Inverted duplication including Endothelin 3 closely related to dermal hyperpigmentation in Silkie chickens

Abstract

The dermal hyperpigmentation phenotype in chickens is controlled by the dominant fibromelanosis allele. One of the ten unique characteristics of Silkie chickens is the fibromelanosis phenotype, which is pigmentation in the dermal layer of the skin and connective tissue. In this study, we found a mutation of fibromelanosis, a genomic rearrangement that included an inverted duplication of endothelin3 (EDN3), is responsible. We show that, as a stimulator of melanoblast proliferation, EDN3 expression was increased in silkie embryos and in both skin and muscle throughout adulthood. EDN3 expression led to an increase in expression of the downstream genes EDNRB2 and TYRP2, and was closely relate with the hyperpigmentation phenotype. We examined eight different Chinese chicken breeds showing hyperpigmentation and conclude that this structural genetic variant exists in all fibromelanosis chicken breeds.

Keywords

dermal hyperpigmentation / duplication / endothelin 3 / Silkie chicken

References

[1] Dorshorst B, Okimoto R, Ashwell C. Genomic regions associated with dermal hyperpigmentation, polydactyly and other morphological traits in the Silkie chicken. Journal of Heredity, 2010, 101(3): 339–350

[2] Smyth J R Jr. Genetics of plumage, skin and eye pigmentation in chickens. Crawford RD, ed. Amsterdam. New York, 1990

[3] Hutt F B. Genetics of the fowl. McGraw-Hill. New York, 1949

[4] Kuklenski J. Über das vorkommen und die verteilung des pigmentes in den organen und geweben bei japanischen seidenhühnern. (Over occurrence and the distribution of the pigment in the organs and tissues of Japanese Silky chickens). Archiv für mikroskopische Anatomie, 1915, 87(1): 1–37 (in German)

[5] Le D M N. The Neural Crest. Cambridge Univ. Cambridge, 1982

[6] Erickson C A, Reedy M V. Neural crest development: the interplay between morphogenesis and cell differentiation. Current Topics in Developmental Biology, 1998, 40: 177–209

[7] Erickson C A, Goins T L. Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes. Development, 1995, 121(3): 915–924

[8] Reedy M V, Faraco C D, Erickson C A. Specification and migration of melanoblasts at the vagal level and in hyperpigmented Silkie chickens. Developmental Dynamics, 1998, 213(4): 476–485

[9] Faraco C D, Vaz S A, Pástor M V, Erickson C A. Hyperpigmentation in the Silkie fowl correlates with abnormal migration of fate-restricted melanoblasts and loss of environmental barrier molecules. Developmental Dynamics, 2001, 220(3): 212–225

[10] Lecoin L, Mercier P, Le Douarin N M. Growth of neural crest cells in vitro is enhanced by extracts from Silky Fowl embryonic tissues. Pigment Cell Research, 1994, 7(4): 210–216

[11] Hallet M M, Ferrand R. Quail melanoblast migration in two breeds of fowl and in their hybrids: evidence for a dominant genic control of the mesodermal pigment cell pattern through the tissue environment. Journal of Experimental Zoology, 1984, 230(2): 229–238

[12] Bateson W, Punnett R. The inheritance of the peculiar pigmentation of the silky fowl. Journal of Genetics, 1911, 1(3): 185–203

[13] Dunn L, Jull M. On the inheritance of some characters op the silky fowl. Journal of Genetics, 1927, 19(1): 27–63

[14] Bitgood J J. Linear relationship of the loci for barring, dermal melanin inhibitor, and recessive white skin on the chicken Z chromosome. Poultry Science, 1988, 67(4): 530–533

[15] Dorshorst B J, Ashwell C M. Genetic mapping of the sex-linked barring gene in the chicken. Poultry Science, 2009, 88(9): 1811–1817

[16] Groenen M A, Cheng H H, Bumstead N, Benkel B F, Briles W E, Burke T, Burt D W, Crittenden L B, Dodgson J, Hillel J, Lamont S, de Leon A P, Soller M, Takahashi H, Vignal A. A consensus linkage map of the chicken genome. Genome Research, 2000, 10(1): 137–147

[17] Levin I, Crittenden L B, Dodgson J B. Genetic map of the chicken Z chromosome using random amplified polymorphic DNA (RAPD) markers. Genomics, 1993, 16(1): 224–230

[18] Wright D, Kerje S, Lundström K, Babol J, Schütz K, Jensen P, Andersson L. Quantitative trait loci analysis of egg and meat production traits in a red junglefowl×White Leghorn cross. Animal Genetics, 2006, 37(6): 529–534

[19] Wang Y, Gu X, Feng C, Song C, Hu X, Li N. A genome-wide survey of copy number variation regions in various chicken breeds by array comparative genomic hybridization method. Animal Genetics, 2012, 43(3): 282–289

[20] Garcia R J, Ittah A, Mirabal S, Figueroa J, Lopez L, Glick A B, Kos L. Endothelin 3 induces skin pigmentation in a keratin-driven inducible mouse model. Journal of Investigative Dermatology, 2008, 128(1): 131–142

[21] Lahav R, Ziller C, Dupin E, Le Douarin N M. Endothelin 3 promotes neural crest cell proliferation and mediates a vast increase in melanocyte number in culture. Proceedings of the National Academy of Sciences of the United States of America, 1996, 93(9): 3892–3897

[22] Nataf V, Lecoin L, Eichmann A, Le Douarin N M. Endothelin-B receptor is expressed by neural crest cells in the avian embryo. Proceedings of the National Academy of Sciences of the United States of America, 1996, 93(18): 9645–9650

[23] Lecoin L, Sakurai T, Ngo M T, Abe Y, Yanagisawa M, Le Douarin N M. Cloning and characterization of a novel endothelin receptor subtype in the avian class. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(6): 3024–3029

[24] Dorshorst B, Molin A M, Rubin C J, Johansson A M, Strömstedt L, Pham M H, Chen C F, Hallböök F, Ashwell C, Andersson L. A complex genomic rearrangement involving the endothelin 3 locus causes dermal hyperpigmentation in the chicken. PLOS Genetics, 2011, 7(12): e1002412

[25] Stranger B E, Forrest M S, Dunning M, Ingle C E, Beazley C, Thorne N, Redon R, Bird C P, de Grassi A, Lee C, Tyler-Smith C, Carter N, Scherer S W, Tavaré S, Deloukas P, Hurles M E, Dermitzakis E T. Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science, 2007, 315(5813): 848–853

[26] Lahav R, Dupin E, Lecoin L, Glavieux C, Champeval D, Ziller C, Le Douarin N M. Endothelin 3 selectively promotes survival and proliferation of neural crest-derived glial and melanocytic precursors in vitro. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(24): 14214–14219

Acknowledgements

We are grateful to the Jiangsu Institute of Poultry Sciences and their members who provided samples, Dr. Zhe Yang (Agilent Technologies) for assistance with the array design, BerryGenomics Company for performing Illumina Solexa sequencing and Dr. Yujun Zhang (Bioyong Tech) for assistance with data analysis. This work was funded by the National Natural Science Foundation of China (U0831003) and the National Advanced Technology Research and Development Program of China (2011AA100301).Supplementary materialƒThe online version of this article at http://dx.doi.org/10.15302/J-FASE-2014026 contains supplementary material (Appendix A–E).

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg