CC BY
0JWPR
Journal of World's Poultry Research
2020, Scienceline Publication
J. World Poult. Res. 10(3): 407-428, September 25, 2020
Research Paper, PII: S2322455X2000048-10 License: CC BY 4.0
DOI: https://dx.doi.org/10.36380/jwpr.2020.48
Genomic Analysis Reveals Strong Signatures of Selection in Guangxi
Three-Yellow Chicken in China
Yuying Liao1*, Junli Sun1, Yingfei Huang1, Fengying Wei1, Guodong Mo1, Lucas Zellmer3, and Dezhong Joshua Liao2*
1Guangxi Academy of Agricultural Sciences, Guangxi Key Laboratory on Livestock Genetic and Improvement, Nanning, Guangxi 530001, P.R. China 2Laboratory of Core Facilities, The Second Hospital, Guizhou University of Traditional Chinese Medicine, 32 Feishan Street, Guiyang 550001, Guizhou Province, China Masonic Cancer Center, University of Minnesota, 435 E. River Road, Minneapolis, MN 55455, USA ♦Corresponding author's Email: 315951610@qq.com; djliao@gzy.edu.cn; ORCID: 0000-0003-3904-349X
Received: 29 Jun. 2020 Accepted: 20 Aug. 2020
ABSTRACT
Much like other indigenous domesticated animals, Guangxi Three-yellow chickens (GX-TYC) in China have experienced strong selective pressure, and show specific phenotypic changes in physiology, morphology and behavior. To identify genomic footprints or selection signatures left by artificial selection during domestication of GX-TYC, the whole genomes of 12 GX-TYC hens were sequenced to executed selective sweep analyses and gene functional enrichment analysis (Gene Ontology and Kyoto Encyclopedia of Genes and Genome pathways). A total of 10.13 million single nucleotide polymorphisms and 842,236 insertion/deletion polymorphisms (Indels) were found. Forty-six windows showed a Z score of heterozygosity (ZHp) lower than -5, which potentially were considered to be positively selected regions. Gene annotation identified 55 genes in these regions. Selection signatures were found mainly on the SSC5, SSC8, SSC23 and SSCZ. GO and KEGG analyses revealed that these genes were related to growth, immune responses as well as carbohydrate, lipid and amino acid metabolisms. In addition, two genes, fructose-1,6-bisphosphatase 1 and fructose-1,6-bisphosphatase 2 were enriched into four signaling pathways, three of which are involved in carbohydrate metabolism and insulin signaling. SHC3, FANCC and PTCH1, in combination with FB1 and FBP2, were clustered together in a region of chromosome Z, and thus might have been selected together. The results have uncovered some genetic footprints of chicken domestication, providing not only an important resource for further improvements of fowl breeding, but also a useful framework for future studies on the genetics of domestic chickens as well as on the phenotypic variations and certain diseases of chickens.
Key words: Chicken; Selective sweeps; Single nucleotide polymorphism; Whole genome resequencing
INTRODUCTION
Three-yellow chicken (TYC) is internationally well known for its desirable meat quality including juiciness, flavor and tenderness. They were named for their yellow feather, yellow beak and yellow feet. Three-yellow chicken is not a particular species, but rather is a collective name for those chicken breeds with these three yellow traits, including Huxu, Qingyuan, Xinghua, Huaixiang, Wenchang and Yangshan chickens in the Guangdong province, Pudong chicken in Shanghai, Xiaoshan chicken in the Zhejiang province, etc. (Zheng et al.1989). Guangxi three-yellow chicken (GX-TYC), a breed that has been intensively selected both naturally and artificially, is mainly distributed in Yulin, Beiliu, Bobai, Cenxi counties or cities in the Guangxi province as a typical traditional breed locally. Because of its aforementioned meat quality, GX-TYC has been widely used in the development of
many special lines of yellow-feather broilers in China (Wei et al. 2019). For future breeding efforts to develop better breeds for the broiler industry, a better understanding of the GX-TYC domestication and identify genetic components obtained from various selections that are likely the consequence of GX-TYC domestication are needed. For these purposes, the whole genome sequencing approach to explore favorable alleles, candidate mutations or single nucleotide polymorphisms (SNPs), and insertions/deletions (Indel) of TX-TYC were used, and the resulting data were reported herein.
MATERIALS AND METHODS
Ethical approval
All animal procedures used in this study were carried out in accordance with the Guide for Care and Use of Laboratory Animals (8th edition, released by the National
Wmmm Liao Y, Sun J, Huang Y, Wei F, Mo G, Zellmer L and Liao DJ (2020). Genomic Analysis Reveals Strong Signatures of Selection in Guangxi Three-Yellow Chicken in China. J. World Poult. Res., 10 (3): 407-428. DOI: https://dx.doi.org/10.36380/jwpr.2020.48
Research Council, USA) and were approved by the Institutional Animal Care and Use Committee (IACUC) of Guangxi Institute of Animal Science.
Sequencing of the Guangxi Three-yellow chicken genome
Twelve GX-TYC hens raised at Chunmao Farming Co. Ltd. of Guangxi, China, were used in this study. Blood samples were collected from the wing vein using standard venipuncture. Genomic DNA was isolated from the blood samples with a bloodGen Mini Kit (Cwbiotech., China), and it was assessed for purity and quality using NanoDrop and gel electrophoresis. A pair-end library with insert sizes varying from 250 to 300 base-pairs (bp) was constructed and sequenced with the Illumina Hiseq 2000/2500 platform by BerryGenomics Biotechnology Co., Ltd., Beijing, China. Raw reads contained some interference information, including the adapter, low quality paired reads and unidentified nucleotides. Clean reads were obtained by removing this interference information (Li et al., 2010), and were mapped onto the chicken reference genome (Gallus gallus, Galgal 14.78) using the BWA software (Li and Durbin, 2009).
Single nucleotide polymorphisms and insertion/deletion polymorphisms Calling
After the alignment, SNP and InDel calling using a Bayesian approach implemented in the package SAMtools were performed. The 'mpileup' command was used to identify SNPs and InDels with the parameters as '-m 2 -F 0.002 -d 1000'. The identified SNPs were filtered with more stringent parameters, i.e., coverage depth > 4, and Root Mean Square (RMS) mapping quality > 20, to obtain high quality SNPs, which were annotated using the Ensembl gene sets (http://www.ensembl.org/biomart/). The SNPs and InDels in gene regions were annotated using the ANNOVAR annotation tool (Wang et al., 2010).
Selective sweep analysis
Selective sweep screen was performed with the sequenced DNA pools. Allele counts at each SNP position were used to detect signatures of selection in 200-Kb sliding windows with a step size of 50% overlapping for the genome sequences of GX-TYC. At each detected SNP position, the sums of major and minor alleles (nMAJ and nMIN) were determined, and then the corresponding heterozygosity score were calculated using the following formula: Hp=2£nMAJXnMIN/ (XnMAJ+XnMIN)2. Individual Hp was then Z-transformed to a standard normal distribution as follows: ZHp=(Hp-^Hp)/cHp. A threshold
of ZHp<-5 was set for putative selective sweeps because windows below it ended the distribution (Rubin et al., 2012).
Analysis of functional enrichment
Functional enrichment analysis of Gene Ontology (GO), as well as Kyoto Encyclopedia of Genes and Genome (KEGG) pathways were performed using "Benjamini-corrected modified Fisher's exact test" in the DAVID web server (Huang et al., 2009). Genes were mapped onto their respective human orthologs. P values that indicated the significance of the overlap between various gene sets were corrected with Benjamini-Hochberg false discovery rate (FDR). Only were terms with a P value less than 0.05 considered significant, and were listed. The GO categories "biological processes", "molecular function" and "cellular component" were used in these analyses.
RESULTS AND DISCUSSION
Data production and short read alignment
Sequencing of the GX-TYC genome generated a total of 35.85 Gbs of paired-end DNA sequences, of which 35.58 (99.25%) Gbs of high quality paired-end reads were mapped onto the chicken reference genome assembly (Gallus_gallus, Galgal 4.78) with 33.66-fold sequence depth using Burrows-Wheeler-Alignment tool (BWA). Several categories of genetic variation, including SNPs and Indels were identified between the uniquely mapped reads and the reference genome.
Single nucleotide polymorphisms and insertion/deletion polymorphisms Identification
Mapping the sequencing reads to the reference genome revealed about 0.13 million SNPs, which exceeded the findings reported in the literature (Wong et al., 2004; Fan et al., 2013). A total of 4,332,562 (43%) SNPs located in genic regions, of which 125,732 were coding ones that leaded to 37,045 nonsynonymous nucleotide substitutions (291 stop gains, 47 stop losses and 36,707 being non-synonymous) detected in a total of 5,839 genes (Figure 1 and supplementary table 1). Identification of 842,236 small Indel polymorphisms ranging from 1 to 50 bps in length (Supplementary table 2) was done, which tended to be detected with a greater frequency than their longer counterparts. About 43% of the Indels were in genic regions, similar to the distribution of SNPs, of which 1613 located in coding sequences (Figure 1).
Stop gain
SNPs Indels
Figure 1. Annotation and distribution of single nucleotide polymorphisms and insertion/deletion polymorphisms
Potential independent signatures of selection in guangxi three-yellow chicken
Domestic animals were excellent models for genetic studies of phenotypic evolution (Andersson, 2001). They evolved genetic adaptations to new environments and were subjected to long-term artificial selections (Rubin et al., 2010). As a result of this process, marks in the proximity of genes influencing breed-defining traits were reduced levels of variability, and showed specific selection
signature, including high population differentiation, greatly reduced variation, temporary increase in linkage disequilibrium, skewed allele frequency, and long-ranged haplotype homozygosity (Kaplan et al., 1989; Fay and Wu 2000; Kim and Stephan 2002; Kim and Nielsen 2004; Pollinger et al., 2005; Smith and Haigh, 2007). Selective sweep drew much attention, and a number of statistical tests, mostly based on summed statistics such as the tests by Lewontin and Krakauer (1973), Li et al. (1985), Tajima
(1989), McDonald and Kreitman (1991), Fu and Li (1993), Fu (1997), Fay and Wu (2000) and Sabeti et al. (2002). Recently, the commonly used method was H-based heterozygosity of SNPs and Fst-based genetic diversification (Rubin et al., 2012). To accurately detect the genomic footprints left by selection in the GX-TYC, a selective sweep screen was performed by searching for genomic regions with high degrees of fixation. The pooled heterozygosity Hp was calculated, in sliding 200-Kb windows crossing the chromosomes from sequence reads that correspond to the most and least frequently observed alleles at all SNP positions. The distribution of observed Hp values and the Z transformations of Hp and ZHp were marked in the Figure 2. The putative sweeps on those reaching a ZHp score of -5 or less were mainly described, as they are in the lower end of the distribution. In the genome-wide screen, only about 0.45% of windows (n=46) showed a Z score of heterozygosity (ZHp) lower than -5 (Figure 2 and supplementary table 3). Striking selection signatures were mainly found on the SSC5, SSC8 and SSCZ regions (Figure 2), while some windows that did not reach the significance threshold may have contributed significantly to chicken domestication. The strongest signature of selection (ZHp = -17.158) was observed at 2.20 to 2.24 Mbs on the chromosome 5, which included two genes, for instance SLC6A5 (Solute Carrier family 6, member 5) and NELL1 (neural EGFL like 1). The SLC6A5 gene encodes a sodium- and chloride-dependent glycine neurotransmitter transporter, which is an important glycoprotein for scavenging extracellular glycine in glycine-mediated neurotransmission. Mutation in this gene can cause hyperekplexia. The neural EGFL like (NELL) gene encoded a cytoplasmic protein that contained epidermal growth factor (EGF) -like repeats. The protein may be involved in cell growth regulation and
differentiation in a variety of tissues, including heart muscle, skeletal muscle and blood vessels, and may promote osteoblast cell differentiation and terminal mineralization (Bokui et al., 2008). The NELL1 gene was identified in a selective sweep in broilers (Elferink et al., 2012). The biological functions of NELL1 may be related to the selection on the muskuloskeletal integrity in modern broiler chickens. Bone integrity was likely to be co-selected with growth rate and meat yield, as the skeleton of modern broilers needed to support a heavier weight (Zhou et al., 2007). The second convincing signature of selection (ZHp = -14.043) occurred on the sex chromosome Z that harbored the death-associated Protein Kinase 1 (DAPK1), cathepsin L2 (CTSL2), fructose-1,6-bisphosphatase 2 (FBP2) and fructose-1,6-bisphosphatase 1 (FBP1). Death-associated Protein Kinase 1 gene is a calmodulin-dependent serine-threonine kinase involved in a variety of cell signaling pathways that regulate cell survival, apoptosis and autophagy. Cathepsin L2, a lysosomal cysteine proteinase, has been shown to be particularly powerful in degrading myofibrillar components in post-mortem autolysis. In fish muscles, CTSL2 exhibits heat-stability on 50 to 60°C, and can degrade surimi protein during the manufacturing of silver carp surimi products (Li et al., 2008). fructose-1,6-bisphosphatase 1 that acts as a rate-limiting enzyme in gluconeogenesis, catalyzes the hydrolysis of fructose 1,6-bisphosphate to fructose 6-phosphate, and inorganic phosphate in the presence of divalent cations, and mediates in gluconeogenesis and carbohydrate biosynthesis. fructose-1,6-bisphosphatase deficiency is associated with hypoglycemia and metabolic acidosis. FBP1 and FBP2 are two important paralogs. Although there is a strong selective signature on chromosome 8, it was impossible to annotated any genes on it.
Figure 2. Genome-wide Z score of heterozygosity (ZHp) distribution. The Y axis is ZHp and the X axis shows positions of windows along each chromosome. Dotted lines indicate the thresholds with ZHp = -5.
Gene Ontology and Kyoto Encyclopedia of Genes and Genome pathways analyses
A total of 55 genes were identified in the regions that were considered to be positively selected (Supplementary table 3). Analysis of gene enrichment within this set of genes showed that, in biological-process (BP), significant enrichment for genes was primarily concentrated on the acid and anion transport, the hexos and monosaccharide metabolisms, the mesonephric development, and the defense response, whereas in cellular-component (CC) enrichment was potentially in cell periphery, plasma membrane and interleukin-28 receptor complex. In molecular-function (MF), enrichment was mainly concentrated on several sugar phosphatase activities and on rRNA (cytosine) methyltransferase activity (Figure 3 and Supplementary table 4). As gene enrichment analysis may yield high false-positive rates (Pavlidis et al., 2012),
additional functional and physiological experiments were needed to verify the contribution of these genes to these processes. KEGG analysis identified eight pathways retaining a statistical significance (P<0.05), i.e. Hedehog signaling pathway (3 genes, P=0.0017), pentose phosphate pathway (2 genes, P=0.0059), fructose and mannose metabolism (2 genes, P=0.012), valine, leucine and isoleucine degradation (2 genes, P=0.020), insulin signaling pathway (3 genes, P=0.022), Fanconi anemia pathway (2 genes, P=0.026), glycolysis/gluconeogenesis (2 genes, P=0.028), as well as synthesis and degradation of ketone bodies (1 gene, P=0.049) (Figure 4, table 1 and Supplementary table 5). Most of these pathways were related to carbohydrate, lipid and amino acid metabolisms, while some were involved in processing genetic information and environmental information (Table 1).
Figure 3. The most enriched gene ontology terms within significant selection of genes on Guangxi Three-yellow chicken of the present study.
Statistics of Pathway Enrichment
Valine, leucine and isoleucine degradation -Synthesis and degradation of ketone bodies -Peroxisome -Pentose phosphate pathway -Other glycan degradation -Lysosome -Lysine degradation -Jak-STAT signaling pathway -Insulin signaling pathway -Hedgehog signaling pathway -Glycolysis / Gluconeogenesis -Galactose metabolism -Fructose and mannose metabolism -Fatty acid metabolism -Fatty acid elongation -Fanconi anemia pathway -Cytokine-cytokine receptor interaction -Carbon metabolism -Butanoate metabolism -Amino sugar and nucleotide sugar metabolism -
0.03
0.06 Rich factor
0.09
qvalue X 1.00
0.75
0.50
0.25
■ 0.00
Gene_number
1.0 1.5 2.0 2.5 3.0
Figure 4. The 20 most enriched Kyoto Encyclopedia of Genes and Genome pathways within significant selection of genes on Guangxi three-yellow chicken in the present study.
Table 1. Results of Kyoto encyclopedia of genes and genome pathways analysis
ID KEGG Term Gene P-Value
Environmental information processing
Gga 04340 Hedgehog signaling pathway GAS1, Novel, PTCH1 1.78E-03
Carbohydrate metabolism
Gga 00030 Pentose phosphate pathway FBP1, FBP2 5.90E-03
Gga00051 Fructose and mannose metabolism FBP1, FBP2 1.26E-02
Gga00010 Glycolysis / Gluconeogenesis FBP1, FBP2 2.82E-02
Amino acid metabolism
Gga 00280 Valine, leucine and isoleucine degradation HMGCL, AUH 1.97E-02
Organismal systems-Endocrine systems
Gga 04910 Insulin signaling pathway FBP1, FBP2, SHC2 2.29E-02
Genetic information processing
Gga 03460 Fanconi anemia pathway FANCF, FANCC 2.62E-02
Lipid metabolism
Gga 00072 Synthesis and degradation of ketone bodies HMGCL 4.93E-02
Three genes, i.e. the growth arrest-specific gene-1 (GAS1), Novel and protein patched homolog-1 (PTCH1), were enriched on the Hedgehog (Hh) signaling pathway that has many roles in development, cell proliferation,
tissue patterning and stem cell maintenance. As a putative tumor suppressor gene (Del et al., 1992; Del et al., 1994; Atsumi et al., 2014), Growth arrest-specific 1(GAS1) inhibits cell replication by blocking the entry into the S
phase of the cell cycle (Del et al., 1992). Protein patched homolog 1 (PTCH1) was a member of the patched gene family, and was the receptor for sonic hedgehog (SHH), which was a secreted molecule implicated in the formation of embryonic structures, and in tumorigenesis (Carpenter et al., 1998). PTCH1 prevented cells from growing and dividing in the absence of SHH, thus it was considered as a tumor suppressor (Villavicencio et al., 2000), although it stoped suppressing cell proliferation in the presence of SHH.Fanconi anemia group F (FANCF) and Fanconi anemia group C (FANCC) belonged to the Fanconi anemia (FA) family, which contained of 22 genes whose protein products form a complex to participate in the efficient repair of damaged DNA (Nepal et al., 2017; Nalepa and Clapp, 2018; Tsui and Crismani, 2019). FANCF stabilized the FANCC/FANCE sub complex and the FANCA/FANCG subcomplex, and locked the whole FA core complex in a conformation that was essential for DNA repair (Leveille et al., 2004), suggesting its important role in maintaining the cell's genomic integrity (Medhurst et al., 2001). FANCF-deficient mice found with no germ cells in the seminiferous tubules, and no or almost no primordial follicles in the ovaries (Bakker et al., 2012). As a mitochondrial enzyme, 3-Hydroxymethyl-3-Methylglutaryl-CoA Lyase (HMGCL) was involved in the valine, leucine and isoleucine degradation and synthesis as well as in the degradation of ketone bodies. When glucose is not available, such as during fasting, ketones are the compounds used for energy by certain organs and tissues, particularly the brain. In human, HMGCL deficiency, often as an autosomal recessive mitochondrial disease (Lin et al., 2009), usually presented with acute episodes of vomiting, hypotonia, hypoketotic, hypoglycemia metabolic acidosis and hyperammonemia in infancy. In the valine, leucine and isoleucine degradation pathways, 3-methylglutaconyl-CoA hydratase (AUH) was another selected gene encoding a bifunctional mitochondrial protein that had both RNA-binding and hydratase activities. The protein can catalyze the transformation of 3-methylglutaconyl-CoA to 3-hydroxy-3 -methyl-glutaryl-CoA, and binds AU-rich elements found in the 3'-untranslated regions of rapidly decaying mRNAs. Decreased levels of AUH also leaded to a slower cell growth. Reduced or elevated levels of AUH can lead to defects in mitochondrial translation, ultimately leading to changes in decreased RNA stability as well as in the mitochondrial morphology, biogenesis and respiratory function (Mack et al., 2006). FBP1 and FBP2 were enriched in pentose phosphate pathway, in fructose and mannose metabolism, in glycolysis/gluconeogenesis, and
in insulin signaling pathway that regulates carbohydrate metabolism and endocrine systems. The pentose phosphate pathway is a glucose metabolism process that produces reduced Nicotinamide Adenine Dinucleotide Phosphate and pentoses, which is an essential part of histidine and purine/pyrimidine biosynthesis nucleotides. Glycolysis/ gluconeogenesis is the process of converting glucose to pyruvate and producing small amounts of ATP (energy) and NADH (reducing power). FBPs ultimately control the rate of gluconeogenesis, whereas the insulin signaling pathway is responsible for regulation of glucose and lipid metabolism, besides many other functions such as regulation of cell proliferation in response to mitogens. Src homology 2 domain containing-transforming protein 2 (SHC2), as a substrate of insulin receptor, can activate the RAS/MAPK pathway independently of IRS-1 (Taha and Klip, 1999; Ferguson et al., 2014). Of the ten genes enriched in the aforementioned pathways, FBP1, FBP2, SHC3, FANCC and PTCH1 were located on the 41.2 to 43.3 region of chromosome Z, which might be integrally chained due to selected certain particular genes, with FBP1 and FBP2 being the most likely objectives and the others likely being jointly selected. Within the selective sweeps in all of the domestic chickens in the present and other studies (Rubin et al., 2010), some of the genes were also found to be associated with domestication traits in chickens and other farmed animals, which reinforced their important roles in chicken domestication. For instance, BCDO2 was found to be associated with the yellow skin (Eriksson et al., 2008). However, this gene in GX-TYC was not detected. ESRP2 is associated with chicken abdominal fat contents (Zhang et al., 2012), and NELL1 was identified in a selective sweep in the broilers (Elferink et al., 2012). In the present study, NELL1 gene was found to undergo a strong selection in GX-TYC, which verified GX-TYC as a broiler, thus conforming to the long-term breeding purpose of GX-TYC and confirming that the present approach and the resulting data were reliable.
CONCLUSION
In summary, herein a whole genome map of Single nucleotide polymorphisms (SNPs), insertion/deletion polymorphisms (InDels) of Guangxi Three-Yellow chicken (GX-TYC) were presented and some genetic footprints of its domestication were uncovered. These data provide important resources for further improvements of fowl breeding and for future studies on the molecular mechanisms of chicken phenotypic variations and certain diseases.
DECLARATIONS
Consent to publish
All authors agree to publish this manuscript.
Availability of data and materials
All data have been presented in the manuscript as figures and tables and as the supplementary data. There is no additional data and materials.
Competing interests
All authors claim that there is no completing interest concerned.
Funding
This work was supported by Guangxi Provincial Natural Science Foundation of China (NO. 2013GXNSFDA019013) to Dr. Yuying Liao. Guangxi Special Fund for Specially-invited Expert.
Authors' contributions
YL drafted the manuscript. YL and DJL formulated the concepts. JS, YH, FW and GM analyzed the data and prepared the figures and tables. LZ performed English editing of the manuscript. DJL finalized the manuscript.
Acknowledgements
We would like to think Dr. Fred Bogott at the Medical Center, Austin of Minnesota for his excellent English editing of the manuscript.
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Supplementary Data
Supplementary Table 1. Summary and annotation of single nucleotide polymorphisms in Guangxi three-yellow chickens Category Number of SNPs
Upstream
Exonic
Intronic
Splicing
Downstream
Upstream/downstream
Intergenic
Stop gain Stop loss Synonymous Non-synonymous Unknowns
140,563 291 47 88,687 36,707 0
3,938,603
387 122,273 5,004 5,806,581
Total
10,139,143
Supplementary Table 2. Summary and annotation of Indels in Guangxi three-yellow chickens
Category Number of Indels
Upstream 10632
Stop gain 13
Stop loss 3
Frameshift deletion 413
Exonic
Frameshift insertion 512
Non-frameshift deletion 377
Non-frameshift insertion 295
Intronic 335096
Splicing 175
Downstream 11948
Upstream/Downstream 418
Intergenic 482323
Insertion 380249
Deletion 461987
Het Rate (%) 0.643
Total 842236
Supplementary Table 3. Detail information of single nucleotide polymorphisms loci with ZHp < -5
Ensembl Gene ID ZHp CHROM Start Gene
ENSGALG00000003958 -11.572 5 2129860 PRMT3
ENSGALG00000003908 -17.158 5 2204843 SLC6A5
ENSGALG00000003777 -17.158 5 2243366 NELL1
ENSGALG00000003748 -9.0503 5 2760128 ANO5
ENSGALG00000003660 -10.144 5 2946165 FANCF
ENSGALG00000003655 -10.144 5 2976276 GAS2
ENSGALG00000003648 -6.1477 5 3060193 SVIP
ENSGALG00000013311 -6.9695 5 3278760 ANO3
ENSGALG00000013304 -11.351 5 3407884 SLC5A12
ENSGALG00000023904 -11.351 5 3505528 FIBIN
ENSGALG00000013297 -11.351 5 3530348 BBOX1
ENSGALG00000012194 -10.236 5 3627318 CCDC34
ENSGALG00000012191 -8.6053 5 3651822 LGR4
ENSGALG00000012170 -8.6053 5 3717817 LIN7B
ENSGALG00000012163 -8.6053 5 3757392 BDNF
ENSGALG00000012162 -8.6053 5 3783967 Novel
ENSGALG00000012160 -8.137 5 3878424 KIF18A
ENSGALG00000012153 -5.0344 5 3921314 METTL15
ENSGALG00000004112 23 5552378 FUCA1
ENSGALG00000004120 23 5558027 CNR2
ENSGALG00000003971 23 5518731 TCEB3
ENSGALG00000004002 23 5540404 LYPLA2
ENSGALG00000004047 23 5545884 GALE
ENSGALG00000003936 -5.0735 23 5514567 PPT1
ENSGALG00000004268 23 5696766 NIPAL3
ENSGALG00000004155 23 5586447 MYOM3
ENSGALG00000003879 23 5493121 MFSD2A
ENSGALG00000004141 23 5581470 LBFABP
ENSGALG00000004057 23 5548630 HMGCL
ENSGALG00000004122 23 5565578 PNRC2
ENSGALG00000004249 23 5643857 GRHL3
ENSGALG00000003986 23 5536714 PITHD1
ENSGALG00000004133 23 5572421 SRSF10
ENSGALG00000004231 23 5625795 IFNLR1
ENSGALG00000004221 23 5618293 IL22RA1
ENSGALG00000003912 23 5502015 CAP1
ENSGALG00000017658 -6.8264 Z 40920596 GAS1
ENSGALG00000026583 -6.8264 Z 40920611 Novel
ENSGALG00000012608 -14.043 Z 41139762 DAPK1
ENSGALG00000012610 -14.043 Z 41267496 CTSL2
ENSGALG00000012612 -14.043 Z 41282076 FBP2
ENSGALG00000012613 -14.043 Z 41306732 FBP1
ENSGALG00000012615 -7.1684 Z 41350384 C9orf3
ENSGALG00000012618 -7.1684 Z 41521328 FANCC
ENSGALG00000012620 -6.5791 Z 41632373 PTCH1
ENSGALG00000010683 -5.8349 Z 43300329 S1PR3
ENSGALG00000010688 -5.8349 Z 43311888 SHC3
ENSGALG00000010694 -5.8349 Z 43414992 SECISBP2
ENSGALG00000010697 -5.8349 Z 43446316 SEMA4D
ENSGALG00000005323 -5.1417 Z 43855798 DIRAS2
ENSGALG00000015216 -5.1608 Z 43939409 SYK
ENSGALG00000015213 -5.1608 Z 43980705 TPPP2
ENSGALG00000021843 -6.6507 Z 44067508 AUH
ENSGALG00000015209 -6.683 Z 44205924 NFIL3
ENSGALG00000000151 -7.1704 Z 45148296 ADAMTS19
Supplementary Table 4. Gene functional enrichment analysis of genes significant selection in Guangxi three-yellow chickens
GO_accession Term_type Description N P Value
GO:0042132 MF fructose 1,6-bisphosphate 1-phosphatase activity 2 9.74E-06
GO:0046942 BP carboxylic acid transport 5 1.72E-04
GO:0015849 BP organic acid transport 5 1.77E-04
GO:0050308 MF sugar-phosphatase activity 2 4.43E-04
GO:0019203 MF carbohydrate phosphatase activity 2 5.40E-04
GO:0015711 BP organic anion transport 5 6.52E-04
GO:0019318 BP hexose metabolic process 4 7.37E-04
GO:0071944 CC cell periphery 17 7.53E-04
GO:0006820 BP anion transport 6 8.51E-04
GO:0005996 BP monosaccharide metabolic process 4 1.12E-03
GO:0005886 CC plasma membrane 16 1.48E-03
GO:0015718 BP monocarboxylic acid transport 3 2.05E-03
GO:0001657 BP ureteric bud development 3 2.60E-03
GO:0007270 BP neuron-neuron synaptic transmission 3 2.65E-03
GO:0072163 BP mesonephric epithelium development 3 2.69E-03
GO:0072164 BP mesonephric tubule development 3 2.69E-03
GO:0006952 BP defense response 7 2.71E-03
GO:0004490 MF methylglutaconyl-CoA hydratase activity 1 3.15E-03
GO:0010157 BP response to chlorate 1 3.15E-03
GO:0016434 MF rRNA (cytosine) methyltransferase activity 1 3.15E-03
GO:0036335 BP intestinal stem cell homeostasis 1 3.15E-03
GO:0071424 MF rRNA (cytosine-N4-)-methyltransferase activity 1 3.15E-03
GO:0070463 MF tubulin-dependent ATPase activity 1 3.15E-03
GO:1901550 BP regulation of endothelial cell development 1 3.15E-03
GO:1901551 BP negative regulation of endothelial cell development 1 3.15E-03
GO:1903140 BP regulation of establishment of endothelial barrier 1 3.15E-03
GO:1903141 BP negative regulation of establishment of endothelial barrier 1 3.15E-03
GO:0005294 MF neutral L-amino acid secondary active transmembrane transporter activity 1 3.15E-03
GO:0015375 MF glycine:sodium symporter activity 1 3.15E-03
GO:0036233 BP glycine import 1 3.15E-03
GO:1990379 BP lipid transport across blood brain barrier 1 3.20E-03
GO:0001823 BP mesonephros development 3 3.21E-03
GO:0046854 BP phosphatidylinositol phosphorylation 2 3.51E-03
GO:0032002 CC interleukin-28 receptor complex 1 3.54E-03
GO:0046834 BP lipid phosphorylation 2 4.02E-03
GO:0050747 BP positive regulation of lipoprotein metabolic process 1 4.18E-03
GO:1903061 BP positive regulation of protein lipidation 1 4.18E-03
GO:0006836 BP neurotransmitter transport 3 4.30E-03
GO:0005548 MF phospholipid transporter activity 2 4.53E-03
GO:0003978 MF UDP-glucose 4-epimerase activity 1 4.53E-03
GO:0005169 MF neurotrophin TRKB receptor binding 1 5.14E-03
GO:0061193 BP taste bud development 1 5.14E-03
G0:0045668 BP negative regulation of osteoblast differentiation 2 5.15E-03
G0:0061005 BP cell differentiation involved in kidney development 2 5.53E-03
G0:0051234 BP establishment of localization 18 5.94E-03
G0:0021997 BP neural plate axis specification 1 6.29E-03
G0:0097108 MF hedgehog family protein binding 1 6.29E-03
G0:2001013 BP epithelial cell proliferation involved in renal tubule morphogenesis 1 6.29E-03
G0:0010693 BP negative regulation of alkaline phosphatase activity 1 6.29E-03
G0:1900220 G0:0071226 BP BP semaphorin-plexin signaling pathway involved in bone trabecula morphogenesis cellular response to molecule of fungal origin 1 1 6.29E-03 6.29E-03
G0:0004300 MF enoyl-CoA hydratase activity 1 6.29E-03
G0:0060995 BP cell-cell signaling involved in kidney development 1 6.29E-03
G0:0061289 BP Wnt signaling pathway involved in kidney development 1 6.29E-03
G0:0061290 BP canonical Wnt signaling pathway involved in metanephric kidney development 1 6.29E-03
G0:0072204 BP cell-cell signaling involved in metanephros development 1 6.29E-03
G0:0045329 BP carnitine biosynthetic process 1 6.29E-03
G0:0005119 MF smoothened binding 1 6.31E-03
G0:0005901 CC caveola 2 6.33E-03
G0:0015908 BP fatty acid transport 2 6.35E-03
G0:0045121 CC membrane raft 3 6.51E-03
G0:0072073 BP kidney epithelium development 3 6.53E-03
G0:0044853 CC plasma membrane raft 2 6.67E-03
G0:0004560 MF alpha-L-fucosidase activity 1 6.72E-03
G0:0006004 BP fucose metabolic process 1 6.72E-03
G0:0015928 MF fucosidase activity 1 6.72E-03
G0:0015850 BP organic hydroxy compound transport 6.81E-03
G0:0008474 MF palmitoyl-(protein) hydrolase activity 1 6.91E-03
G0:0098599 MF palmitoyl hydrolase activity 1 6.91E-03
G0:0007042 BP lysosomal lumen acidification 1 7.03E-03
G0:1903070 BP negative regulation of ER-associated ubiquitin-dependent protein catabolic 1 7.32E-03
G0:1903059 BP process regulation of protein lipidation 1 7.32E-03
G0:0070475 BP rRNA base methylation 1 7.66E-03
G0:0019388 BP galactose catabolic process 1 7.67E-03
G0:0016049 BP cell growth 4 7.89E-03
G0:0004888 MF transmembrane signaling receptor activity 7 7.92E-03
G0:0046717 BP acid secretion 2 7.98E-03
G0:0032229 BP negative regulation of synaptic transmission, GABAergic 1 8.42E-03
G0:0007166 BP cell surface receptor signaling pathway 13 8.58E-03
G0:0007267 BP cell-cell signaling 6 8.83E-03
G0:0044425 CC membrane part 19 8.87E-03
G0:0007611 BP learning or memory 3 9.03E-03
G0:0060012 BP synaptic transmission, glycinergic 1 9.42E-03
G0:0008469 MF histone-arginine N-methyltransferase activity 1 9.42E-03
G0:0019919 BP peptidyl-arginine methylation, to asymmetrical-dimethyl arginine 1 9.42E-03
G0:0035242 MF protein-arginine omega-N asymmetric methyltransferase activity 1 9.42E-03
G0:0035247 BP peptidyl-arginine omega-N-methylation 1 9.42E-03
G0:0045602 BP negative regulation of endothelial cell differentiation 1 9.42E-03
G0:0097025 CC MPP7-DLG1-LIN7 complex 1 9.42E-03
G0:0002238 BP response to molecule of fungal origin 1 9.42E-03
G0:0097016 MF L27 domain binding 1 9.42E-03
G0:0009957 BP epidermal cell fate specification 1 9.44E-03
G0:0002351 BP serotonin production involved in inflammatory response 1 9.48E-03
G0:0002442 BP serotonin secretion involved in inflammatory response 1 9.48E-03
G0:0002554 BP serotonin secretion by platelet 1 9.48E-03
G0:0006578 BP amino-acid betaine biosynthetic process 1 9.49E-03
G0:0045926 BP negative regulation of growth 9.54E-03
G0:0006094 BP gluconeogenesis 9.60E-03
G0:0042806 MF fucose binding 1 9.87E-03
G0:0042015 MF interleukin-20 binding 1 9.96E-03
G0:0048549 BP positive regulation of pinocytosis 1 1.00E-02
G0:0002084 BP protein depalmitoylation 1 1.00E-02
G0:0098734 BP macromolecule depalmitoylation 1 1.00E-02
G0:0006810 BP transport 17 1.01E-02
G0:0035751 BP regulation of lysosomal lumen pH 1 1.02E-02
G0:0040007 BP growth 6 1.04E-02
G0:0031324 BP negative regulation of cellular metabolic process 10 1.04E-02
G0:2000027 BP regulation of organ morphogenesis 3 1.07E-02
G0:1903069 BP regulation of ER-associated ubiquitin-dependent protein catabolic process 1 1.09E-02
G0:0090237 BP regulation of arachidonic acid secretion 1 1.10E-02
G0:0071286 BP cellular response to magnesium ion 1 1.10E-02
G0:0004419 MF hydroxymethylglutaryl-CoA lyase activity 1 1.12E-02
G0:0016833 MF oxo-acid-lyase activity 1 1.12E-02
G0:0019319 BP hexose biosynthetic process 1.14E-02
G0:0032429 BP regulation of phospholipase A2 activity 1 1.19E-02
G0:0007412 BP axon target recognition 1 1.21E-02
G0:0008589 BP regulation of smoothened signaling pathway 1.25E-02
G0:0043313 BP regulation of neutrophil degranulation 1 1.25E-02
G0:1902563 BP regulation of neutrophil activation 1 1.25E-02
G0:0016273 MF arginine N-methyltransferase activity 1 1.25E-02
G0:0016274 MF protein-arginine N-methyltransferase activity 1 1.25E-02
G0:0035246 BP peptidyl-arginine N-methylation 1 1.25E-02
G0:0005828 CC kinetochore microtubule 1 1.25E-02
G0:0017128 MF phospholipid scramblase activity 1 1.25E-02
G0:0061588 BP calcium activated phospholipid scrambling 1 1.25E-02
G0:0061590 BP calcium activated phosphatidylcholine scrambling 1 1.25E-02
G0:0061591 BP calcium activated galactosylceramide scrambling 1 1.25E-02
G0:0030279 BP negative regulation of ossification 2 1.25E-02
G0:0008170 MF N-methyltransferase activity 2 1.27E-02
G0:0034969 BP histone arginine methylation 1 1.29E-02
G0:0050890 BP cognition 3 1.29E-02
G0:0032009 CC early phagosome 1 1.30E-02
G0:0001658 BP branching involved in ureteric bud morphogenesis 2 1.30E-02
G0:0006002 BP fructose 6-phosphate metabolic process 1 1.31E-02
G0:0046364 BP monosaccharide biosynthetic process 2 1.31E-02
G0:0004949 MF cannabinoid receptor activity 1 1.32E-02
G0:0038023 MF signaling receptor activity 7 1.35E-02
G0:0000835 CC ER ubiquitin ligase complex 1 1.36E-02
G0:0000836 CC Hrd1p ubiquitin ligase complex 1 1.36E-02
G0:0005113 MF patched binding 1 1.37E-02
G0:0015187 MF glycine transmembrane transporter activity 1 1.38E-02
G0:0048511 BP rhythmic process 3 1.39E-02
G0:0019320 BP hexose catabolic process 1 1.39E-02
G0:0046849 BP bone remodeling 2 1.41E-02
G0:0031982 CC vesicle 14 1.42E-02
G0:0071345 BP cellular response to cytokine stimulus 4 1.42E-02
G0:0001649 BP osteoblast differentiation 3 1.47E-02
G0:0060675 BP ureteric bud morphogenesis 2 1.53E-02
G0:0007406 BP negative regulation of neuroblast proliferation 1 1.53E-02
G0:0005319 MF lipid transporter activity 2 1.54E-02
G0:0015293 MF symporter activity 2 1.55E-02
G0:0097484 BP dendrite extension 1 1.56E-02
G0:0032368 BP regulation of lipid transport 2 1.57E-02
G0:0010692 BP regulation of alkaline phosphatase activity 1 1.57E-02
G0:0016051 BP carbohydrate biosynthetic process 3 1.58E-02
G0:0071702 BP organic substance transport 10 1.58E-02
G0:0030812 BP negative regulation of nucleotide catabolic process 1 1.59E-02
G0:0045820 BP negative regulation of glycolytic process 1 1.59E-02
G0:0051195 BP negative regulation of cofactor metabolic process 1 1.59E-02
G0:0051198 BP negative regulation of coenzyme metabolic process 1 1.59E-02
G0:0072171 BP mesonephric tubule morphogenesis 2 1.60E-02
G0:0018216 BP peptidyl-arginine methylation 1 1.60E-02
G0:0006869 BP lipid transport 3 1.61E-02
G0:0042159 BP lipoprotein catabolic process 1 1.63E-02
G0:0048548 BP regulation of pinocytosis 1 1.64E-02
G0:0015816 BP glycine transport 1 1.69E-02
G0:0016208 MF AMP binding 1 1.71E-02
G0:0072203 BP cell proliferation involved in metanephros development 1 1.71E-02
G0:0045056 BP transcytosis 1 1.73E-02
G0:0032026 BP response to magnesium ion 1 1.73E-02
G0:0006811 BP ion transport 8 1.74E-02
G0:0016139 BP glycoside catabolic process 1 1.76E-02
G0:0060896 BP neural plate pattern specification 1 1.77E-02
GO:0044724 BP single-organism carbohydrate catabolic process 2 1.77E-02
GO:0038036 MF sphingosine-1-phosphate receptor activity 1 1.79E-02
GO:0010629 BP negative regulation of gene expression 7 1.80E-02
GO:0044723 BP single-organism carbohydrate metabolic process 5 1.89E-02
GO:0001820 BP serotonin secretion 1 1.92E-02
GO:0033008 BP positive regulation of mast cell activation involved in immune response 1 1.93E-02
GO:0043306 BP positive regulation of mast cell degranulation 1 1.93E-02
GO:0032928 BP regulation of superoxide anion generation 1 1.94E-02
GO:0016052 BP carbohydrate catabolic process 2 1.95E-02
GO:0038171 BP cannabinoid signaling pathway 1 1.97E-02
GO:0009892 BP negative regulation of metabolic process 10 1.97E-02
GO:0072078 BP nephron tubule morphogenesis 2 1.98E-02
GO:0032940 BP secretion by cell 5 2.00E-02
GO:0034097 BP response to cytokine 4 2.01E-02
GO:0017121 BP phospholipid scrambling 1 2.02E-02
GO:0072088 BP nephron epithelium morphogenesis 2 2.04E-02
GO:0061333 BP renal tubule morphogenesis 2 2.09E-02
GO:0000153 CC cytoplasmic ubiquitin ligase complex 1 2.09E-02
GO:0098542 BP defense response to other organism 3 2.09E-02
GO:0072028 BP nephron morphogenesis 2 2.10E-02
GO:0016137 BP glycoside metabolic process 1 2.11E-02
GO:0046365 BP monosaccharide catabolic process 1 2.11E-02
GO:0007269 BP neurotransmitter secretion 2 2.12E-02
GO:0005167 MF neurotrophin TRK receptor binding 1 2.13E-02
GO:0002281 BP macrophage activation involved in immune response 1 2.18E-02
GO:0046668 BP regulation of retinal cell programmed cell death 1 2.19E-02
GO:0009437 BP carnitine metabolic process 1 2.20E-02
GO:0051010 MF microtubule plus-end binding 1 2.21E-02
GO:0002576 BP platelet degranulation 1 2.22E-02
GO:0008509 MF anion transmembrane transporter activity 3 2.23E-02
GO:0033005 BP positive regulation of mast cell activation 1 2.24E-02
GO:0017075 MF syntaxin-1 binding 1 2.25E-02
GO:0072282 BP metanephric nephron tubule morphogenesis 1 2.26E-02
GO:0001558 BP regulation of cell growth 3 2.27E-02
GO:0050746 BP regulation of lipoprotein metabolic process 1 2.28E-02
GO:0016857 MF racemase and epimerase activity, acting on carbohydrates and derivatives 1 2.28E-02
GO:0010876 BP lipid localization 3 2.30E-02
GO:0010605 BP negative regulation of macromolecule metabolic process 9 2.32E-02
GO:0007035 BP vacuolar acidification 1 2.33E-02
GO:0003376 BP sphingosine-1-phosphate signaling pathway 1 2.41E-02
GO:0005283 MF sodium:amino acid symporter activity 1 2.49E-02
GO:0005229 MF intracellular calcium activated chloride channel activity 1 2.50E-02
GO:0004896 MF cytokine receptor activity 2 2.51E-02
GO:0006577 BP amino-acid betaine metabolic process 1 2.52E-02
G0:0018195 BP peptidyl-arginine modification 1 2.55E-02
G0:0002888 BP positive regulation of myeloid leukocyte mediated immunity 1 2.56E-02
G0:0031988 CC membrane-bounded vesicle 13 2.58E-02
G0:0040008 BP regulation of growth 4 2.62E-02
G0:0002009 BP morphogenesis of an epithelium 4 2.64E-02
G0:0001656 BP metanephros development 2 2.65E-02
G0:0015129 MF lactate transmembrane transporter activity 1 2.67E-02
G0:0015727 BP lactate transport 1 2.67E-02
G0:0035873 BP lactate transmembrane transport 1 2.67E-02
G0:0031430 CC M band 1 2.68E-02
G0:0014047 BP glutamate secretion 1 2.69E-02
G0:0043090 BP amino acid import 1 2.71E-02
G0:0043092 BP L-amino acid import 1 2.71E-02
G0:0090520 BP sphingolipid mediated signaling pathway 1 2.72E-02
G0:0072080 BP nephron tubule development 2.75E-02
G0:0042157 BP lipoprotein metabolic process 2.77E-02
G0:0002251 BP organ or tissue specific immune response 1 2.79E-02
G0:0002385 BP mucosal immune response 1 2.79E-02
G0:0032303 BP regulation of icosanoid secretion 1 2.81E-02
G0:0060856 BP establishment of blood-brain barrier 1 2.81E-02
G0:0045978 BP negative regulation of nucleoside metabolic process 1 2.83E-02
G0:0006837 BP serotonin transport 1 2.85E-02
G0:0019370 BP leukotriene biosynthetic process 1 2.86E-02
G0:0048588 BP developmental cell growth 2.86E-02
G0:0045125 MF bioactive lipid receptor activity 1 2.86E-02
G0:0043302 BP positive regulation of leukocyte degranulation 1 2.86E-02
G0:0006865 BP amino acid transport 2.87E-02
G0:0072173 BP metanephric tubule morphogenesis 1 2.88E-02
G0:2000310 BP regulation of N-methyl-D-aspartate selective glutamate receptor activity 1 2.88E-02
G0:0046666 BP retinal cell programmed cell death 1 2.90E-02
G0:0001843 BP neural tube closure 2 2.90E-02
G0:0001822 BP kidney development 3 2.91E-02
G0:0030856 BP regulation of epithelial cell differentiation 2 2.92E-02
G0:0005165 MF neurotrophin receptor binding 1 2.94E-02
G0:0060606 BP tube closure 2 2.96E-02
G0:0060993 BP kidney morphogenesis 2 2.99E-02
G0:0061029 BP eyelid development in camera-type eye 1 2.99E-02
G0:0061326 BP renal tubule development 2 3.01E-02
G0:0006012 BP galactose metabolic process 1 3.01E-02
G0:0032269 BP negative regulation of cellular protein metabolic process 5 3.01E-02
G0:0046903 BP secretion 5 3.01E-02
G0:0031330 BP negative regulation of cellular catabolic process 2 3.03E-02
G0:0010875 BP positive regulation of cholesterol efflux 1 3.06E-02
G0:0043240 CC Fanconi anaemia nuclear complex 1 3.06E-02
G0:0048589 BP developmental growth 4 3.08E-02
G0:0008150 BP biological_process 46 3.09E-02
G0:0008649 MF rRNA methyltransferase activity 1 3.10E-02
G0:0060831 BP smoothened signaling pathway involved in dorsal/ventral neural tube patterning 1 3.11E-02
G0:0044459 CC plasma membrane part 8 3.12E-02
G0:0090330 BP regulation of platelet aggregation 1 3.12E-02
G0:0040015 BP negative regulation of multicellular organism growth 1 3.13E-02
G0:0004872 MF receptor activity 7 3.14E-02
G0:0048672 BP positive regulation of collateral sprouting 1 3.17E-02
G0:0014020 BP primary neural tube formation 2 3.19E-02
G0:0002283 BP neutrophil activation involved in immune response 1 3.19E-02
G0:0043312 BP neutrophil degranulation 1 3.19E-02
G0:0016021 CC integral component of membrane 14 3.23E-02
G0:0005416 MF cation:amino acid symporter activity 1 3.23E-02
G0:0045667 BP regulation of osteoblast differentiation 2 3.24E-02
G0:0008757 MF S-adenosylmethionine-dependent methyltransferase activity 2 3.25E-02
G0:0045579 BP positive regulation of B cell differentiation 1 3.27E-02
G0:1902578 BP single-organism localization 14 3.28E-02
G0:0042742 BP defense response to bacterium 2 3.28E-02
G0:0006907 BP pinocytosis 1 3.32E-02
G0:0060080 BP regulation of inhibitory postsynaptic membrane potential 1 3.32E-02
G0:0016192 BP vesicle-mediated transport 6 3.33E-02
G0:0072001 BP renal system development 3 3.35E-02
G0:0001840 BP neural plate development 1 3.37E-02
G0:0048025 BP negative regulation of mRNA splicing, via spliceosome 1 3.38E-02
G0:0061430 BP bone trabecula morphogenesis 1 3.41E-02
G0:0043524 BP negative regulation of neuron apoptotic process 2 3.42E-02
G0:0060429 BP epithelium development 6 3.44E-02
G0:1903307 BP positive regulation of regulated secretory pathway 1 3.48E-02
G0:0044712 BP single-organism catabolic process 5 3.48E-02
G0:0048771 BP tissue remodeling 2 3.49E-02
G0:0006691 BP leukotriene metabolic process 1 3.49E-02
G0:0043586 BP tongue development 1 3.51E-02
G0:0030308 BP negative regulation of cell growth 2 3.52E-02
G0:0072009 BP nephron epithelium development 2 3.52E-02
G0:0072661 BP protein targeting to plasma membrane 1 3.56E-02
G0:0048523 BP negative regulation of cellular process 14 3.58E-02
G0:0090322 BP regulation of superoxide metabolic process 1 3.59E-02
G0:0046488 BP phosphatidylinositol metabolic process 2 3.60E-02
G0:0034122 BP negative regulation of toll-like receptor signaling pathway 1 3.61E-02
G0:0008574 MF ATP-dependent microtubule motor activity, plus-end-directed 1 3.64E-02
G0:0031224 CC intrinsic component of membrane 14 3.65E-02
G0:0016500 MF protein-hormone receptor activity 1 3.67E-02
G0:0032373 BP positive regulation of sterol transport 1 3.67E-02
G0:0032376 BP positive regulation of cholesterol transport 1 3.67E-02
G0:0046943 MF carboxylic acid transmembrane transporter activity 2 3.78E-02
G0:0072111 BP cell proliferation involved in kidney development 1 3.78E-02
G0:1900449 BP regulation of glutamate receptor signaling pathway 1 3.80E-02
G0:0050482 BP arachidonic acid secretion 1 3.80E-02
G0:1903963 BP arachidonate transport 1 3.80E-02
G0:0050829 BP defense response to Gram-negative bacterium 1 3.80E-02
G0:2000191 BP regulation of fatty acid transport 1 3.82E-02
G0:0045934 BP negative regulation of nucleobase-containing compound metabolic process 6 3.83E-02
G0:0005342 MF organic acid transmembrane transporter activity 2 3.85E-02
G0:0090179 BP planar cell polarity pathway involved in neural tube closure 1 3.85E-02
G0:0001505 BP regulation of neurotransmitter levels 2 3.85E-02
G0:0050691 BP regulation of defense response to virus by host 1 3.85E-02
G0:0060627 BP regulation of vesicle-mediated transport 3 3.85E-02
G0:0006629 BP lipid metabolic process 6 3.86E-02
G0:0016854 MF racemase and epimerase activity 1 3.87E-02
G0:0001841 BP neural tube formation 2 3.87E-02
G0:0045780 BP positive regulation of bone resorption 1 3.88E-02
G0:0046852 BP positive regulation of bone remodeling 1 3.88E-02
G0:0051248 BP negative regulation of protein metabolic process 5 3.91E-02
G0:0072202 BP cell differentiation involved in metanephros development 1 3.95E-02
G0:0046641 BP positive regulation of alpha-beta T cell proliferation 1 3.99E-02
G0:0005975 BP carbohydrate metabolic process 5 4.00E-02
G0:0045601 BP regulation of endothelial cell differentiation 1 4.01E-02
G0:0051172 BP negative regulation of nitrogen compound metabolic process 6 4.04E-02
G0:0060628 BP regulation of ER to Golgi vesicle-mediated transport 1 4.05E-02
G0:0072224 BP metanephric glomerulus development 1 4.07E-02
G0:0043304 BP regulation of mast cell degranulation 1 4.11E-02
G0:0090178 BP regulation of establishment of planar polarity involved in neural tube closure 1 4.15E-02
G0:0031167 BP rRNA methylation 1 4.18E-02
G0:0007398 BP ectoderm development 1 4.18E-02
G0:0007224 BP smoothened signaling pathway 2 4.21E-02
G0:0044765 BP single-organism transport 13 4.24E-02
G0:0061436 BP establishment of skin barrier 1 4.24E-02
G0:0007625 BP grooming behavior 1 4.24E-02
G0:0072330 BP monocarboxylic acid biosynthetic process 2 4.25E-02
G0:0060037 BP pharyngeal system development 1 4.25E-02
G0:0031672 CC A band 1 4.29E-02
G0:0070062 CC extracellular exosome 11 4.29E-02
G0:1903561 CC extracellular vesicle 11 4.29E-02
G0:1901215 BP negative regulation of neuron death 2 4.29E-02
G0:0043931 BP ossification involved in bone maturation 1 4.30E-02
G0:0070977 BP bone maturation 1 4.30E-02
G0:0043230 CC extracellular organelle 11 4.30E-02
GO:0065010 CC extracellular membrane-bounded organelle 11 4.30E-02
GO:0008158 MF hedgehog receptor activity 1 4.31E-02
GO:0045087 BP innate immune response 3 4.38E-02
GO:0033006 BP regulation of mast cell activation involved in immune response 1 4.42E-02
GO:0051649 BP establishment of localization in cell 9 4.42E-02
GO:0031579 BP membrane raft organization 1 4.45E-02
GO:0000154 BP rRNA modification 1 4.48E-02
GO:0090177 BP establishment of planar polarity involved in neural tube closure 1 4.51E-02
GO:0033561 BP regulation of water loss via skin 1 4.54E-02
GO:0033119 BP negative regulation of RNA splicing 1 4.55E-02
GO:0008514 MF organic anion transmembrane transporter activity 2 4.56E-02
GO:0006006 BP glucose metabolic process 2 4.56E-02
GO:0009895 BP negative regulation of catabolic process 2 4.57E-02
GO:0015095 MF magnesium ion transmembrane transporter activity 1 4.57E-02
GO:0004871 MF signal transducer activity 7 4.58E-02
GO:0003854 MF 3-beta-hydroxy-delta5-steroid dehydrogenase activity 1 4.62E-02
GO:0072006 BP nephron development 2 4.62E-02
GO:2000647 BP negative regulation of stem cell proliferation 1 4.67E-02
GO:0001655 BP urogenital system development 3 4.67E-02
GO:0051181 BP cofactor transport 1 4.70E-02
GO:0060562 BP epithelial tube morphogenesis 3 4.70E-02
GO:0007623 BP circadian rhythm 2 4.71E-02
GO:0015693 BP magnesium ion transport 1 4.73E-02
GO:2000178 BP negative regulation of neural precursor cell proliferation 1 4.75E-02
GO:0016358 BP dendrite development 2 4.76E-02
GO:0010874 BP regulation of cholesterol efflux 1 4.78E-02
GO:0034105 BP positive regulation of tissue remodeling 1 4.79E-02
GO:0042249 BP establishment of planar polarity of embryonic epithelium 1 4.81E-02
GO:0004683 MF calmodulin-dependent protein kinase activity 1 4.82E-02
GO:0044700 BP single organism signaling 18 4.85E-02
GO:0048670 BP regulation of collateral sprouting 1 4.85E-02
GO:0033630 BP positive regulation of cell adhesion mediated by integrin 1 4.85E-02
GO:0032228 BP regulation of synaptic transmission, GABAergic 1 4.86E-02
GO:0000184 BP nuclear-transcribed mRNA catabolic process, nonsense-mediated decay 1 4.87E-02
GO:0002446 BP neutrophil mediated immunity 1 4.88E-02
GO:0023052 BP signaling 18 4.90E-02
GO:0042554 BP superoxide anion generation 1 4.94E-02
GO:0008038 BP neuron recognition 1 4.95E-02
GO:0009620 BP response to fungus 1 5.03E-02
GO:0071526 BP semaphorin-plexin signaling pathway 1 5.05E-02
GO:0005215 MF transporter activity 7 5.07E-02
GO:0006110 BP regulation of glycolytic process 1 5.08E-02
N: The enrichment number of genes; MF: molecular function; BP: biological process; CC: cellular component
Supplementary Table 5. KEGG pathway analysis of genes showing significant selection in TY chickens
Term jP Input Background number number P-Value Hyperlink
Hedgehog signaling pathway gga04340 3 45 1.78E-03 http://www.2enome.ip/ke22-bin/show pathway?22a04340/22a:770168%09red/2ga:395806%09red
Pentose phosphate pathway gga00030 2 21 5.90E-03 http://www.genome.Jp/kegg-bin/show_pathway7gga00030/gga:395218%09red/gga:395217%09red
Fructose and mannose metabolism gga00051 2 32 1.26E-02 http://www.genome.Jp/kegg-bin/show_pathway7gga00051/gga:395218%09red/gga:395217%09red
Valine, leucine and isoleucine degradation gga00280 2 41 1.97E-02 http://www.genome.Jp/kegg-bin/show_pathway7gga00280/gga:396316%09red/gga:427269%09red
Insulin signaling pathway gga04910 3 118 2.29E-02 http://www.2enome.ip/ke22- bin/show pathway?22a04910/22a:431265%09red/22a:395218%09red/22a:395217%09red
Fanconi anemia pathway gga03460 2 48 2.62E-02 http://www.genome.Jp/kegg-bin/show_pathway7gga03460/gga:427468%09red/gga:101750641%09red
Glycolysis / Gluconeogenesis gga00010 2 50 2.82E-02 http://www.genome.Jp/kegg-bin/show_pathway7gga00010/gga:395218%09red/gga:395217%09red
Synthesis and degradation of ketone bodies gga00072 1 9 4.93E-02 http://www.genome.jp/kegg-bin/show pathway?gga00072/gga:396316%09red
Carbon metabolism gga01200 2 90 7.84E-02 http://www.genome.Jp/kegg-bin/show_pathway7gga01200/gga:395218%09red/gga:395217%09red
Other glycan degradation gga00511 1 18 9.17E-02 http://www.genome.jp/kegg-bin/show pathway?gga00511/gga:419687%09red
Fatty acid elongation gga00062 1 20 1.01E-01 http://www.genome.Jp/kegg-bin/show pathway?gga00062/gga:419681%09red
Lysosome gga04142 2 107 1.05E-01 http://www.genome.Jp/kegg-bin/show_pathway7gga04142/gga:419681%09red/gga:427466%09red
Butanoate metabolism gga00650 1 23 1.14E-01 http://www.genome.Jp/kegg-bin/show pathway?gga00650/gga:396316%09red
Jak-STAT signaling pathway gga04630 2 125 1.34E-01 http://www.genome.Jp/kegg-bin/show_pathway7gga04630/gga:419692%09red/gga:419694%09red
Galactose metabolism gga00052 1 32 1.54E-01 http://www.genome.Jp/kegg-bin/show pathway?gga00052/gga:419686%09red
Fatty acid metabolism gga01212 1 42 1.96E-01 http://www. genome .J p/kegg-bin/show pathway?gga01212/gga:419681 %09red
Amino sugar and nucleotide sugar metabolism gga00520 1 44 2.04E-01 http://www.genome.Jp/kegg-bin/show pathway?gga00520/gga:419686%09red
Cytokine-cytokine receptor interaction gga04060 2 165 2.06E-01 http://www.genome.Jp/ke22-bin/show pathway?22a04060/22a:419692%09red/gga:419694%09red
Lysine degradation gga00310 1 45 2.08E-01 http://www.genome.Jp/kegg-bin/show pathway?gga00310/gga:426932%09red
Peroxisome gga04146 1 74 3.17E-01 http://www.genome.Jp/kegg-bin/show pathway?gga04146/gga:396316%09red
ErbB signaling pathway gga04012 1 77 3.27E-01 http://www.genome.Jp/kegg-bin/show pathway?gga04012/gga:431265%09red
Glycerophospholipid metabolism gga00564 1 86 3.57E-01 http://www.genome.Jp/kegg-bin/show pathway?gga00564/gga:419685%09red
Neuroactive ligand-receptor interaction gga04080 2 261 3.85E-01 http://www.genome.Jp/kegg-bin/show_pathway7gga04080/gga:431264%09red/gga:428232%09red
Spliceosome gga03040 1 105 4.17E-01 http://www.genome.Jp/kegg-bin/show pathway?gga03040/gga:419689%09red http://www. genome .J p/kegg-
Metabolic pathways gga01100 6 1049 4.44E-01 bin/show_pathway?gga01100/gga:395217%09red/gga:419681%09red/gga:395218%09red/gga:419686%09 red/gga:427269%09red/gga:396316%09red
Phagosome gga04145 1 127 4.79E-01 http://www.genome.Jp/kegg-bin/show pathway?gga04145/gga:427466%09red
Protein processing in endoplasmic reticulum gga04141 1 146 5.27E-01 http://www.genome.Jp/kegg-bin/show pathway?gga04141/gga:771022%09red
Focal adhesion gga04510 1 184 6.11E-01 http://www.2enome.ip/ke22-bin/show pathway?22a04510/22a:431265%09red
MAPK signaling pathway gga04010 1 214 6.67E-01 http://www.2enome.ip/ke22- bin/show pathway?22a04010/22a:396186%09red
nBIWHRftHSMBil Liao Y, Sun J, Huang Y, Wei F, Mo G, Zellmer L and Liao DJ (2020). Genomic Analysis Reveals Strong Signatures of Selection in Guangxi Three-Yellow Chicken in China. J. World Poult. Res., 10 (3): 407-428. DOI: https://dx.doi.org/10.36380/jwpr.2020.48
