The Chicken Frizzle Feather Is Due to an α-Keratin () Mutation That Causes a Defective Rachis

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Feathers have complex forms and are an excellent model to study the development and evolution of morphologies. Existing chicken feather mutants are especially useful for identifying genetic determinants of feather formation. This study focused on the gene F, underlying the frizzle feather trait that has a characteristic curled feather rachis and barbs in domestic chickens. Our developmental biology studies identified defects in feather medulla formation, and physical studies revealed that the frizzle feather curls in a stepwise manner. The frizzle gene is transmitted in an autosomal incomplete dominant mode. A whole-genome linkage scan of five pedigrees with 2678 SNPs revealed association of the frizzle locus with a keratin gene-enriched region within the linkage group E22C19W28_E50C23. Sequence analyses of the keratin gene cluster identified a 69 bp in-frame deletion in a conserved region of KRT75, an α-keratin gene. Retroviral-mediated expression of the mutated F cDNA in the wild-type rectrix qualitatively changed the bending of the rachis with some features of frizzle feathers including irregular kinks, severe bending near their distal ends, and substantially higher variations among samples in comparison to normal feathers. These results confirmed KRT75 as the F gene. This study demonstrates the potential of our approach for identifying genetic determinants of feather forms.

Vyšlo v časopise: The Chicken Frizzle Feather Is Due to an α-Keratin () Mutation That Causes a Defective Rachis. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002748
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002748

Souhrn

Zdroje

1. DarwinC 1868 The Variation of Plants and Animals under Domestication London, UK John Murray

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. WidelitzRBVeltmaatJMMayerJAFoleyJChuongCM 2007 Mammary glands and feathers: comparing two skin appendages which help define novel classes during vertebrate evolution. Semin Cell Dev Biol 18 255 266

4. LinCMJiangTXWidelitzRBChuongCM 2006 Molecular signaling in feather morphogenesis. Curr Opin Cell Biol 18 730 741

5. WuPHouLPlikusMHughesMScehnetJ 2004 Evo-Devo of amniote integuments and appendages. Int J Dev Biol 48 249 270

6. YuMYueZWuPWuDYMayerJA 2004 The developmental biology of feather follicles. Int J Dev Biol 48 181 191

7. WidelitzRBJiangTXYuMShenTShenJY 2003 Molecular biology of feather morphogenesis: a testable model for evo-devo research. J Exp Zool B Mol Dev Evol 298 109 122

8. ChuongCMHombergerDG 2003 Development and evolution of the amniote integument: current landscape and future horizon. J Exp Zool B Mol Dev Evol 298 1 11

9. YuMWuPWidelitzRBChuongCM 2002 The morphogenesis of feathers. Nature 420 308 312

10. ChuongCMChodankarRWidelitzRBJiangTX 2000 Evo-devo of feathers and scales: building complex epithelial appendages. Curr Opin Genet Dev 10 449 456

11. PrumRO 2005 Evolution of the morphological innovations of feathers. J Exp Zool B Mol Dev Evol 304 570 579

12. PrumRODyckJ 2003 A hierarchical model of plumage: morphology, development, and evolution. J Exp Zool B Mol Dev Evol 298 73 90

13. PrumROBrushAH 2002 The evolutionary origin and diversification of feathers. Q Rev Biol 77 261 295

14. PrumROWilliamsonS 2001 Theory of the growth and evolution of feather shape. J Exp Zool 291 30 57

15. PrumRO 1999 Development and evolutionary origin of feathers. J Exp Zool 285 291 306

16. SawyerRHRogersLWashingtonLGlennTCKnappLW 2005 Evolutionary origin of the feather epidermis. Dev Dyn 232 256 267

17. SawyerRHKnappLW 2003 Avian skin development and the evolutionary origin of feathers. J Exp Zool B Mol Dev Evol 298 57 72

18. SomesRG 1990 Mutations and major variants of plumage and skin in chickens. CrawfordRD Poultry Breeding and Genetics Amsterdam, Netherlands Elsevier 169 208

19. LucasAMStettenheimPR 1972 Avian Anatomy - Integument, Parts I and II Washington, D. C. United States Agricultural Research Service

20. AertsJCrooijmansRCornelissenSHemmatianKVeenendaalT 2003 Integration of chicken genomic resources to enable whole-genome sequencing. Cytogenet Genome Res 102 297 303

21. AntinPB 2004 Chicken genomic and gene expression resources. FASEB J 18 A762 A762

22. AntinPBKonieczkaJH 2005 Genomic resources for chicken. Dev Dyn 232 877 882

23. BurtDPourquieO 2003 Genetics. Chicken genome–science nuggets to come soon. Science 300 1669

24. BurtDW 2002 Comparative mapping in farm animals. Brief Funct Genomic Proteomic 1 159 168

25. BurtDW 2004 Chicken genomics charts a path to the genome sequence. Brief Funct Genomic Proteomic 3 60 67

26. BurtDW 2004 The chicken genome and the developmental biologist. Mech Dev 121 1129 1135

27. BurtDW 2007 Emergence of the chicken as a model organism: Implications for agriculture and biology. Poult Sci 86 1460 1471

28. BurtDWWhiteSJ 2007 Avian genomics in the 21st century. Cytogenet Genome Res 117 6 13

29. CogburnLAPorterTEDuclosMJSimonJBurgessSC 2007 Functional genomics of the chicken - A model organism. Poult Sci 86 2059 2094

30. de KoningDJCabreraCPHaleyCS 2007 Genetical genomics: Combining gene expression with marker genotypes in poultry. Poultry Sci 86 1501 1509

31. DelanyME 2004 Genetic variants for chick biology research: from breeds to mutants. Mech Dev 121 1169 1177

32. DequeantMLPourquieO 2005 Chicken genome: new tools and concepts. Dev Dyn 232 883 886

33. DodgsonJB 2003 Chicken genome sequence: a centennial gift to poultry genetics. Cytogenet Genome Res 102 291 296

34. EdwardsSVBryan JenningsWShedlockAM 2005 Phylogenetics of modern birds in the era of genomics. Proc Biol Sci 272 979 992

35. BurtDW 2005 Chicken genome: current status and future opportunities. Genome Res 15 1692 1698

36. EllegrenH 2005 The avian genome uncovered. Trends Ecol Evol 20 180 186

37. EllegrenH 2007 Molecular evolutionary genomics of birds. Cytogenet Genome Res 117 120 130

38. AndersonKVInghamPW 2003 The transformation of the model organism: a decade of developmental genetics. Nat Genet 33 Suppl 285 293

39. AnderssonL 2001 Genetic dissection of phenotypic diversity in farm animals. Nat Rev Genet 2 130 138

40. AnderssonLGeorgesM 2004 Domestic-animal genomics: deciphering the genetics of complex traits. Nat Rev Genet 5 202 212

41. WrightDBoijeHMeadowsJRBed'homBGourichonD 2009 Copy number variation in intron 1 of SOX5 causes the Pea-comb phenotype in chickens. PLoS Genet 5 e1000512 doi:10.1371/journal.pgen.1000512

42. WrightDKerjeSBrandstromHSchutzKKindmarkA 2008 The genetic architecture of a female sexual ornament. Evolution 62 86 98

43. SomesRG 1990 Mutations and major variants of muscles and skeleton in Guinea Fowl. CrawfordRD Poultry Breeding and Genetics Amsterdam, Netherlands Elsevier 363 370

44. LandauerWDunnLC 1930 The “Frizzle” character of fowls - Its expression and inheritance. J Hered 21 291 305

45. HuttFB 1930 The genetics of the fowl I The inheritance of frizzled plumage. J Genet 22 109 127

46. WinterHRogersMALangbeinLStevensHPLeighIM 1997 Mutations in the hair cortex keratin hHb6 cause the inherited hair disease monilethrix. Nat Genet 16 372 374

47. ChapalainVWinterHLangbeinLLe RoyJMLabrezeC 2002 Is the loose anagen hair syndrome a keratin disorder? A clinical and molecular study. Arch Dermatol 138 501 506

48. ChenJJaegerKDenZKochPJSundbergJP 2008 Mice expressing a mutant Krt75 (K6hf) allele develop hair and nail defects resembling pachyonychia congenita. J Invest Dermatol 128 270 279

49. Ting-BerrethSAChuongCM 1996 Sonic Hedgehog in feather morphogenesis: induction of mesenchymal condensation and association with cell death. Dev Dyn 207 157 170

50. MadersonPFHilleniusWJHillerUDoveCC 2009 Towards a comprehensive model of feather regeneration. J Morphol 270 1166 1208

51. AlibardiLToniM 2008 Cytochemical and molecular characteristics of the process of cornification during feather morphogenesis. Prog Histochem Cytochem 43 1 69

52. KrimmS 1960 Structure of Frizzle Mutant Feather Keratin. J Mol Biol 2 247 &

53. BrushAH 1972 Correlation of protein electrophoretic pattern with morphology of normal and mutant feathers. Biochem Genet 7 87 93

54. SzeverenyiICassidyAJChungCWLeeBTCommonJE 2008 The Human Intermediate Filament Database: comprehensive information on a gene family involved in many human diseases. Hum Mutat 29 351 360

55. ParryDASteinertPM 1999 Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism. Q Rev Biophys 32 99 187

56. WangZWongPLangbeinLSchweizerJCoulombePA 2003 Type II epithelial keratin 6hf (K6hf) is expressed in the companion layer, matrix, and medulla in anagen-stage hair follicles. J Invest Dermatol 121 1276 1282

57. MouCPitelFGourichonDVignolesFTzikaA 2011 Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering. PLoS Biol 9 e1001028 doi:10.1371/journal.pbio.1001028

58. SchweizerJBowdenPECoulombePALangbeinLLaneEB 2006 New consensus nomenclature for mammalian keratins. J Cell Biol 174 169 174

59. MollRDivoMLangbeinL 2008 The human keratins: biology and pathology. Histochem Cell Biol 129 705 733

60. McLeanWHMooreCB 2011 Keratin disorders: from gene to therapy. Hum Mol Genet 20 R189 197

61. FuchsETynerALGiudiceGJMarchukDRaychaudhuryA 1987 The Human Keratin Genes and Their Differential Expression. Curr Top Dev Biol 22 5 34

62. FuchsEClevelandDW 1998 A structural scaffolding of intermediate filaments in health and disease. Science 279 514 519

63. DhouaillyDRogersGESengelP 1978 The specification of feather and scale protein synthesis in epidermal-dermal recombinations. Dev Biol 65 58 68

64. HaakeARKonigGSawyerRH 1984 Avian feather development: relationships between morphogenesis and keratinization. Dev Biol 106 406 413

65. BellEThathachariYT 1963 Development of feather keratin during embryogenesis of the chick. J Cell Biol 16 215 223

66. ChangCHYuMWuPJiangTXYuHS 2004 Sculpting skin appendages out of epidermal layers via temporally and spatially regulated apoptotic events. J Invest Dermatol 122 1348 1355

67. TongXCoulombePA 2006 Keratin 17 modulates hair follicle cycling in a TNFalpha-dependent fashion. Genes Dev 20 1353 1364

68. LandauerWAberleSD 1935 Studies on the endocrine glands of Frizzle fowl. Am J Anat 57 99 134

69. BenedictFGLandauerWFoxEL 1932 The physiology of normal and frizzle fowl, with special reference to the basal metabolism. Storrs Agric Exp Sta Bull 177 1 118

70. BoasEPLandauerW 1933 The effect of elevated metabolism on the hearts of frizzle fowl. Am J Med Sci 185 654 664

71. LandauerWUphamE 1936 Weight and size in frizzle fowl. Storrs Agric Exp Sta Bull 210

72. LandauerW 1933 A gene modifying frizzling in the fowl. J Hered 24 153 156

73. HuttFB 1936 Genetics of the fowl V The modified frizzle. J Genet 32 277 285

74. SperlingLCHusseySSorrellsTWangJADarlingT 2010 Cytokeratin 75 expression in central, centrifugal, cicatricial alopecia - new observations in normal and diseased hair follicles. J Cutan Pathol 37 243 248

75. WinterHLangbeinLPraetzelSJacobsMRogersMA 1998 A novel human type II cytokeratin, K6hf, specifically expressed in the companion layer of the hair follicle. J Invest Dermatol 111 955 962

76. LangbeinLSpringHRogersMAPraetzelSSchweizerJ 2004 Hair keratins and hair follicle-specific epithelial keratins. Methods Cell Biol 78 413 451

77. CoulombePAWangZLWongPLangbeinLSchweizerJ 2003 Type II epithelial keratin 6hf (K6hf) is expressed in the companion layer, matrix, and medulla in anagen-stage hair follicles. J Invest Dermatol 121 1276 1282

78. GuLHCoulombePA 2007 Keratin expression provides novel insight into the morphogenesis and function of the companion layer in hair follicles. J Invest Dermatol 127 1061 1073

79. WinterHSchisselDParryDASmithTALiovicM 2004 An unusual Ala12Thr polymorphism in the 1A alpha-helical segment of the companion layer-specific keratin K6hf: evidence for a risk factor in the etiology of the common hair disorder pseudofolliculitis barbae. J Invest Dermatol 122 652 657

80. SchweizerJLangbeinLRogersMAWinterH 2007 Hair follicle-specific keratins and their diseases. Exp Cell Res 313 2010 2020

81. ShimomuraYWajidMPetukhovaLKurbanMChristianoAM 2010 Autosomal-dominant woolly hair resulting from disruption of keratin 74 (KRT74), a potential determinant of human hair texture. Am J Hum Genet 86 632 638

82. WasifNNaqviSKBasitSAliNAnsarM 2011 Novel mutations in the keratin-74 (KRT74) gene underlie autosomal dominant woolly hair/hypotrichosis in Pakistani families. Hum Genet 129 419 424

83. RogersMAEdlerLWinterHLangbeinLBeckmannI 2005 Characterization of new members of the human type II keratin gene family and a general evaluation of the keratin gene domain on chromosome 12q13.13. J Invest Dermatol 124 536 544

84. RogersMAWinterHLangbeinLBleilerRSchweizerJ 2004 The human type I keratin gene family: characterization of new hair follicle specific members and evaluation of the chromosome 17q21.2 gene domain. Differentiation 72 527 540

85. HesseMZimekAWeberKMaginTM 2004 Comprehensive analysis of keratin gene clusters in humans and rodents. Eur J Cell Biol 83 19 26

86. SmithF 2003 The molecular genetics of keratin disorders. Am J Clin Dermatol 4 347 364

87. VandeberghWBossuytF 2012 Radiation and Functional Diversification of Alpha Keratins during Early Vertebrate Evolution. Mol Biol Evol 29 995 1004

88. PadgettRAGrabowskiPJKonarskaMMSeilerSSharpPA 1986 Splicing of messenger RNA precursors. Annu Rev Biochem 55 1119 1150

89. GreenMR 1986 Pre-mRNA splicing. Annu Rev Genet 20 671 708

90. KrainerARRocaXSachidanandamR 2003 Intrinsic differences between authentic and cryptic 5 ′ splice sites. Nucleic Acids Res 31 6321 6333

91. KrainerARHastingsMLRestaNTraumDStellaA 2005 An LKB1 AT-AC intron mutation causes Peutz-Jeghers syndrome via splicing at noncanonical cryptic splice sites. Nat Struct Mol Biol 12 54 59

92. Lopez-BigasNAuditBOuzounisCParraGGuigoR 2005 Are splicing mutations the most frequent cause of hereditary disease? FEBS Lett 579 1900 1903

93. BurattiEChiversMKralovicovaJRomanoMBaralleM 2007 Aberrant 5′ splice sites in human disease genes: mutation pattern, nucleotide structure and comparison of computational tools that predict their utilization. Nucleic Acids Res 35 4250 4263

94. WangGSCooperTA 2007 Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 8 749 761

95. JiangT-XStottSWidelitzRBChuongC-M 1998 Current methods in the study of avian skin appendages. ChuongC-M Molecular Basis of Epithelial Appendage Morphogenesis Austin, TX Landes Bioscience 395 408

96. ChuongCMWidelitzRBTing-BerrethSJiangTX 1996 Early events during avian skin appendage regeneration: dependence on epithelial-mesenchymal interaction and order of molecular reappearance. J Invest Dermatol 107 639 646

97. PreslandRBWhitbreadLARogersGE 1989 Avian keratin genes. II. Chromosomal arrangement and close linkage of three gene families. J Mol Biol 209 561 576

98. LoftusSKLarsonDMWatkins-ChowDChurchDMPavanWJ 2001 Generation of RCAS vectors useful for functional genomic analyses. DNA Res 8 221 226