Transcriptome Analysis of Breast Muscle Reveals Pathways Related to Protein Deposition in High Feed Efficiency of Native Turkeys
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethical Approval Statements
2.2. Selecting Animals and Sampling
2.3. RNA Extraction and Sequencing
2.4. RNA-Seq Analysis
2.5. Identification of Differently Expressed Genes (DEGs) and Function Annotation Analysis
2.6. Gene Set Enrichment Analysis (GSEA)
2.7. Quantitative RT-PCR Confirmations
3. Results
Gene Expression Profile
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Gene Name | Accession Number | Sequence of Primers (5′ → 3′) * | Product Length (bp) | |
---|---|---|---|---|
GATM | XM_019619468 | Forward | CGTTTAATATCATTGGACCTGG | 216 |
Reverse | TTGAAGTCTCATTGGCATCG | |||
GNMT | XM_010706618 | Forward | CTGGAGCAGGACCTGGAGAAG | 246 |
Reverse | CTTGGTCAGGTCGCTCTTGTAG | |||
KRAS | NM_001303223 | Forward | CTGAAGATGTCCCAATGGTGCT | 182 |
Reverse | GTGTTTTCTGATTCTCGAACTAATG | |||
MAT1A | XM_003207784 | Forward | ATGCCAAAGTTGCTTGTGAGAC | 192 |
Reverse | GTGATTGCTGTTCCAGTGCCA | |||
CAV3 | XM_003210208 | Forward | CAAAGCGGATCAACGAAGAC | 200 |
Reverse | GATGAGGGCGAAGAGGAAGC | |||
MYOZ2 | XM_003205713 | Forward | CACAACGAAACAGTACGCAAGG | 196 |
Reverse | TGGGTGAGACTCAATACAATGAG | |||
MUSK | XM_010726142 | Forward | GAATATAACCAGGACTTGCTACAG | 164 |
Reverse | CAGTAATTCTCAGCATCAGACAG | |||
SMTN | XM_010720500 | Forward | GACAGGCAGCATCTTTGACC | 135 |
Reverse | CTGTGAGGTTGATGTCTTGGG | |||
MAP2K6 | XM_010721466 | Forward | TTTAGCAACCGAGTCAACGA | 105 |
Reverse | TTTAGCAACCGAGTCAACGA | |||
ALG6 | XM_003208901 | Forward | CAAGAAGGGACTGAAAGGAAAGG | 169 |
Reverse | CTACTTTATCCTCAAACAAGCCTC | |||
MTHFD2 | XM_003206271 | Forward | TCATAAAGAGAACAGGCATCCCA | 154 |
Reverse | TAACGGTGTGATATTGTGACTGTG | |||
CD36 | XM_010726962 | Forward | CCAGGAAGCTCTGTTTACAGG | 121 |
Reverse | TATCGCACCCTATATGTGTAAGGT | |||
APP | XM_010722443 | Forward | GAAGTTGTCAGAGTCCCTACC | 173 |
Reverse | TTCTGCCTCCTCCCATTCTC | |||
AGO2 | XM_031552935 | Forward | TGGAAGAGATAAAGTGGAGTGGA | 156 |
Reverse | CTGGATGGTTTCAAATGGGAC | |||
ACAT2 | XM_003204090 | Forward | AGGAAAGCTATTGACAAAGCCA | 186 |
Reverse | CAAGGATGCGACAACCAGAG | |||
DLL1 | XM_031552428 | Forward | CTTGTGCTAATGGAGCCCAG | 196 |
Reverse | GCAGTTCTTCCCGTTGTATCC | |||
WIPI1 | XM_010721504 | Forward | CAGGTTATTCGGAGGATGGT | 118 |
Reverse | ACGGCACAAGATTATAGGAGGA | |||
ASNS | XM_019616348 | Forward | ATATTTCCATAAGGCACCATCTCC | 159 |
Reverse | GTAAGAAGTAAGCGATGATCCAG | |||
SRC | XM_003211956 | Forward | CAGCAAGAGCAAACCCAAAGA | 103 |
Reverse | CTTGTTGGGGGTCTGCGAG | |||
EIF2AK3 | XM_010710584 | Forward | GAGTCAAGACCCTGAGCGATGT | 178 |
Reverse | GGTTTGGCTGGGAGTTCCA | |||
18S | AJ419877 | Forward | CTGCCCTATCAACTTTCGATGG | 171 |
Reverse | GGATGTGGTAGCCGTTTCTCA | |||
GAPDH | NM_001303179 | Forward | CCCAGAACATCATCCCAGCAT | 137 |
Reverse | ACGGCAGGTCAGGTCAACAAC | |||
RPS7 | NM_001285787 | Forward | TGAAGTAGGTGGTGGCAGGAA | 165 |
Reverse | CTCGTTGGCTTGGGCAGAA |
Sample | Raw Reads | Trimmed Reads | Mapped Ratio (%) |
---|---|---|---|
H1 | 71,407,390 | 71,397,082 | 74.56 |
H2 | 81,000,062 | 80,986,086 | 72.76 |
H3 | 80,467,686 | 80,451,478 | 74.25 |
L1 | 93,253,472 | 93,235,602 | 74.56 |
L2 | 75,960,342 | 75,946,338 | 73.1 |
L3 | 69,196,190 | 69,186,026 | 74.63 |
Term | Biological Process | Count | p-Value | Genes |
---|---|---|---|---|
Up-regulated | ||||
mgp00260 | Glycine, serine, and threonine metabolism | 6 | 1.64 × 10−5 | GATM, PHGDH, GNMT, PSPH, PSAT1, LOC100550886 |
mgp01230 | Biosynthesis of amino acids | 5 | 0.001 | MAT1A, PHGDH, PSPH, PSAT1, LOC100550886 |
mgp04920 | Adipocytokine signaling pathway | 5 | 0.0022 | CD36, ACSBG2, AMPK, ACC2, ADIPOQ |
mgp01100 | Metabolic pathways | 17 | 0.021 | POLR3H, GATM, ACSBG2, ASNS, ALG6, ACC2, PSPH, ACAT2, PMM2, PMM1, MTHFD2, MAT1A, PHGDH, PSAT1, DCXR, DHCR24, LOC100550886 |
Down-regulated | ||||
mgp04320 | Dorso-ventral axis formation | 4 | 0.002 | KRAS, CPEB3, ETS2, CPEB4 |
mgp04810 | Regulation of actin cytoskeleton | 7 | 0.022 | ENAH, PIKFYVE, MRAS, SRC, MSN, KRAS, NCKAP1L |
Term | Biological Process | Count | p-Value | Genes |
---|---|---|---|---|
GO:0006564 | L-serine biosynthetic process | 3 | 3.09 × 10−4 | PHGDH, PSPH, PSAT1 |
GO:0009298 | GDP-mannose biosynthetic process | 2 | 0.03 | PMM2, PMM1 |
GO:0048630 | skeletal muscle tissue growth | 2 | 0.03 | DLL1, CHRND |
GO:1990000 | amyloid fibril formation | 2 | 0.03 | APP, CD36 |
GO:0034383 | low-density lipoprotein particle clearance | 2 | 0.03 | CD36, ADIPOQ |
GO:0010881 | regulation of cardiac muscle contraction by regulation of the release of sequestered calcium ion | 2 | 0.03 | PLN, FKBP1B |
GO:0051289 | protein homotetramerization | 3 | 0.033 | GNMT, ACC2, DCXR |
GO:0010459 | negative regulation of heart rate | 2 | 0.04 | PLN, FKBP1B |
Cellular component | ||||
GO:0005615 | extracellular space | 9 | 0.033 | CPNE9, MTHFD2, APP, CD36, IGFBP7, ANGPTL1, SPON2, ADIPOQ, ANGPT4 |
GO:0033017 | sarcoplasmic reticulum membrane | 2 | 0.039 | PLN, FKBP1B |
GO:0070062 | extracellular exosome | 21 | 0.046 | CPNE9, SPON2, APP, SLC20A2, DCXR, PMM2, ADIPOQ, ACOT11, SEMA3G, SLC1A4, ACAT2, MYLK, GATM, TP53I3, BAIAP2L1, LOC100551072, PSAT1, PHGDH, IGFBP7, ANGPTL1, DDR2 |
GO:0030018 | Z disc | 3 | 0.0498 | ITGB1BP2, MYOZ2, FKBP1B |
Molecular function | ||||
GO:0004615 | phosphomannomutase activity | 2 | 0.02 | PMM2, PMM1 |
Term | Biological Process | Count | p-Value | Genes |
---|---|---|---|---|
GO:0035914 | skeletal muscle cell differentiation | 6 | 4.41× 10−5 | BTG2, MYF6, HIVEP3, FOXN2, ATF3, BCL9L |
GO:0050731 | positive regulation of peptidyl-tyrosine phosphorylation | 5 | 0.003 | CD74, SRC, ABL1, ENPP2, RICTOR |
GO:0060213 | positive regulation of nuclear-transcribed mRNA poly(A) tail shortening | 3 | 0.0083 | BTG2, AGO2, CPEB3 |
GO:0000122 | negative regulation of transcription from RNA polymerase II promoter | 10 | 0.0086 | PLK3, ZFHX3, MYOCD, NR4A3, TRPS1, NRIP1, OTUD7B, CPEB3, HDAC9, BARX2 |
GO:0045944 | positive regulation of transcription from RNA polymerase II promoter | 12 | 0.0106 | RPS6KA3, MLLT10, SBNO2, ATXN7, NRIP1, AGO2, TET2, NFATC1, ETS2, BCL9L, ARNTL, FOSL2 |
GO:0048536 | spleen development | 3 | 0.0252 | TET2, ABL1, JARID2 |
GO:0070374 | positive regulation of ERK1 and ERK2 cascade | 5 | 0.0273 | CD74, SRC, ABL1, RAPGEF2, NOX4 |
GO:0048008 | platelet-derived growth factor receptor signaling pathway | 3 | 0.0287 | CSRNP1, ZFAND5, ARID5B |
GO:0009791 | post-embryonic development | 4 | 0.03 | CSRNP1, AGO2, TET2, ARID5B |
GO:0030968 | endoplasmic reticulum unfolded protein response | 3 | 0.04 | STC2, EIF2AK3, ATF3 |
GO:0048705 | skeletal system morphogenesis | 3 | 0.049 | CSRNP1, ZFAND5, ARID5B |
Term | Cellular Component | |||
GO:0005634 | Nucleus | 31 | 0.001 | CSRNP1, CCNJ, SRC, NAB1, CELF2, NEDD9, TNFAIP3, OTUD7B, ABHD5, UACA, BACH1, BARX2, NR3C2, NFIL3, SERTAD2, NFKBIZ, HIVEP3, SKIL, MYOCD, ARID5B, MSN, BTBD7, FOXN2, PISD, NR4A3, ALOX5AP, AGO2, MYF6, NOX4, CPEB3, CPEB4 |
GO:0005667 | transcription factor complex | 7 | 0.0025 | ZFHX3, NR4A3, HDAC9, SKIL, BARX2, ETS2, ARNTL |
GO:0005730 | Nucleolus | 13 | 0.013 | PLK3, ZFHX3, DDX24, NUP153, STON2, PPM1E, BTBD10, NOL6, NRIP1, ABL1, KDM7A, ATF3, BCL9L |
Term | Molecular function | |||
GO:0001078 | transcriptional repressor activity, RNA polymerase II core promoter proximal region sequence-specific binding | 7 | 9.69E-05 | NFIL3, AEBP2, ZNF536, BACH1, SKIL, ATF3, ETS2 |
GO:0043565 | sequence-specific DNA binding | 8 | 0.0059 | CSRNP1, ZFHX3, TRPS1, FOXN2, SKIL, ETS2, CREB5, NR3C2 |
GO:0000978 | RNA polymerase II core promoter proximal region sequence-specific DNA binding | 8 | 0.009 | ELF1, NR4A3, AEBP2, IRF1, ZNF536, SKIL, ATF3, ETS2 |
GO:0003713 | transcription coactivator activity | 6 | 0.01 | MYOCD, MAML1, SERTAD2, JMY, NRIP1, ARID5B |
GO:0008270 | zinc ion binding | 18 | 0.02 | ZFHX3, ANKIB1, ZFAND5, TET2, TNFAIP3, OTUD7B, NUP153, NR3C2, MLLT10, PIKFYVE, NR4A3, TRAF3, TRPS1, DHX58, ENPP2, HIVEP3, LONRF2, KDM7A |
GO:0046872 | metal ion binding | 13 | 0.028 | ZBTB21, ZBTB44, PPM1E, HDAC9, ZC3H12C, PDE10A, PDP2, AEBP2, MB, ZNF536, PRKCQ, ZNF644, PDE7B |
GO:0003700 | transcription factor activity, sequence-specific DNA binding | 7 | 0.035 | TRPS1, NFATC1, FOXN2, CREB5, ARNTL, FOSL2, NR3C2 |
KEGG Set | SIZE | NES | p-Value | FDR Q-Value | Higher Expression |
---|---|---|---|---|---|
KEGG_GLYCINE_SERINE_AND_THREONINE_METABOLISM | 20 | 1.66 | 0 | 0.194 | HFE |
KEGG_RIG_I_LIKE_RECEPTOR_SIGNALING_PATHWAY | 33 | −1.85395 | 0 | 0.046 | LFE |
KEGG_JAK_STAT_SIGNALING_PATHWAY | 70 | −1.51451 | 0 | 0.188488 | LFE |
KEGG_DORSO_VENTRAL_AXIS_FORMATION | 15 | −1.46771 | 0 | 0.19519 | LFE |
KEGG_NOD_LIKE_RECEPTOR_SIGNALING_PATHWAY | 30 | −1.42309 | 0 | 0.200888 | LFE |
KEGG_WNT_SIGNALING_PATHWAY | 96 | −1.4685 | 0 | 0.202649 | LFE |
KEGG_NATURAL_KILLER_CELL_MEDIATED_CYTOTOXICITY | 54 | −1.43289 | 0 | 0.205478 | LFE |
KEGG_NEUROTROPHIN_SIGNALING_PATHWAY | 92 | −1.4886 | 0 | 0.205977 | LFE |
KEGG_PROGESTERONE_MEDIATED_OOCYTE_MATURATION | 57 | −1.48398 | 0 | 0.206473 | LFE |
KEGG_FC_EPSILON_RI_SIGNALING_PATHWAY | 49 | −1.49622 | 0 | 0.210286 | LFE |
KEGG_MAPK_SIGNALING_PATHWAY | 163 | −1.51628 | 0 | 0.212236 | LFE |
KEGG_HEDGEHOG_SIGNALING_PATHWAY | 33 | −1.44312 | 0 | 0.215766 | LFE |
KEGG_TOLL_LIKE_RECEPTOR_SIGNALING_PATHWAY | 51 | −1.52378 | 0 | 0.238885 | LFE |
KEGG_B_CELL_RECEPTOR_SIGNALING_PATHWAY | 48 | −1.51919 | 0 | 0.241404 | LFE |
KEGG_GNRH_SIGNALING_PATHWAY | 61 | −1.38625 | 0 | 0.246314 | LFE |
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Pezeshkian, Z.; Mirhoseini, S.Z.; Ghovvati, S.; Ebrahimie, E. Transcriptome Analysis of Breast Muscle Reveals Pathways Related to Protein Deposition in High Feed Efficiency of Native Turkeys. Animals 2022, 12, 1240. https://doi.org/10.3390/ani12101240
Pezeshkian Z, Mirhoseini SZ, Ghovvati S, Ebrahimie E. Transcriptome Analysis of Breast Muscle Reveals Pathways Related to Protein Deposition in High Feed Efficiency of Native Turkeys. Animals. 2022; 12(10):1240. https://doi.org/10.3390/ani12101240
Chicago/Turabian StylePezeshkian, Zahra, Seyed Ziaeddin Mirhoseini, Shahrokh Ghovvati, and Esmaeil Ebrahimie. 2022. "Transcriptome Analysis of Breast Muscle Reveals Pathways Related to Protein Deposition in High Feed Efficiency of Native Turkeys" Animals 12, no. 10: 1240. https://doi.org/10.3390/ani12101240
APA StylePezeshkian, Z., Mirhoseini, S. Z., Ghovvati, S., & Ebrahimie, E. (2022). Transcriptome Analysis of Breast Muscle Reveals Pathways Related to Protein Deposition in High Feed Efficiency of Native Turkeys. Animals, 12(10), 1240. https://doi.org/10.3390/ani12101240