- Currently, there is a huge paucity in knowledge of the genetic determinants responsible for phenotypic and biochemical properties of these iconic chickens. - This study aimed to uncover the genetic structure and the molecular underpinnings of the YFCs trademark coloration.. - Through genome-wide scans for selective sweeps, we identified RALY heterogeneous nuclear ribonucleoprotein (RALY), leucine rich repeat containing G protein-coupled receptor 4 (LGR4), solute carrier family 23 member 2 (SLC23A2), and solute carrier family 2 member 14 (SLC2A14), besides the classical beta-carotene dioxygenase 2 (BCDO2), as major candidates pigment determining genes in the YFCs.. - The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. - If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. - 1 Guangdong Provincial Key Laboratory of Conservation and Precision Utilization of Characteristic Agricultural Resources in Mountainous Areas, Guangdong Innovation Centre for Science and Technology of Wuhua Yellow Chicken, School of Life Science of Jiaying University, Meizhou 514015, China Full list of author information is available at the end of the article Huang et al. - Conclusion: We provide the first comprehensive genomic data of the YFCs. - Our analyses show phylogeographical patterns among the YFCs and potential candidate genes giving rise to the yellow color trait of the YFCs. - YFCs have been de- scribed in the ancient Chinese agricultural text “ Qimin Yaoshu ” written around 540 C.E [3], and their import- ance is evidenced by the incredible leap in their demand.. - For instance, the production of YFC meat in China reached 4445 kt in 2015, representing 31.8% of the na- tional broiler meat yields [4]. - In addition to serving as a traditional nutritional and commercial mainstay for mil- lions of people living in China and its purlieus, YFCs are reported to have contributed to the recent breeding of European chickens [5], indicating a broadening utility of the YFCs. - Hardly any genome-wide investigations of the population structure and genetic basis of the unique YFC phenotypic traits have been con- ducted, a major drawback in rational improvement and conservation of these chickens.. - We also aimed to implement comparative population genetic analyses to determine the genetic structure of the YFCs and retrieve the footprints of selection for their unique color property. - Characteristics of the genome datasets. - We performed an initial in-depth characterization of the genomes of the 100 YFCs from 10 different breeds and 10 Huaibei (HB) partridge chickens (used for comparisons) sequenced in this study ( Fig. - Genome variants in the yellow-feathered chickens After filtration single nucleotide polymorphisms (SNPs) and 1,289,024 InDels (insertion or deletion of bases. - The structural variations (SVs) and the increase or decrease of the copy number of large (>. - All these genomic variants in the newly generated dataset are summarized in Additional file 4: Fig. - Briefly, most of the SNPs are lo- cated in intergenic followed by intronic genomic regions (Additional file 4: Fig. - 28.98%) in the dataset. - Different transversions show a low but relatively uniform distri- bution rate in the dataset. - Analysis of the heterogeneity of clean SNPs shows that about 2,033,275 and 2,259,628 SNPs per genome are homogenous and heterozygous hybrids, respect- ively (Additional file 7).. - Addition- ally, the four most common genomic consequences of the InDels include frameshift or non-frameshift insertions and deletions (Additional file 4: Fig. - Intrachro- mosomal translocations (65%) and deletions (26%) are pre- dominant in the dataset, while inversions and interchromosomal translocations are present in lower. - 1 Population genomic analysis of the YFCs. - In the PCA (Fig. - These patterns imply a close congruity in the total genomic architecture of the YFCs.. - 2c and d) corroborates the findings of the PCA and further clarifies the northern, central, and southern YFC cluster- ing pattern inferred from Fig. - Genome-wide scans for signals of selection attributable to the YFCs phenotype identified 268 analytical windows within the top 1% of the Locus-specific branch length (LSBL) test, and 370 windows in the π-ratio test (Additional files 10 and 11).. - A total of 28 PSGs were concurrently identified in the top 1% by the two selection tests (Fig. - This is a relatively small overlap, possibly owing to the differ- ences in the selection tests. - There are additional genes above the top 1% significance threshold in either of the selection tests. - These genes are im- portant for understanding the color trait and other properties of interest like meat quality of the YFCs. - and GDF8, HSPA5, SHISA9, COL4A1, and COL23A1 in the π-ratio test (Fig. - We also describe the genetic structure and molecular back- ground of the distinguished color phenotype of these chickens. - In this study, we characterize not only the SNPs in the genomes of the YFCs but also other variants including InDels, structural variations (SV), and copy number variations (CNV) to facilitate re- search of these chickens. - Our current comparative population genomics analysis was anchored on genome-wide SNPs of the YFCs, other indigenous chickens, and wild ancestors. - Population struc- ture analysis revealed an overall distinctive genomic archi- tecture of the YFCs from other Chinese indigenous chickens (PCA and NJ phylogenetic tree). - Interestingly, a three-way sub-clustering pattern is consistent in PCA, ADMIXTURE, and NJ phylogenetic tree and amazingly mirrors the geographical distributions of the YFCs. - A crucial point to note is the signals of admixture at K = 3 and 4 in the ADMIXTURE analysis. - The results of PCA and ADMIXTURE (K = 2 and 3) suggest that the Huaibei (HB) partridge chickens have a close relationship with YFCs of the northern cluster, consistent with their geographical proximity. - Compared to other indigenous Chinese chickens, the YFCs tend have a closer genetic semblance among themselves than with other chickens, inferring a possible overriding effect of se- lection for the outstanding phenotypic traits of the YFCs.. - 2 Population genomic analysis of YFCs in the context of other Chinese indigenous chickens. - selection in the YFCs, having significant signals both in LSBL and π-ratio scans. - 90 kb deletion upstream of avian ASIP, encompassing portions of the RALY locus, places ASIP under the regulatory control of RALY promoter [40].. - We detected two members of the solute car- rier family (SLC), SLC23A2 and SLC2A14. - SLC23A2 is a major mediator of the transport of ascorbic acid, an indis- pensable metabolite that is fundamental for survival [42].. - Anomalies in the availability of this vitamin have been asso- ciated with neonatal jaundice and yellow chromophore in eye lenses of human and humanized mouse model [43, 44].. - a PSGs in the top 1% windows of LSBL and π -ratio genome selection tests. - b Summary of the functional enrichment analysis of the 28 overlapping PSGs. - ASIP and MC1R in the determination of the yellow color trait of the YFCs.. - From the selection sweep analysis, it was not a surprise to detect a strong selection for the BCDO2 gene and a common genetic architecture of the gene among all the YFCs. - Even the HB chickens which are phylogenetically and geographically close to the YFCs in the northern clus- ter were clearly distinguishable based on the BCDO2 haplotype structure, depicting a possible marked differen- tiation of indigenous chickens at trait-linked genome compartment under selection pressure, despite likely closeness at the total genome level. - all bearing strong selection signals in the YFCs, are important determinants of meat quality in domestic ani- mals. - These genes provide a foundation for understand- ing the meat properties of the YFCs, which would attract more concerns to investigate the detailed func- tion roles in future studies.. - Samplings and sequencing of the yellow-feathered chickens. - Further quality control processes were performed using the SortSam and Mark- Duplicates tools in the Picards package (picard-tools- 1.56) to sort and remove possible duplicates in the aligned BAM files, and the RealignerTargetCreator, IndelRealigner, and BaseRecalibrator tools in the Gen- ome Analysis Toolkit (GATK for local re- alignment and base quality recalibration. - Haplotype pattern analysis of the yellow skin gene, BCDO2 across different populations separated by white gaps. - Initials represent chicken breeds/population names as defined in the methods. - To perform a compara- tive analysis of the YFC genomes generated in this study against those of other chicken populations, 104 previously published whole genomes [13, 14] of Chinese indigenous chickens (Sichuan, n = 50. - After merging our dataset of the 110 chicken genomes with the add- itional 115 genomes common SNPs were retained for subsequent analyses. - Genomic targets of selection in yellow-feathered chickens To retrieve the genetic foundation for the outstanding phenotypic properties of the YFCs, we performed genome-wide scans for signals of selection using locus- specific branch length (LSBL) statistics [67] and π-ratio.. - Use of multiple statistical approaches helps to manage inherent differences of individual tests and increase the reliability of the selective sweep detection [68]. - The comparative genomic analysis approach involved ge- nomes of the YFCs against 24 chickens with contrasting non-yellow phenotypes (non-YFCs), i.e. - In the LSBL, we computed LSBL(A;B,C. - Profiler [72] to obtain a global overview on the biological functions of the candidate PSGs with concordantly sig- nificant selection signals in the two genomic selection scans employed. - Assessment of the classical yellow skin gene, BCDO2 BCDO2 gene, located in chromosome reverse strand (Galgal5, [54. - We evaluated the haplotype variability of BCDO2 gene and its flanking genes, a stretch of the genome from chromosome . - S2 Summary of the average sequencing coverage of all 110 chicken genomes generated in this study. - S4 Annotation of the clean genomic SNPs of all 110 chickens sequenced in this study. - S5 Transition-transversion analysis of the clean SNPs of all 110 chicken genomes sequenced in this study. - S6 Annotation of the clean InDels of all 110 chicken genomes sequenced in this study. - S7 Summary of the structural variations (SVs) and copy number variations (CNVs) in all 110 chicken genomes gen- erated in this study.. - Annotation of the hybrid status of SNPs in each chicken genome sequenced in this study.. - Annotation of structural variations in the chicken genomes sequenced in this study.. - Annotation of copy number variations in the chicken genomes sequenced in this study.. - The top 1% genomic windows in the selection scan by LSBL test.. - The top 1% genomic windows in the selection scan by π -ratio test.. - NO, MP, ZW and XH performed data analysis, interpretation of results, and writing of the manuscript. - The funding bodies did not participate in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.. - All new sequencing data generated in this study have been deposited in the NCBI sequence read archive (SRA) under accession number SRP155577.. - Chicken art – ancient Chinese wisdom on chicken-raising with an appendix of the Chinese art of calligraphy.. - 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Characterization of Japanese quail yellow as a genomic deletion upstream of the avian homolog of the mammalian ASIP (agouti) gene. - Temporo-spacial microanatomical distribution of the murine sodium-dependent ascorbic acid transporters Slc23a1 and. - Slc23a2 in the kidney throughout development. - A new single nucleotide polymorphism in the ryanodine gene of chicken skeletal muscle. - Pale, soft, exudative Turkey — the role of ryanodine receptor variation in meat quality. - Polymorphisms in the promoter region of myostatin gene are associated with carcass traits in pigs. - In: proceedings of the eighth international workshop on algorithms in bioinformatics: 15 – 19 September 2008.. - Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken.
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