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Hair follicles transcriptome profiles in Bashang long-tailed chickens with different plumage colors

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A Correction to this article was published on 27 May 2019

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Abstract

Despite the rich variety in plumage color found in nature, genetic studies on how hair follicles affect pigmentation are often limited to animals that have black and white pigment. To test how gene expression influences plumage color, transcriptomes of chicken hair follicles with white, black, hemp, reed catkins, silvery grey, and landscape plumage colors were generated using Illumina sequencing. We generated six RNA-Seq libraries with over 25 million paired-end clean reads per library with percentage of paired-end clean reads ranging from 96.73 to 96.98%. 78% of the reads mapped to the chicken genome, and approximately 70% of the reads were mapped to exons and 6% mapped to introns. Transcriptomes of hair follicles producing hemp and land plumage were similar, but these two showed moderate differences compared with gray and reed colored plumage. The black and white follicle transcriptomes were most divergent from the other colors. We identified several candidate genes, including GPNMB, PMEL, TYRP1, GPR143, OCA2, SOX10, SLC45A2, KRT75, and TYR. All of these genes are known to induce pigment formation in mice. White feathers result from the lack of pigment formation, and our results suggest that the white chickens due to the recessive insertion mutation of TYR. The formation of black area size and color depth may be due to the expression levels of GPNMB, PMEL, TYRP1, GPR143, OCA2, SOX10, SLC45A2, KRT75, and TYR. The GO analysis of the differentially expressed genes (DEGs) revealed that DEGs in our transcriptome analysis were enriched in cytoskeleton and cell structure related pathways. The black plumage transcriptome showed significant differences in melanogenesis, tyrosine metabolism, and riboflavin metabolism compared with transcriptomes of other plumage colors. The transcriptome profiles of the different chicken plumage colors provide a valuable resource to understand how gene expression influences plumage color, and will be an important resource for identifying candidate genes in breeding programs.

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Change history

  • 27 May 2019

    The words ‘hair follicles’ was replaced with ‘feather follicles’ in the title and the main text.

References

  • Bennett DC, Lamoreux ML (2003) The color loci of mice–a genetic century. Pigm Cell Res 16:333–344

    CAS  Google Scholar 

  • Berryere T, Schmutz S, Schimpf R, Cowan C, Potter J (2003) TYRP1 is associated with dun coat colour in Dexter cattle or how now brown cow? Anim genet 34:169–175

    CAS  PubMed  Google Scholar 

  • Botchkarev VA, Kishimoto J (2003) Molecular control of epithelial–mesenchymal interactions during hair follicle cycling. J Investig Dermatol Symp Proc 8:46–55

    CAS  PubMed  Google Scholar 

  • Brunberg E, Andersson L, Cothran G, Sandberg K, Mikko S, Lindgren G (2006) A missense mutation in PMEL17 is associated with the Silver coat color in the horse. BMC Genet 7:46

    PubMed  PubMed Central  Google Scholar 

  • Candille S, Van Raamsdonk CD, Chen C, Kuijper S, Chen-Tsai Y, Russ A, Meijlink F, Barsh GS (2004) Dorsoventral patterning of the mouse coat by Tbx15. PLoS Biol 2:E3–E3

    PubMed  PubMed Central  Google Scholar 

  • Chang C-M, Coville J-L, Coquerelle G, Gourichon D, Oulmouden A, Tixier-Boichard M (2006a) Complete association between a retroviral insertion in the tyrosinase gene and the recessive white mutation in chickens. BMC Genomics 7:19

    PubMed  PubMed Central  Google Scholar 

  • Chang CM, Coville JL, Coquerelle G, Gourichon D, Oulmouden A, Tixier-Boichard M (2006b) Complete association between a retroviral insertion in the tyrosinase gene and the recessive white mutation in chickens. Bmc Genomics 7:19–19

    PubMed  PubMed Central  Google Scholar 

  • Charconnet-Harding F, Dalgliesh C, Neuberger A (1953) The relation between riboflavin and tryptophan metabolism, studied in the rat. Biochem J 53:513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cieslak M, Reissmann M, Hofreiter M, Ludwig A (2011) Colours of domestication. Biol Rev Camb Philos Soc 86:885–899

    PubMed  Google Scholar 

  • Clark LA, Wahl JM, Rees CA, Murphy KE (2006) Retrotransposon insertion in SILV is responsible for merle patterning of the domestic dog. Proc Natl Acad Sci USA 103:1376–1381

    CAS  PubMed  Google Scholar 

  • Costin GE, Valencia JC, Wakamatsu K, Ito S, Solano F, Milac AL, Vieira WD, Yamaguchi Y, Rouzaud F, Petrescu AJ et al (2005) Mutations in dopachrome tautomerase (Dct) affect eumelanin/pheomelanin synthesis, but do not affect intracellular trafficking of the mutant protein. Biochem J 391:249–259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    CAS  PubMed  Google Scholar 

  • Fernández A, Silió L, Rodríguez C, Ovilo C (2006) Characterization of OCA2 cDNA in different porcine breeds and analysis of its potential effect on skin pigmentation in a red Iberian strain. Anim Genet 37:166–170

    PubMed  Google Scholar 

  • Fontanesi L, Beretti F, Riggio V, Dall’Olio S, González E, Finocchiaro R, Davoli R, Russo V, Portolano B (2009) Missense and nonsense mutations in melanocortin 1 receptor (MC1R) gene of different goat breeds: association with red and black coat colour phenotypes but with unexpected evidences. BMC Genet 10:47

    PubMed  PubMed Central  Google Scholar 

  • Fontanesi L, Scotti E, Colombo M, Beretti F, Forestier L, Dall’Olio S, Deretz S, Russo V, Allain D, Oulmouden A (2010) A composite six bp in-frame deletion in the melanocortin 1 receptor (MC1R) gene is associated with the Japanese brindling coat colour in rabbits (Oryctolagus cuniculus). BMC Genet 11:59

    PubMed  PubMed Central  Google Scholar 

  • Fuchs E (2007) Scratching the surface of skin development. Nature 445:834–842

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao L, Dong CS, He XY, He JP, Geng JJ (2008) Gene expression levels of alpaca tyrosinase gene family in individuals of different colors. Chin J Anim Vet Sci 39:895–899

    CAS  Google Scholar 

  • Gutierrez-Gil B, Wiener P, Williams JL (2007) Genetic effects on coat colour in cattle: dilution of eumelanin and phaeomelanin pigments in an F2-Backcross Charolais × Holstein population. BMC Genet 8:56

    PubMed  PubMed Central  Google Scholar 

  • Guyonneau L, Murisier F, Rossier A, Moulin A, Beermann F (2004) Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Mol Cell Biol 24:3396–3403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Henderson LM, Weinstock I, Ramasarma G (1951) Effect of deficiency of B vitamins on the metabolism of tryptophan by the rat. J Biol Chem 189:19–29

    CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    CAS  PubMed  Google Scholar 

  • Kerje S, Sharma P, Gunnarsson U, Kim H, Bagchi S, Fredriksson R, Schutz K, Jensen P, von Heijne G, Okimoto R et al (2004) The Dominant white, Dun and Smoky color variants in chicken are associated with insertion/deletion polymorphisms in the PMEL17 gene. Genetics 168:1507–1518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Urabe K, Winder A, Jimenez-Cervantes C, Imokawa G, Brewington T, Solano F, Garcia-Borron J, Hearing V (1994) Tyrosinase related protein 1 (TRP1) functions as a DHICA oxidase in melanin biosynthesis. EMBO J 13:5818

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Imokawa G, Bennett DC, Hearing VJ (1998) Tyrosinase stabilization by Tyrp1 (the brown locus protein). J Biol Chem 273:31801–31805

    CAS  PubMed  Google Scholar 

  • Kühn C, Weikard R (2007) An investigation into the genetic background of coat colour dilution in a Charolais × German Holstein F2 resource population. Anim Genet 38:109–113

    PubMed  Google Scholar 

  • Li S, Wang C, Yu W, Zhao S, Gong Y (2012) Identification of genes related to white and black plumage formation by RNA-Seq from white and black feather bulbs in ducks. PLoS ONE 7:e36592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    CAS  Google Scholar 

  • Ludwig A, Pruvost M, Reissmann M, Benecke N, Brockmann GA, Castaños P, Cieslak M, Lippold S, Llorente L, Malaspinas A-S (2009) Coat color variation at the beginning of horse domestication. Science 324:485–485

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lyon MF, King TR, Gondo Y, Gardner JM, Nakatsu Y, Eicher EM, Brilliant MH (1992) Genetic and molecular analysis of recessive alleles at the pink-eyed dilution (p) locus of the mouse. Proc Natl Acad Sci USA 89:6968–6972

    CAS  PubMed  Google Scholar 

  • Lyons LA, Foe IT, Rah HC, Grahn RA (2005) Chocolate coated cats: TYRP1 mutations for brown color in domestic cats. Mamm Genome 16:356–366

    CAS  PubMed  Google Scholar 

  • Millar SE (2002) Molecular mechanisms regulating hair follicle development. J Invest Dermatol 118:216–225

    CAS  PubMed  Google Scholar 

  • Miwa M, Inoue-Murayama M, Aoki H, Kunisada T, Hiragaki T, Mizutani M, Ito S (2007) Endothelin receptor B2 (EDNRB2) is associated with the panda plumage colour mutation in Japanese quail. Anim Genet 38:103–108

    CAS  PubMed  Google Scholar 

  • Mockus SM, Vrana KE (1998) Advances in the molecular characterization of tryptophan hydroxylase. J Mol Neurosci 10:163–179

    CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Methods 5:621–628

    CAS  Google Scholar 

  • Murisier F, Guichard S, Beermann F (2007) The tyrosinase enhancer is activated by Sox10 and Mitf in mouse melanocytes. Pigm Cell Res 20:173–184

    CAS  Google Scholar 

  • Nadeau NJ, Mundy NI, Gourichon D, Minvielle F (2007) Association of a single-nucleotide substitution in TYRP1 with roux in Japanese quail (Coturnix japonica). Anim Genet 38:609–613

    CAS  PubMed  Google Scholar 

  • Nadeau NJ, Minvielle F, Ito S, Inoue-Murayama M, Gourichon D, Follett SA, Burke T, Mundy NI (2008) Characterization of Japanese quail yellow as a genomic deletion upstream of the avian homolog of the mammalian ASIP (agouti) gene. Genetics 178:777–786

    CAS  PubMed  PubMed Central  Google Scholar 

  • Porter C, Clark I, Silber R (1948) The effect of B vitamin deficiencies on tryptophan metabolism in the rat. Arch Biochem 18:339–343

    CAS  PubMed  Google Scholar 

  • Reissmann M, Bierwolf J, Brockmann GA (2007) Two SNPs in the SILV gene are associated with silver coat colour in ponies. Anim Genet 38:1–6

    CAS  PubMed  Google Scholar 

  • Sato S, Otake T, Suzuki C, Saburi J, Kobayashi E (2007) Mapping of the recessive white locus and analysis of the tyrosinase gene in chickens. Poult Sci 86:2126–2133

    CAS  PubMed  Google Scholar 

  • Schmidt-Ullrich R, Paus R (2005) Molecular principles of hair follicle induction and morphogenesis. Bioessays 27:247–261

    CAS  PubMed  Google Scholar 

  • Schmutz SM, Berryere TG, Goldfinch AD (2002) TYRP1 and MC1R genotypes and their effects on coat color in dogs. Mamm Genome 13:380–387

    CAS  PubMed  Google Scholar 

  • Slominski A, Semak I, Pisarchik A, Sweatman T, Szczesniewski A, Wortsman J (2002) Conversion ofL-tryptophan to serotonin and melatonin in human melanoma cells. FEBS Lett 511:102–106

    CAS  PubMed  Google Scholar 

  • Sulem P, Gudbjartsson DF, Stacey SN, Helgason A, Rafnar T, Magnusson KP, Manolescu A, Karason A, Palsson A, Thorleifsson G et al (2007) Genetic determinants of hair, eye and skin pigmentation in Europeans. Nat Genet 39:1443–1452

    CAS  PubMed  Google Scholar 

  • Sylianco CYL, Berg CP (1959) The effect of riboflavin deficiency upon the metabolism of tryptophan by liver and kidney tissue. J Biol Chem 234:912–917

    CAS  PubMed  Google Scholar 

  • Tadano R, Sekino M, Nishibori M, Tsudzuki M (2007) Microsatellite marker analysis for the genetic relationships among Japanese long-tailed chicken breeds. Poult Sci 86:460–469

    CAS  PubMed  Google Scholar 

  • Theos AC, Truschel ST, Raposo G, Marks MS (2005) The Silver locus product Pmel17/gp100/Silv/ME20: controversial in name and in function. Pigment Cell Res 18:322–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tobita-Teramoto T, Jang G, Kino K, Salter D, Brumbaugh J, Akiyama T (2000) Autosomal albino chicken mutation (ca/ca) deletes hexanucleotide (-∆GACTGG817) at a copper-binding site of the tyrosinase gene. Poult Sci 79:46–50

    CAS  PubMed  Google Scholar 

  • Tomihari M, Hwang SH, Chung JS Jr, Ariizumi CP K (2009) Gpnmb is a melanosome-associated glycoprotein that contributes to melanocyte/keratinocyte adhesion in a RGD-dependent fashion. Exp Dermatol 18:586–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winkler PA, Gornik KR, Ramsey DT, Dubielzig RR, Venta PJ, Petersen-Jones SM, Bartoe JT (2014) A partial gene deletion of SLC45A2 causes oculocutaneous albinism in doberman pinscher dogs. PLoS ONE 9:e92127

    PubMed  PubMed Central  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Method Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14

    PubMed  PubMed Central  Google Scholar 

  • Zhang P, Liu W, Zhu C, Yuan X, Li D, Gu W, Ma H, Xie X, Gao T (2012) Silencing of GPNMB by siRNA inhibits the formation of melanosomes in melanocytes in a MITF-independent fashion. PLoS ONE 7:e42955

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Liu F, Cao J, Liu X (2015) Skin Transcriptome Profiles Associated with Skin Color in Chickens. PLoS ONE 10:e0127301

    PubMed  PubMed Central  Google Scholar 

  • Zhao YB, Sun ZZ, Bai JY, Zhang XF, Li AX, Liu JX, Sui LH, Hu ZM, Zeng L (2012) Comparison of Gene Expression Levels of TYR, TYRP1 Gene in Cricetulus barabensis and the Albino mutant. Chin J Comp Med 22:1–4

    Google Scholar 

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Acknowledgements

We thank help from lab members, especially for sample collection. This work was supported by the Earmarked Fund for Hebei Layer Innovation Team of Modern Agro-industry Technology Research System (No: HBCT2013090206), and the Science and Technology Plan Projects of Hebei (group recovery and utilization of Bashang long-tailed chicken, No: 15226302D). RNA sequences were completed by Novogene Bioinformatics Institute.

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Authors and Affiliations

  1. College of Animal Science and Technology, Hebei Normal University of Science and Technology, Qinhuangdao, 066004, Hebei, People’s Republic of China

    Xiaohui Liu, Yongdong Peng, Chuansheng Zhang & Xianglong Li

  2. College of Animal Science and Technology, Hebei Agricultural University, Baoding, 071000, Hebei, People’s Republic of China

    Xiaohui Liu, Rongyan Zhou, Lanhui Li & Xianglong Li

  3. Zhangjiakou Animal Production Technology Promotion Center, Zhangjiakou, 075000, Hebei, People’s Republic of China

    Chunxiang Lu

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  1. Xiaohui Liu
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Correspondence to Xianglong Li.

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Liu, X., Zhou, R., Peng, Y. et al. Hair follicles transcriptome profiles in Bashang long-tailed chickens with different plumage colors. Genes Genom 41, 1357–1367 (2019). https://doi.org/10.1007/s13258-018-0740-y

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