Turn off MathJax
Article Contents
Xiao-Ning Zhu, Yu-Zhe Wang, Chong Li, Han-Yu Wu, Ran Zhang, Xiao-Xiang Hu. Chicken chromatin accessibility atlas accelerates epigenetic annotation of birds and gene fine-mapping associated with growth traits. Zoological Research, 2023, 44(1): 53-62. doi: 10.24272/j.issn.2095-8137.2022.228
Citation: Xiao-Ning Zhu, Yu-Zhe Wang, Chong Li, Han-Yu Wu, Ran Zhang, Xiao-Xiang Hu. Chicken chromatin accessibility atlas accelerates epigenetic annotation of birds and gene fine-mapping associated with growth traits. Zoological Research, 2023, 44(1): 53-62. doi: 10.24272/j.issn.2095-8137.2022.228

Chicken chromatin accessibility atlas accelerates epigenetic annotation of birds and gene fine-mapping associated with growth traits

doi: 10.24272/j.issn.2095-8137.2022.228
All new sequence reads were deposited in the National Center for Biotechnology Information (NCBI) sequence read archive (SRA) under BioProjectID PRJNA847569, in the Genome Sequence Archive under Accession No. CRA008349, and in the Science Data Bank under DOI: 10.57760/sciencedb.02970. All data generated in this study are available within the article and its Supplementary Data files.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
Y.Z.W. and X.X.H. conceived and designed the study and conducted the primary analyses. X.N.Z. collected samples and performed the experiments. C.L. carried out experimental verification. X.X.H., H.Y.W., and R.Z. helped analyze and interpret the data. Y.Z.W. wrote the initial manuscript. X.N.Z. and X.X.H. were responsible for statistical analyses and manuscript revision. All authors read and approved the final version of the manuscript.
Funds:  This study was supported by the National Natural Science Foundation of China (U2002205, 32272862)
More Information
  • The development of epigenetic maps, such as the ENCODE project in humans, provides resources for gene regulation studies and a reference for research of disease-related regulatory elements. However, epigenetic information, such as a bird-specific chromatin accessibility atlas, is currently lacking for the thousands of bird species currently described. The major genomic difference between birds and mammals is their shorter introns and intergenic distances, which seriously hinders the use of humans and mice as a reference for studying the function of important regulatory regions in birds. In this study, using chicken as a model bird species, we systematically compiled a chicken chromatin accessibility atlas using 53 Assay of Transposase Accessible Chromatin sequencing (ATAC-seq) samples across 11 tissues. An average of 50 796 open chromatin regions were identified per sample, cumulatively accounting for 20.36% of the chicken genome. Tissue specificity was largely reflected by differences in intergenic and intronic peaks, with specific functional regulation achieved by two mechanisms: recruitment of several sequence-specific transcription factors and direct regulation of adjacent functional genes. By integrating data from genome-wide association studies, our results suggest that chicken body weight is driven by different regulatory variants active in growth-relevant tissues. We propose CAB39L (active in the duodenum), RCBTB1 (muscle and liver), and novel long non-coding RNA ENSGALG00000053256 (bone) as candidate genes regulating chicken body weight. Overall, this study demonstrates the value of epigenetic data in fine-mapping functional variants and provides a compendium of resources for further research on the epigenetics and evolution of birds and mammals.
  • All new sequence reads were deposited in the National Center for Biotechnology Information (NCBI) sequence read archive (SRA) under BioProjectID PRJNA847569, in the Genome Sequence Archive under Accession No. CRA008349, and in the Science Data Bank under DOI: 10.57760/sciencedb.02970. All data generated in this study are available within the article and its Supplementary Data files.
    Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    Y.Z.W. and X.X.H. conceived and designed the study and conducted the primary analyses. X.N.Z. collected samples and performed the experiments. C.L. carried out experimental verification. X.X.H., H.Y.W., and R.Z. helped analyze and interpret the data. Y.Z.W. wrote the initial manuscript. X.N.Z. and X.X.H. were responsible for statistical analyses and manuscript revision. All authors read and approved the final version of the manuscript.
  • loading
  • [1]
    Barefield DY, Puckelwartz MJ, Kim EY, Wilsbacher LD, Vo AH, Waters EA, et al. 2017. Experimental modeling supports a role for MyBP-HL as a novel myofilament component in arrhythmia and dilated cardiomyopathy. Circulation, 136(16): 1477−1491. doi: 10.1161/CIRCULATIONAHA.117.028585
    [2]
    Bikle DD. 2020. The vitamin D receptor as tumor suppressor in skin. Advances in Experimental Medicine and Biology, 1268: 285−306.
    [3]
    Boyle EA, Li YI, Pritchard JK. 2017. An expanded view of complex traits: from polygenic to omnigenic. Cell, 169(7): 1177−1186. doi: 10.1016/j.cell.2017.05.038
    [4]
    Buenrostro JD, Wu BJ, Litzenburger UM, Ruff D, Gonzales ML, Snyder MP, et al. 2015. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature, 523(7561): 486−490. doi: 10.1038/nature14590
    [5]
    Carter B, Zhao KJ. 2021. The epigenetic basis of cellular heterogeneity. Nature Reviews Genetics, 22(4): 235−250. doi: 10.1038/s41576-020-00300-0
    [6]
    Corces MR, Trevino AE, Hamilton EG, Greenside PG, Sinnott-Armstrong NA, Vesuna S, et al. 2017. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nature Methods, 14(10): 959−962. doi: 10.1038/nmeth.4396
    [7]
    Foissac S, Djebali S, Munyard K, Vialaneix N, Rau A, Muret K, et al. 2019. Multi-species annotation of transcriptome and chromatin structure in domesticated animals. BMC Biology, 17(1): 108. doi: 10.1186/s12915-019-0726-5
    [8]
    Giuffra E, Tuggle CK, FAANG Consortium. 2019. Functional annotation of animal genomes (FAANG): current achievements and roadmap. Annual Review of Animal Biosciences, 7: 65−88. doi: 10.1146/annurev-animal-020518-114913
    [9]
    Gorkin DU, Barozzi I, Zhao Y, Zhang YX, Huang H, Lee AY, et al. 2020. An atlas of dynamic chromatin landscapes in mouse fetal development. Nature, 583(7818): 744−751. doi: 10.1038/s41586-020-2093-3
    [10]
    Groß C, Bortoluzzi C, de Ridder D, Megens HJ, Groenen MAM, Reinders M, et al. 2020. Prioritizing sequence variants in conserved non-coding elements in the chicken genome using chCADD. PLoS Genetics, 16(9): e1009027. doi: 10.1371/journal.pgen.1009027
    [11]
    Guo DF, Tardif V, Ghelima K, Chan JSD, Ingelfinger JR, Chen XM, et al. 2004. A novel angiotensin II type 1 receptor-associated protein induces cellular hypertrophy in rat vascular smooth muscle and renal proximal tubular cells. Journal of Biological Chemistry, 279(20): 21109−21120. doi: 10.1074/jbc.M401544200
    [12]
    Halstead MM, Kern C, Saelao P, Chanthavixay G, Wang Y, Delany ME, et al. 2020a. Systematic alteration of ATAC-seq for profiling open chromatin in cryopreserved nuclei preparations from livestock tissues. Scientific Reports, 10(1): 5230. doi: 10.1038/s41598-020-61678-9
    [13]
    Halstead MM, Kern C, Saelao P, Wang Y, Chanthavixay G, Medrano JF, et al. 2020b. A comparative analysis of chromatin accessibility in cattle, pig, and mouse tissues. BMC Genomics, 21(1): 698. doi: 10.1186/s12864-020-07078-9
    [14]
    Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell, 38(4): 576−589. doi: 10.1016/j.molcel.2010.05.004
    [15]
    Hitachi K, Inagaki H, Kurahashi H, Okada H, Tsuchida K, Honda M. 2019. Deficiency of Vgll2 gene alters the gene expression profiling of skeletal muscle subjected to mechanical overload. Frontiers in Sports and Active Living, 1: 41. doi: 10.3389/fspor.2019.00041
    [16]
    Hutton SR, Pevny LH. 2011. SOX2 expression levels distinguish between neural progenitor populations of the developing dorsal telencephalon. Developmental Biology, 352(1): 40−47. doi: 10.1016/j.ydbio.2011.01.015
    [17]
    Jiang LD, Zheng ZL, Qi T, Kemper KE, Wray NR, Visscher PM, et al. 2019. A resource-efficient tool for mixed model association analysis of large-scale data. Nature Genetics, 51(12): 1749−1755. doi: 10.1038/s41588-019-0530-8
    [18]
    Kern C, Wang Y, Xu XQ, Pan ZY, Halstead M, Chanthavixay G, et al. 2021. Functional annotations of three domestic animal genomes provide vital resources for comparative and agricultural research. Nature Communications, 12(1): 1821. doi: 10.1038/s41467-021-22100-8
    [19]
    Lai YC, Liang YC, Jiang TX, Widelitz RB, Wu P, Chuong CM. 2018. Transcriptome analyses of reprogrammed feather / scale chimeric explants revealed co-expressed epithelial gene networks during organ specification. BMC Genomics, 19(1): 780. doi: 10.1186/s12864-018-5184-x
    [20]
    Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
    [21]
    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2078−2079. doi: 10.1093/bioinformatics/btp352
    [22]
    Li M, Sun CJ, Xu NY, Bian PP, Tian XM, Wang XH, et al. 2022. De novo assembly of 20 chicken genomes reveals the undetectable phenomenon for thousands of core genes on microchromosomes and subtelomeric regions. Molecular Biology and Evolution, 39(4): msac066. doi: 10.1093/molbev/msac066
    [23]
    Liu CY, Wang MY, Wei XY, Wu L, Xu JS, Dai X, et al. 2019. An ATAC-seq atlas of chromatin accessibility in mouse tissues. Scientific Data, 6(1): 65. doi: 10.1038/s41597-019-0071-0
    [24]
    Luo W, Li EX, Nie QH, Zhang XQ. 2015. Myomaker, regulated by MYOD, MYOG and miR-140-3p, promotes chicken myoblast fusion. International Journal of Molecular Sciences, 16(11): 26186−26201. doi: 10.3390/ijms161125946
    [25]
    Martin M. 2011. CUTADAPT removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal, 17(1): 10−12. doi: 10.14806/ej.17.1.200
    [26]
    Ou JH, Liu HB, Yu J, Kelliher MA, Castilla LH, Lawson ND, et al. 2018. ATACseqQC: a Bioconductor package for post-alignment quality assessment of ATAC-seq data. BMC Genomics, 19(1): 169. doi: 10.1186/s12864-018-4559-3
    [27]
    Pan ZY, Yao YL, Yin HW, Cai ZX, Wang Y, Bai LJ, et al. 2021. Pig genome functional annotation enhances the biological interpretation of complex traits and human disease. Nature Communications, 12(1): 5848. doi: 10.1038/s41467-021-26153-7
    [28]
    Patoori S, Jean-Charles N, Gopal A, Sulaiman S, Gopal S, Wang B, et al. 2020. Cis-regulatory analysis of Onecut1 expression in fate-restricted retinal progenitor cells. Neural Development, 15(1): 5. doi: 10.1186/s13064-020-00142-w
    [29]
    Pérez C, Dastot-Le Moal F, Collot N, Legendre M, Abadie I, Bertrand AM, et al. 2012. Screening of LHX2 in patients presenting growth retardation with posterior pituitary and ocular abnormalities. European Journal of Endocrinology, 167(1): 85−91. doi: 10.1530/EJE-12-0026
    [30]
    Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81(3): 559−575. doi: 10.1086/519795
    [31]
    Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26(6): 841−842. doi: 10.1093/bioinformatics/btq033
    [32]
    Ramírez F, Ryan DP, Grüning B, Bhardwaj V, Kilpert F, Richter AS, et al. 2016. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Research, 44(W1): W160−W165. doi: 10.1093/nar/gkw257
    [33]
    Roadmap Epigenomics Consortium, Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, et al. 2015. Integrative analysis of 111 reference human epigenomes. Nature, 518(7539): 317−330. doi: 10.1038/nature14248
    [34]
    Rothstein M, Simoes-Costa M. 2020. Heterodimerization of TFAP2 pioneer factors drives epigenomic remodeling during neural crest specification. Genome Research, 30(1): 35−48. doi: 10.1101/gr.249680.119
    [35]
    Sackton TB, Grayson P, Cloutier A, Hu ZR, Liu JS, Wheeler NE, et al. 2019. Convergent regulatory evolution and loss of flight in paleognathous birds. Science, 364(6435): 74−78. doi: 10.1126/science.aat7244
    [36]
    Schug J, Schuller WP, Kappen C, Salbaum JM, Bucan M, Stoeckert CJ Jr. 2005. Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biology, 6(4): R33. doi: 10.1186/gb-2005-6-4-r33
    [37]
    Seki R, Li C, Fang Q, Hayashi S, Egawa S, Hu J, et al. 2017. Functional roles of Aves class-specific cis-regulatory elements on macroevolution of bird-specific features. Nature Communications, 8: 14229. doi: 10.1038/ncomms14229
    [38]
    Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, et al. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature, 488(7409): 116−120. doi: 10.1038/nature11243
    [39]
    The ENCODE Project Consortium. 2004. The ENCODE (ENCyclopedia of DNA Elements) project. Science, 306(5696): 636−640. doi: 10.1126/science.1105136
    [40]
    The ENCODE Project Consortium, Snyder MP, Gingeras TR, Moore JE, Weng ZP, Gerstein MB, et al. 2020. Perspectives on ENCODE. Nature, 583(7818): 693−698. doi: 10.1038/s41586-020-2449-8
    [41]
    Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, et al. 2015. Proteomics. Tissue-based map of the human proteome. Science, 347(6220): 1260419. doi: 10.1126/science.1260419
    [42]
    Wang MS, Thakur M, Peng MS, Jiang Y, Frantz LAF, Li M, et al. 2020a. 863 genomes reveal the origin and domestication of chicken. Cell Research, 30(8): 693−701. doi: 10.1038/s41422-020-0349-y
    [43]
    Wang YZ, Bu LN, Cao XM, Qu H, Zhang CY, Ren JL, et al. 2020b. Genetic dissection of growth traits in a unique chicken advanced intercross line. Frontiers in Genetics, 11: 894. doi: 10.3389/fgene.2020.00894
    [44]
    Wang YZ, Cao XM, Luo CL, Sheng ZY, Zhang CY, Bian C, et al. 2020c. Multiple ancestral haplotypes harboring regulatory mutations cumulatively contribute to a QTL affecting chicken growth traits. Communications Biology, 3(1): 472. doi: 10.1038/s42003-020-01199-3
    [45]
    Wu Z, Bortoluzzi C, Derks MFL, Liu LQ, Bosse M, Hiemstra SJ, et al. 2021. Heterogeneity of a dwarf phenotype in Dutch traditional chicken breeds revealed by genomic analyses. Evolutionary Applications, 14(4): 1095−1108. doi: 10.1111/eva.13183
    [46]
    Xu M, Xie XL, Dong XH, Liang GQ, Gan L. 2018. Generation and characterization of Lhx3GFP reporter knockin and Lhx3loxP conditional knockout mice. Genesis, 56(4): e23098. doi: 10.1002/dvg.23098
    [47]
    Xue Q, Zhang GX, Li TT, Ling JJ, Zhang XQ, Wang JY. 2017. Transcriptomic profile of leg muscle during early growth in chicken. PLoS One, 12(3): e0173824. doi: 10.1371/journal.pone.0173824
    [48]
    Yang J, Lee SH, Goddard ME, Visscher PM. 2011. GCTA: a tool for genome-wide complex trait analysis. American Journal of Human Genetics, 88(1): 76−82. doi: 10.1016/j.ajhg.2010.11.011
    [49]
    Yang RF, Guo XL, Zhu D, Tan C, Bian C, Ren JL, et al. 2021. Accelerated deciphering of the genetic architecture of agricultural economic traits in pigs using a low-coverage whole-genome sequencing strategy. GigaScience, 10(7): giab048. doi: 10.1093/gigascience/giab048
    [50]
    Young JJ, Grayson P, Edwards SV, Tabin CJ. 2019. Attenuated Fgf signaling underlies the forelimb heterochrony in the Emu Dromaius novaehollandiae. Current Biology, 29(21): 3681−3691.e5. doi: 10.1016/j.cub.2019.09.014
    [51]
    Yue F, Cheng Y, Breschi A, Vierstra J, Wu WS, Ryba T, et al. 2014. A comparative encyclopedia of DNA elements in the mouse genome. Nature, 515(7527): 355−364. doi: 10.1038/nature13992
    [52]
    Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, et al. 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215): 1311−1320. doi: 10.1126/science.1251385
    [53]
    Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biology, 9(9): R137. doi: 10.1186/gb-2008-9-9-r137
    [54]
    Zhao YX, Hou Y, Xu YY, Luan Y, Zhou HH, Qi XL, et al. 2021. A compendium and comparative epigenomics analysis of cis-regulatory elements in the pig genome. Nature Communications, 12(1): 2217. doi: 10.1038/s41467-021-22448-x
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(4)  / Tables(1)

    Article Metrics

    Article views (823) PDF downloads(155) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return