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Genes & Genomics

, Volume 41, Issue 11, pp 1357–1367 | Cite as

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

  • Xiaohui Liu
  • Rongyan Zhou
  • Yongdong Peng
  • Chuansheng Zhang
  • Lanhui Li
  • Chunxiang Lu
  • Xianglong LiEmail author
Research Article

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.

Keywords

Hair follicle Plumage color Gene expression RNA-Seq 

Notes

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.

References

  1. Bennett DC, Lamoreux ML (2003) The color loci of mice–a genetic century. Pigm Cell Res 16:333–344Google Scholar
  2. 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 34:169–175PubMedGoogle Scholar
  3. Botchkarev VA, Kishimoto J (2003) Molecular control of epithelial–mesenchymal interactions during hair follicle cycling. J Investig Dermatol Symp Proc 8:46–55PubMedGoogle Scholar
  4. 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 7:46PubMedPubMedCentralGoogle Scholar
  5. 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–E3PubMedPubMedCentralGoogle Scholar
  6. 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 7:19PubMedPubMedCentralGoogle Scholar
  7. 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 7:19–19PubMedPubMedCentralGoogle Scholar
  8. Charconnet-Harding F, Dalgliesh C, Neuberger A (1953) The relation between riboflavin and tryptophan metabolism, studied in the rat. Biochem J 53:513PubMedPubMedCentralGoogle Scholar
  9. Cieslak M, Reissmann M, Hofreiter M, Ludwig A (2011) Colours of domestication. Biol Rev Camb Philos Soc 86:885–899PubMedGoogle Scholar
  10. 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 103:1376–1381PubMedGoogle Scholar
  11. 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 391:249–259PubMedPubMedCentralGoogle Scholar
  12. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868PubMedGoogle Scholar
  13. 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 37:166–170PubMedGoogle Scholar
  14. 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 10:47PubMedPubMedCentralGoogle Scholar
  15. 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 11:59PubMedPubMedCentralGoogle Scholar
  16. Fuchs E (2007) Scratching the surface of skin development. Nature 445:834–842PubMedPubMedCentralGoogle Scholar
  17. 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 39:895–899Google Scholar
  18. 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 8:56PubMedPubMedCentralGoogle Scholar
  19. Guyonneau L, Murisier F, Rossier A, Moulin A, Beermann F (2004) Melanocytes and pigmentation are affected in dopachrome tautomerase knockout mice. Mol Cell Biol 24:3396–3403PubMedPubMedCentralGoogle Scholar
  20. Henderson LM, Weinstock I, Ramasarma G (1951) Effect of deficiency of B vitamins on the metabolism of tryptophan by the rat. J Biol Chem 189:19–29PubMedGoogle Scholar
  21. 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–D484PubMedGoogle Scholar
  22. 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 168:1507–1518PubMedPubMedCentralGoogle Scholar
  23. 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 13:5818PubMedPubMedCentralGoogle Scholar
  24. Kobayashi T, Imokawa G, Bennett DC, Hearing VJ (1998) Tyrosinase stabilization by Tyrp1 (the brown locus protein). J Biol Chem 273:31801–31805PubMedGoogle Scholar
  25. 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 38:109–113PubMedGoogle Scholar
  26. 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:e36592PubMedPubMedCentralGoogle Scholar
  27. 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 25:402–408Google Scholar
  28. 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 324:485–485PubMedPubMedCentralGoogle Scholar
  29. 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 89:6968–6972PubMedGoogle Scholar
  30. Lyons LA, Foe IT, Rah HC, Grahn RA (2005) Chocolate coated cats: TYRP1 mutations for brown color in domestic cats. Mamm Genome 16:356–366PubMedGoogle Scholar
  31. Millar SE (2002) Molecular mechanisms regulating hair follicle development. J Invest Dermatol 118:216–225PubMedGoogle Scholar
  32. 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 38:103–108PubMedGoogle Scholar
  33. Mockus SM, Vrana KE (1998) Advances in the molecular characterization of tryptophan hydroxylase. J Mol Neurosci 10:163–179PubMedGoogle Scholar
  34. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Methods 5:621–628Google Scholar
  35. Murisier F, Guichard S, Beermann F (2007) The tyrosinase enhancer is activated by Sox10 and Mitf in mouse melanocytes. Pigm Cell Res 20:173–184Google Scholar
  36. 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 38:609–613PubMedGoogle Scholar
  37. 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 178:777–786PubMedPubMedCentralGoogle Scholar
  38. Porter C, Clark I, Silber R (1948) The effect of B vitamin deficiencies on tryptophan metabolism in the rat. Arch Biochem 18:339–343PubMedGoogle Scholar
  39. Reissmann M, Bierwolf J, Brockmann GA (2007) Two SNPs in the SILV gene are associated with silver coat colour in ponies. Anim Genet 38:1–6PubMedGoogle Scholar
  40. 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 86:2126–2133PubMedGoogle Scholar
  41. Schmidt-Ullrich R, Paus R (2005) Molecular principles of hair follicle induction and morphogenesis. Bioessays 27:247–261PubMedGoogle Scholar
  42. Schmutz SM, Berryere TG, Goldfinch AD (2002) TYRP1 and MC1R genotypes and their effects on coat color in dogs. Mamm Genome 13:380–387PubMedGoogle Scholar
  43. 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 511:102–106PubMedGoogle Scholar
  44. 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 39:1443–1452PubMedGoogle Scholar
  45. Sylianco CYL, Berg CP (1959) The effect of riboflavin deficiency upon the metabolism of tryptophan by liver and kidney tissue. J Biol Chem 234:912–917PubMedGoogle Scholar
  46. Tadano R, Sekino M, Nishibori M, Tsudzuki M (2007) Microsatellite marker analysis for the genetic relationships among Japanese long-tailed chicken breeds. Poult Sci 86:460–469PubMedGoogle Scholar
  47. 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 18:322–336PubMedPubMedCentralGoogle Scholar
  48. 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 79:46–50PubMedGoogle Scholar
  49. 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 18:586–595PubMedPubMedCentralGoogle Scholar
  50. 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:e92127PubMedPubMedCentralGoogle Scholar
  51. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Method Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14PubMedPubMedCentralGoogle Scholar
  52. 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:e42955PubMedPubMedCentralGoogle Scholar
  53. Zhang J, Liu F, Cao J, Liu X (2015) Skin Transcriptome Profiles Associated with Skin Color in Chickens. PLoS ONE 10:e0127301PubMedPubMedCentralGoogle Scholar
  54. 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 22:1–4Google Scholar

Copyright information

© The Genetics Society of Korea and Springer Nature B.V. 2018

Authors and Affiliations

  • Xiaohui Liu
    • 1
    • 2
  • Rongyan Zhou
    • 2
  • Yongdong Peng
    • 1
  • Chuansheng Zhang
    • 1
  • Lanhui Li
    • 2
  • Chunxiang Lu
    • 3
  • Xianglong Li
    • 1
    • 2
    Email author
  1. 1.College of Animal Science and TechnologyHebei Normal University of Science and TechnologyQinhuangdaoPeople’s Republic of China
  2. 2.College of Animal Science and TechnologyHebei Agricultural UniversityBaodingPeople’s Republic of China
  3. 3.Zhangjiakou Animal Production Technology Promotion CenterZhangjiakouPeople’s Republic of China

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