A -Regulatory Mutation of Causes Silky-Feather in Chickens

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The feather is an excellent model for evolution and development due to its complex structure and vast diversity. Some chickens have silky-feather because of a loss of hooklets in pennaceous feathers, while most chickens have the wild-type normal feather. Hooklets are formed in the last differentiation stage of the life cycle of a pennaceous feather. Chickens with silky-feather are homozygous for a recessive allele (hookless, h). Silkie chicken from China is one of the breeds showing the fascinating silky-feather phenotype and the breed has been known for hundreds of years. In this study, we mapped the silky-feather locus to an 18.9 kb interval and identified a single nucleotide polymorphism (SNP) completely associated with silky-feather. The causative mutation is located 103 base pairs upstream of the coding sequence of prenyl (decaprenyl) diphosphate synthase, subunit 2 (PDSS2). The expression of the PDSS2 gene is decreased in silky-feather skin during feather development in vivo. The silky-feather allele also reduces the PDSS2 promoter activity in vitro. This is the first report of feather structure variation associated with PDSS2 and provides new insight into molecular signaling in the late development stage of feather morphogenesis.

Vyšlo v časopise: A -Regulatory Mutation of Causes Silky-Feather in Chickens. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004576
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004576

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Zdroje

1. Lucas AM, Stettenheim PR (1972) Avian anatomy: integument: U.S. Agricultural Research Service (Washington)

2. BartelsT (2003) Variations in the morphology, distribution, and arrangement of feathers in domesticated birds. J Exp Zool B Mol Dev Evol 298: 91–108.

3. MouC, PitelF, GourichonD, VignolesF, TzikaA, et al. (2011) Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering. PLoS Biol 9: e1001028.

4. WangY, GaoY, ImslandF, GuX, FengC, et al. (2012) The crest phenotype in chicken is associated with ectopic expression of HOXC8 in cranial skin. PLoS One 7: e34012.

5. NgCS, WuP, FoleyJ, FoleyA, McDonaldML, et al. (2012) The chicken frizzle feather is due to an alpha-keratin (KRT75) mutation that causes a defective rachis. PLoS Genet 8: e1002748.

6. Haw SG (2006) Marco Polo's China : a Venetian in the realm of Khubilai Khan. London and New York: Routledge. 224 p.

7. Darwin C (1868) The variation of animals and plants under domestication: London: John Murray.

8. DunnLC, JullMA (1927) On the Inheritance of some characters of the Silky fowl. J Genet 19: 27–63.

9. JonesSVH (1921) Inheritance of silkiness in fowls. J Hered 12: 117–128.

10. LandauerW, DunnLC (1930) The “Frizzle” character of fowls - Its expression and inheritance. Journal of Heredity 21: 291–305.

11. ColeLJ, HollanderWF (1939) The inheritance of silky plumage in the domestic pigeon. Journal of Heredity 30: 197–201.

12. MillerWJ (1956) Silky plumage in the ring neck dove. Journal of Heredity 47: 37–40.

13. Ting-BerrethSA, ChuongCM (1996) Sonic Hedgehog in feather morphogenesis: induction of mesenchymal condensation and association with cell death. Dev Dyn 207: 157–170.

14. JungHS, Francis-WestPH, WidelitzRB, JiangTX, Ting-BerrethS, et al. (1998) Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Dev Biol 196: 11–23.

15. JiangTX, JungHS, WidelitzRB, ChuongCM (1999) Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development 126: 4997–5009.

16. HarrisMP, FallonJF, PrumRO (2002) Shh-Bmp2 signaling module and the evolutionary origin and diversification of feathers. J Exp Zool 294: 160–176.

17. HarrisMP, WilliamsonS, FallonJF, MeinhardtH, PrumRO (2005) Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc Natl Acad Sci U S A 102: 11734–11739.

18. YuM, WuP, WidelitzRB, ChuongCM (2002) The morphogenesis of feathers. Nature 420: 308–312.

19. ChuongCM, ChodankarR, WidelitzRB, JiangTX (2000) Evo-devo of feathers and scales: building complex epithelial appendages. Curr Opin Genet Dev 10: 449–456.

20. PrumRO, WilliamsonS (2001) Theory of the growth and evolution of feather shape. J Exp Zool 291: 30–57.

21. GaoY, HuXX, DuZQ, DengXM, HuangYH, et al. (2006) A genome scan for quantitative trait loci associated with body weight at different developmental stages in chickens. Anim Genet 37: 276–278.

22. DorshorstB, OkimotoR, AshwellC (2010) Genomic regions associated with dermal hyperpigmentation, polydactyly and other morphological traits in the Silkie chicken. J Hered 101: 339–350.

23. AnderssonL (2001) Genetic dissection of phenotypic diversity in farm animals. Nat Rev Genet 2: 130–138.

24. DorshorstB, MolinAM, RubinCJ, JohanssonAM, StromstedtL, et al. (2011) A complex genomic rearrangement involving the endothelin 3 locus causes dermal hyperpigmentation in the chicken. PLoS Genet 7: e1002412.

25. TianM, WangY, GuX, FengC, FangS, et al. (2013) Copy number variants in locally raised Chinese chicken genomes determined using array comparative genomic hybridization. BMC Genomics 14: 262.

26. KischerCW (1963) Fine structure of the developing down feather. J Ultrastruct Res 8: 305–321.

27. HeinemeyerT, WingenderE, ReuterI, HermjakobH, KelAE, et al. (1998) Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 26: 362–367.

28. MignoneF, GissiC, LiuniS, PesoleG (2002) Untranslated regions of mRNAs. Genome Biol 3: REVIEWS0004.

29. ChatterjeeS, PalJK (2009) Role of 5′- and 3′-untranslated regions of mRNAs in human diseases. Biol Cell 101: 251–262.

30. LiuW, LiN (2012) Chicken sine oculis binding protein homolog (sobp), a novel gene that may regulate feather development. Poult Sci 91: 1950–1955.

31. WidelitzRB, JiangTX, ChenCW, StottNS, JungHS, et al. (1999) Wnt-7a in feather morphogenesis: involvement of anterior-posterior asymmetry and proximal-distal elongation demonstrated with an in vitro reconstitution model. Development 126: 2577–2587.

32. ChenCW, ChuongCM (1999) Avian integument provides multiple possibilities to analyse different phases of skin appendage morphogenesis. J Investig Dermatol Symp Proc 4: 333–337.

33. HarrapBS, WoodsEF (1964) Soluble derivatives of feather keratin. 1. Isolation, fractionation and amino acid composition. Biochem J 92: 8–18.

34. BrushAH (1972) Correlation of protein electrophoretic pattern with morphology of normal and mutant feathers. Biochem Genet 7: 87–93.

35. AlibardiL (2006) Structural and immunocytochemical characterization of keratinization in vertebrate epidermis and epidermal derivatives. Int Rev Cytol 253: 177–259.

36. AlibardiL (2007) Cell organization of barb ridges in regenerating feathers of the quail: implications of the elongation of barb ridges for the evolution and diversification of feathers. Acta Zool 88: 101–117.

37. AlibardiL, ToniM (2008) Cytochemical and molecular characteristics of the process of cornification during feather morphogenesis. Prog Histochem Cytochem 43: 1–69.

38. AlibardiL (2007) Wedge cells during regeneration of juvenile and adult feathers and their role in carving out the branching pattern of barbs. Ann Anatomy 189: 234–242.

39. GreenwoldMJ, SawyerRH (2013) Molecular evolution and expression of archosaurian beta-keratins: diversification and expansion of archosaurian beta-keratins and the origin of feather beta-keratins. J Exp Zool B Mol Dev Evol 320: 393–405.

40. KowataK, NakaokaM, NishioK, FukaoA, SatohA, et al. (2014) Identification of a feather beta-keratin gene exclusively expressed in pennaceous barbule cells of contour feathers in chicken. Gene 542: 23–28.

41. PrumRO (1999) Development and evolutionary origin of feathers. J Exp Zool 285: 291–306.

42. PrumRO, DyckJ (2003) A hierarchical model of plumage: morphology, development, and evolution. J Exp Zool B Mol Dev Evol 298: 73–90.

43. PrumRO, BrushAH (2002) The evolutionary origin and diversification of feathers. Q Rev Biol 77: 261–295.

44. MadersonPFA, AlibardiL (2000) The development of the sauropsid integument: a contribution to the problem of the origin and evolution of feathers. Amer Zool 40: 513–529.

45. LopezLC, SchuelkeM, QuinziiCM, KankiT, RodenburgRJ, et al. (2006) Leigh syndrome with nephropathy and CoQ10 deficiency due to decaprenyl diphosphate synthase subunit 2 (PDSS2) mutations. Am J Hum Genet 79: 1125–1129.

46. QuinziiCM, LopezLC, Von-MoltkeJ, NainiA, KrishnaS, et al. (2008) Respiratory chain dysfunction and oxidative stress correlate with severity of primary CoQ10 deficiency. FASEB J 22: 1874–1885.

47. PengM, FalkMJ, HaaseVH, KingR, PolyakE, et al. (2008) Primary coenzyme Q deficiency in Pdss2 mutant mice causes isolated renal disease. PLoS Genet 4: e1000061.

48. SaikiR, LuncefordAL, ShiY, MarboisB, KingR, et al. (2008) Coenzyme Q10 supplementation rescues renal disease in Pdss2kd/kd mice with mutations in prenyl diphosphate synthase subunit 2. Am J Physiol Renal Physiol 295: F1535–1544.

49. QuinziiCM, GaroneC, EmmanueleV, TadesseS, KrishnaS, et al. (2013) Tissue-specific oxidative stress and loss of mitochondria in CoQ-deficient Pdss2 mutant mice. FASEB J 27: 612–621.

50. LuS, LuLY, LiuMF, YuanQJ, ShamMH, et al. (2012) Cerebellar defects in Pdss2 conditional knockout mice during embryonic development and in adulthood. Neurobiol Dis 45: 219–233.

51. HamanakaRB, GlasauerA, HooverP, YangS, BlattH, et al. (2013) Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci Signal 6: ra8.

52. GaoY, DuZQ, WeiWH, YuXJ, DengXM, et al. (2009) Mapping quantitative trait loci regulating chicken body composition traits. Anim Genet 40: 952–954.

53. GuX, FengC, MaL, SongC, WangY, et al. (2011) Genome-wide association study of body weight in chicken F2 resource population. PLoS One 6: e21872.

54. GaoY, FengCG, SongC, DuZQ, DengXM, et al. (2011) Mapping quantitative trait loci affecting chicken body size traits via genome scanning. Anim Genet 42: 670–674.

55. DanforthCH, FosterF (1929) Skin transplantation as a means of studying genetic and endocrine factors in the fowl. J Exp Zool 52: 443–470.

56. GreenwoodAW, BlythJSS (1927) Thyroid Gland and Plumage in Chickens. Nature 120: 476–476.

57. ColeRK (1966) Hereditary hypothyroidism in the domestic fowl. Genetics 53: 1021–1033.

58. MartinJH (1929) Effect of excessive dosages of thyroid on the domestic fowl. Biol Bull 56: 357–370.

59. JuhnM (1956) Barbulation induced in silky plumage by thyroxine. Nature 178: 1182.

60. JuhnM, BatesRW (1960) Thyroid function in silky feathering. J Exp Zool 143: 239–243.

61. AlonsoLC, RosenfieldRL (2003) Molecular genetic and endocrine mechanisms of hair growth. Horm Res 60: 1–13.

62. PatiAK, PathakVK (1986) Thyroid and gonadal hormones in feather regeneration of the redheaded bunting, Emberiza bruniceps. J Exp Zool 238: 175–181.

63. PillarTM, SeitzHJ (1997) Thyroid hormone and gene expression in the regulation of mitochondrial respiratory function. Eur J Endocrinol 136: 231–239.

64. XuX, ZhengX, YouH (2010) Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464: 1338–1341.

65. XuX, ZhouZ, WangX, KuangX, ZhangF, et al. (2003) Four-winged dinosaurs from China. Nature 421: 335–340.

66. QiangJ, CurriePJ, NorellMA, Shu-AnJ (1998) Two feathered dinosaurs from northeastern China. Nature 393: 753–761.

67. LiQ, GaoKQ, VintherJ, ShawkeyMD, ClarkeJA, et al. (2010) Plumage color patterns of an extinct dinosaur. Science 327: 1369–1372.

68. KingMC, WilsonAC (1975) Evolution at two levels in humans and chimpanzees. Science 188: 107–116.

69. CarrollSB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25–36.

70. FortiniME, RubinGM (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev 4: 444–463.

71. ErikssonJ, LarsonG, GunnarssonU, Bed'homB, Tixier-BoichardM, et al. (2008) Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet 4: e1000010.

72. WrightD, BoijeH, MeadowsJR, Bed'homB, GourichonD, et al. (2009) Copy number variation in intron 1 of SOX5 causes the Pea-comb phenotype in chickens. PLoS Genet 5: e1000512.

73. GunnarssonU, KerjeS, Bed'homB, SahlqvistAS, EkwallO, et al. (2011) The Dark brown plumage color in chickens is caused by an 8.3-kb deletion upstream of SOX10. Pigment Cell Melanoma Res 24: 268–274.

74. ImslandF, FengC, BoijeH, Bed'homB, FillonV, et al. (2012) The Rose-comb mutation in chickens constitutes a structural rearrangement causing both altered comb morphology and defective sperm motility. PLoS Genet 8: e1002775.

75. WangZ, QuL, YaoJ, YangX, LiG, et al. (2013) An EAV-HP insertion in 5′ Flanking region of SLCO1B3 causes blue eggshell in the chicken. PLoS Genet 9: e1003183.

76. WraggD, MwacharoJM, AlcaldeJA, WangC, HanJL, et al. (2013) Endogenous retrovirus EAV-HP linked to blue egg phenotype in Mapuche fowl. PLoS One 8: e71393.

77. GroenenMA, MegensHJ, ZareY, WarrenWC, HillierLW, et al. (2011) The development and characterization of a 60K SNP chip for chicken. BMC Genomics 12: 274.

78. Green P, Falls K, Crooks S (1990) Documentation for CRI-MAP, version 2.4: Washington University School of Medicine, St. Louis.

79. LiuW, LiuZ, HuX, ZhangY, YuanJ, et al. (2003) Construction and characterization of a novel 13.34-fold chicken bacterial artificial chromosome library. Anim Biotechnol 14: 145–153.

80. LiB, KrishnanVG, MortME, XinF, KamatiKK, et al. (2009) Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 25: 2744–2750.