A Genomic Duplication is Associated with Ectopic Eomesodermin Expression in the Embryonic Chicken Comb and Two Duplex-comb Phenotypes

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There are three major variant comb types found in the domestic chicken; Rose-comb, Pea-comb and Duplex-comb. Within the Duplex-comb there are two distinct types, V-shaped and Buttercup. Previous experiments have shown that these two Duplex-comb types represent different alleles at a single locus. We have mapped the location of the Duplex-comb locus and identified a 20 Kb duplication that is present only in chickens that have a Duplex-comb phenotype. The 20 Kb duplication is located 200 Kb upstream of EOMES, a gene that was found to be abnormally expressed in the comb-developing region of V-shaped and Buttercup comb chicken embryos. This suggests that the 20 Kb duplication contains regulatory elements affecting EOMES expression. These findings complete our characterization of the genetic basis of the three major comb loci in the chicken, all of which are caused by large-scale structural genomic variants that drive ectopic expression of transcription factors in the comb region during chicken embryo development.

Vyšlo v časopise: A Genomic Duplication is Associated with Ectopic Eomesodermin Expression in the Embryonic Chicken Comb and Two Duplex-comb Phenotypes. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1004947
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004947

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1. Johnsson M, Gustafson I, Rubin C-J, Sahlqvist A-S, Jonsson KB, et al. (2012) A sexual ornament in chickens is affected by pleiotropic alleles at HAO1 and BMP2, selected during domestication. PLoS Genet 8: e1002914. doi: 10.1371/journal.pgen.1002914 22956912

2. Schantz Von T, Tufvesson M, Göransson G (1995) Artificial selection for increased comb size and its effects on other sexual characters and viability in Gallus domesticus (the domestic chicken). Heredity 75 : 518–529. doi: 10.1038/hdy.1995.168

3. Boije H, Harun-Or-Rashid M, Lee Y-J, Imsland F, Bruneau N, et al. (2012) Sonic Hedgehog-signalling patterns the developing chicken comb as revealed by exploration of the pea-comb mutation. PLoS ONE 7: e50890. doi: 10.1371/journal.pone.0050890 23227218

4. Imsland F, Feng C, Boije H, Bed'hom B, Fillon V, 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. doi: 10.1371/journal.pgen.1002775 22761584

5. Wright D, Boije H, Meadows JRS, Bed'hom B, Gourichon D, et al. (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 19521496

6. Somes RG (1991) Some observations on high cavernous nostrils in the chicken. J Hered 82 : 172–174. 2013692

7. Aldrovandi U (1600) Ornithologiae tomus alter cum indice copiosissimo. Bologna.

8. Somes RG (1991) Duplex comb in the chicken: a multi-allelic trait. J Hered 82 : 169–172. 2013691

9. Showell C, Binder O, Conlon FL (2004) T-box genes in early embryogenesis. Dev Dyn 229 : 201–218. doi: 10.1002/dvdy.10480 14699590

10. Dorshorst B, Okimoto R, Ashwell C (2010) Genomic regions associated with dermal hyperpigmentation, polydactyly and other morphological traits in the Silkie chicken. J. Hered 101 : 339–350. doi: 10.1093/jhered/esp120 20064842

11. Groenen MAM, Megens H-J, Zare Y, Warren WC, Hillier LW, et al. (2011) The development and characterization of a 60K SNP chip for chicken. BMC Genomics 12 : 274. doi: 10.1186/1471-2164-12-274 21627800

12. Wragg D, Mwacharo JM, Alcalde JA, Hocking PM, Hanotte O (2012) Analysis of genome-wide structure, diversity and fine mapping of Mendelian traits in traditional and village chickens. Heredity 109 : 6–18. doi: 10.1038/hdy.2012.9 22395157

13. Rubin C-J, Zody MC, Eriksson J, Meadows JRS, Sherwood E, et al. (2010) Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464 : 587–591. doi: 10.1038/nature08832 20220755

14. Wong GK-S, Liu B, Wang J, Zhang Y, Yang X, et al. (2004) A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 432 : 717–722. doi: 10.1038/nature03156 15592405

15. Cooper GM (2005) Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15 : 901–913. doi: 10.1101/gr.3577405 15965027

16. Hutt FB, Mueller CD (1943) The linkage of polydactyly with multiple spurs and duplex comb in the fowl. Am Nat.77 : 70–78. doi: 10.2307/2457381

17. Pitel F, Bergé R, Coquerelle G, Crooijmans R, Groenen MA, et al. (2000) Mapping the naked neck (NA) and polydactyly (PO) mutants of the chicken with microsatellite molecular markers. Genet Sel Evol 32 : 73–86. doi: 10.1051/gse:2000107 14736408

18. Dunn IC, Paton IR, Clelland AK, Sebastian S, Johnson EJ, et al. (2011) The chicken polydactyly (Po) locus causes allelic imbalance and ectopic expression of Shh during limb development. Dev Dyn 240 : 1163–1172. doi: 10.1002/dvdy.22623 21465618

19. Maas SA, Fallon J (2005) Single base pair change in the long-range Sonic hedgehog limb-specific enhancer is a genetic basis for preaxial polydactyly. Dev Dyn 232 : 345–348. doi: 10.1002/dvdy.20254 15637698

20. Bateson W, Punnett R (1908) Experimental studies in the physiology of heredity. Repts Evol Comm Roy Soc 4 : 18–35.

21. Pernaute B, Cañon S, Crespo M, Fernandez-Tresguerres B, Rayon T, et al. (2010) Comparison of extraembryonic expression of Eomes and Cdx2 in pregastrulation chick and mouse embryo unveils regulatory changes along evolution. Dev Dyn 239 : 620–629. doi: 10.1002/dvdy.22176 20014105

22. Marcucio RS, Cordero DR, Hu D, Helms JA (2005) Molecular interactions coordinating the development of the forebrain and face. Dev Biol 284 : 48–61. doi: 10.1016/j.ydbio.2005.04.030 15979605

23. Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10 : 551–564. doi: 10.1038/nrg2593 19597530

24. Andersson L (2013) Molecular consequences of animal breeding. Curr Opin Genet Dev 23 : 295–301. doi: 10.1016/j.gde.2013.02.014 23601626

25. Dorshorst B, Molin A-M, Rubin C-J, Johansson AM, Strömstedt L, et al. (2011) A complex genomic rearrangement involving the endothelin 3 locus causes dermal hyperpigmentation in the chicken. PLoS Genet 7: e1002412. doi: 10.1371/journal.pgen.1002412 22216010

26. Gunnarsson U, Kerje S, Bed'hom B, Sahlqvist A-S, Ekwall O, 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. doi: 10.1111/j.1755-148X.2011.00825.x 21210960

27. Rubin C-J, Megens H-J, Martinez Barrio A, Maqbool K, Sayyab S, et al. (2012) Strong signatures of selection in the domestic pig genome. Proc Natl Acad Sci 109 : 19529–19536. doi: 10.1073/pnas.1217149109 23151514

28. Sundström E, Komisarczuk AZ, Jiang L, Golovko A, Navratilova P, et al. (2011) Identification of a melanocyte-specific, microphthalmia-associated transcription factor-dependent regulatory element in the intronic duplication causing hair greying and melanoma in horses. Pigment Cell Melanoma Res 25 : 28–36. doi: 10.1111/j.1755-148X.2011.00902.x 21883983

29. Durkin K, Coppieters W, Drögemüller C, Ahariz N, Cambisano N, et al. (2012) Serial translocation by means of circular intermediates underlies colour sidedness in cattle. Nature 482 : 81–84. doi: 10.1038/nature10757 22297974

30. Allais-Bonnet A, Grohs C, Medugorac I, Krebs S, Djari A, et al. (2013) Novel insights into the bovine polled phenotype and horn ontogenesis in Bovidae. PLoS ONE 8:e63512. doi: 10.1371/journal.pone.0063512.s007 23717440

31. Medugorac I, Seichter D, Graf A, Russ I, Blum H, et al. (2012) Bovine polledness—an autosomal dominant trait with allelic heterogeneity. PLoS ONE 7:e39477. doi: 10.1371/journal.pone.0039477 22737241

32. Rothammer S, Capitan A, Mullaart E, Seichter D, Russ I, et al. (2014) The 80-kb DNA duplication on BTA1 is the only remaining candidate mutation for the polled phenotype of Friesian origin. Genet Sel Evol 46 : 44. doi: 10.1186/1297-9686-46-44 24993890

33. Kijas JM, Moller M, Plastow GS, Andersson L (2001) A frameshift mutation in MC1R and a high frequency of somatic reversions cause black spotting in pigs. Genetics 158 : 779–785. 11404341

34. Livak K (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25 : 402–408. doi: 10.1006/meth.2001.1262 11846609

35. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 : 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

36. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43 : 491–498. doi: 10.1038/ng.806 21478889

37. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034. doi: 10.1186/gb-2002-3-7-research0034

38. Hillel J, Groenen MAM, Tixier-Boichard M, Korol AB, David L, et al. (2003) Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet Sel Evol 35 : 533–557. doi: 10.1051/gse:2003038 12939204