA | 0.016287514 | |
GO:0060560 | developmental growth involved in morphogenesis | POU4F3 | 0.01159443 | |
GO:0005515 | protein binding | ARFGEF1, ATAD2, LYN, MYBL1, RB1CC1, AKIRIN2, CRH, CGA, NPBWR1, PENK, PPP1R42, RGS20, TCERG1, ZHX1, ZHX2 | 0.006901346 | |
KEGG:04080 | Neuroactive ligand-receptor interaction | CGA, HTR1E, NPBWR1, OPRK1, PENK, CRH | 0.039862933 | |
EMA | GO:0006629 | lipid metabolic process | LYN, SDR16C5 | 0.049805624 |
GO:0019216 | regulation of lipid metabolic process | LYN | 0.042803519 | |
GO:0033993 | response to lipid | DDX5 | 0.043747312 | |
GO:0008289 | lipid binding | TEX2 | 0.049508111 | |
KEGG:04514 | Cell adhesion molecules | LOC100140873, PECAM1 | 0.04067771 | |
REAC:R-BTA-210990 | PECAM1 interactions | LYN, PECAM1 | 0.049805624 | |
MS | GO:0006629 | lipid metabolic process | CREBL2 | 0.01889403 |
GO:0006869 | lipid transport | APOLD1, MSR1 | 0.041826385 | |
GO:0008610 | lipid biosynthetic process | CREBL2 | 0.021157549 | |
GO:0010876 | lipid localization | APOLD1 | 0.016791777 | |
GO:0019915 | lipid storage | MSR1 | 0.025742261 | |
GO:0045444 | fat cell differentiation | CREBL2 | 0.019486141 | |
GO:0008289 | lipid transport | APOLD1 | 0.017945142 | |
GO:0071814 | protein-lipid complex binding | MSR1 | 0.016404143 | |
KEGG:04010 | MAPK signaling pathway | DUSP16, FGF20 | 0.014863145 | |
REAC:R-BTA-5673001 | RAF/MAP kinase cascade | DUSP16, FGF20, GRIN2B | 0.016791777 | |
YW | GO:0001558 | regulation of cell growth | ADAM10, SGK3 | 0.046130564 |
GO:0016049 | cell growth | ADAM10 | 0.043928692 | |
GO:0035264 | multicellular organism growth | PLAG1 | 0.04172682 | |
GO:0035265 | organ growth | PLAG1 | 0.039524949 | |
GO:0040007 | growth | ADAM10, PLAG1, SGK3 | 0.037323077 | |
GO:0040008 | regulation of growth | ADAM10, SGK3, MYO1E | 0.035121205 | |
GO:0048589 | developmental growth | PLAG1 | 0.032919333 | |
GO:0070848 | response to growth factor | IBSP, RNF111 | 0.030717462 | |
GO:0071363 | cellular response to growth factor stimulus | RNF111 | 0.02851559 | |
GO:0005515 | protein binding | ADAM10, ARFGEF1, LYN, MYBL1, PPARGC1A, RB1CC1, CRH, MEPE, NPBWR1, PKD2, PENK, PPP1R24, RGS20, SPP1 | 0.026313718 | |
GO:0140096 | catalytic activity, acting on a protein | ADAM10, CCNB2, COPS5, CPA6, GGH, HERC3, HERC5, HERC6, LYN, MOS, PCMTD1, PPM1K, RNF111, RNF139, SGK3, VCPIP1, NSMCE2 | 0.048130564 |
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Naserkheil, M.; Bahrami, A.; Lee, D.; Mehrban, H. Integrating Single-Step GWAS and Bipartite Networks Reconstruction Provides Novel Insights into Yearling Weight and Carcass Traits in Hanwoo Beef Cattle. Animals 2020, 10, 1836. https://doi.org/10.3390/ani10101836
Naserkheil M, Bahrami A, Lee D, Mehrban H. Integrating Single-Step GWAS and Bipartite Networks Reconstruction Provides Novel Insights into Yearling Weight and Carcass Traits in Hanwoo Beef Cattle. Animals. 2020; 10(10):1836. https://doi.org/10.3390/ani10101836
Chicago/Turabian StyleNaserkheil, Masoumeh, Abolfazl Bahrami, Deukhwan Lee, and Hossein Mehrban. 2020. "Integrating Single-Step GWAS and Bipartite Networks Reconstruction Provides Novel Insights into Yearling Weight and Carcass Traits in Hanwoo Beef Cattle" Animals 10, no. 10: 1836. https://doi.org/10.3390/ani10101836