The Mutation in Chickens Constitutes a Structural Rearrangement Causing Both Altered Comb Morphology and Defective Sperm Motility
Rose-comb, a classical monogenic trait of chickens, is characterized by a drastically altered comb morphology compared to the single-combed wild-type. Here we show that Rose-comb is caused by a 7.4 Mb inversion on chromosome 7 and that a second Rose-comb allele arose by unequal crossing over between a Rose-comb and wild-type chromosome. The comb phenotype is caused by the relocalization of the MNR2 homeodomain protein gene leading to transient ectopic expression of MNR2 during comb development. We also provide a molecular explanation for the first example of epistatic interaction reported by Bateson and Punnett 104 years ago, namely that walnut-comb is caused by the combined effects of the Rose-comb and Pea-comb alleles. Transient ectopic expression of MNR2 and SOX5 (causing the Pea-comb phenotype) occurs in the same population of mesenchymal cells and with at least partially overlapping expression in individual cells in the comb primordium. Rose-comb has pleiotropic effects, as homozygosity in males has been associated with poor sperm motility. We postulate that this is caused by the disruption of the CCDC108 gene located at one of the inversion breakpoints. CCDC108 is a poorly characterized protein, but it contains a MSP (major sperm protein) domain and is expressed in testis. The study illustrates several characteristic features of the genetic diversity present in domestic animals, including the evolution of alleles by two or more consecutive mutations and the fact that structural changes have contributed to fast phenotypic evolution.
Vyšlo v časopise:
The Mutation in Chickens Constitutes a Structural Rearrangement Causing Both Altered Comb Morphology and Defective Sperm Motility. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002775
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002775
Souhrn
Rose-comb, a classical monogenic trait of chickens, is characterized by a drastically altered comb morphology compared to the single-combed wild-type. Here we show that Rose-comb is caused by a 7.4 Mb inversion on chromosome 7 and that a second Rose-comb allele arose by unequal crossing over between a Rose-comb and wild-type chromosome. The comb phenotype is caused by the relocalization of the MNR2 homeodomain protein gene leading to transient ectopic expression of MNR2 during comb development. We also provide a molecular explanation for the first example of epistatic interaction reported by Bateson and Punnett 104 years ago, namely that walnut-comb is caused by the combined effects of the Rose-comb and Pea-comb alleles. Transient ectopic expression of MNR2 and SOX5 (causing the Pea-comb phenotype) occurs in the same population of mesenchymal cells and with at least partially overlapping expression in individual cells in the comb primordium. Rose-comb has pleiotropic effects, as homozygosity in males has been associated with poor sperm motility. We postulate that this is caused by the disruption of the CCDC108 gene located at one of the inversion breakpoints. CCDC108 is a poorly characterized protein, but it contains a MSP (major sperm protein) domain and is expressed in testis. The study illustrates several characteristic features of the genetic diversity present in domestic animals, including the evolution of alleles by two or more consecutive mutations and the fact that structural changes have contributed to fast phenotypic evolution.
Zdroje
1. BatesonW 1902 Experiments with poultry. Rep Evol Comm Roy Soc 1 87 124
2. BatesonWPunnettRC 1908 Experimental studies in the physiology of heredity. Poultry. Repts Evol Comm Roy Soc 4 18 35
3. SomesRGJ 1996 Mutations and major variants of plumage and skin in chickens. CrawfordRD Poultry Breeding and Genetics New York Elsevier Science 169 208
4. CavalieAMératP 1965 Un nouveau gène, modificateur de la forme des crêtes en rose, et son incidence possible sur la fertilité. Ann Biol Anim Bioch Biophys 5 451 468
5. PunnettRC 1923 Heredity in Poultry London Mac Millan and Co., Ltd
6. HindhaughWLS 1932 Some observations on fertility in White Wyandottes. Poultry J 17 555 560
7. HuttFB 1940 A relationship between breed characteristics and poor reproduction in white wyandotte fowls. American Naturalist 74 148 156
8. CrawfordRD 1971 Rose comb and fertility in Silver Spangled Hamburgs. Poultry Sci 47 867 869
9. CrawfordRDSmythJRJ 1964 Studies of the relationship between fertility and the gene for Rose Comb in the domestic fowl - 1. The relationship between comb genotype and fertility. Poultry Sci 43 1009 1017
10. CrawfordRDSmythJRJ 1964 Studies of the relationship between fertility and the gene for Rose Comb in the domestic fowl - 2.The relationship between comb genotype and duration of fertility. Poultry Sci 43 1018 1026
11. CrawfordRDSmythJRJ 1964 Semen quality and the gene for Rose Comb in the domestic fowl. Poultry Sci 43 1551 1557
12. PetitjeanMServouseM 1981 Comparative study of some characteristics of the semen of RR (Rose Comb) and rr (Single Comb) cockerels. Reprod Nutr Develop 21 1085 1093
13. KirbyJD 1994 Analysis of subfertility associated with homozygosity of the Rose Comb allele in the male domestic fowl. Poultry Sci 73 871
14. McLeanDJFromanDP 1996 Identification of a sperm cell attribute responsible for subfertility of roosters homozygous for the Rose Comb allele. Biol Reprod 54 168 172
15. McLeanDJJonesLGJFromanDP 1997 Reduced glucose transport in sperm from roosters (Gallus domesticus) with heritable subfertility. Biol Reprod 57 791 795
16. CrawfordRD 1965 Comb dimorphism in Wyandotte domestic fowl. I Sperm competition in relation to Rose and Single Comb alleles. Can J Genet Cytol 7 500 504
17. BucklandRBHawesRO 1968 Comb type and reproduction in the male fowl. Segregation of the Rose and Pea comb genes. Can J Genet Cytol 10 395 400
18. CrawfordRDMerrittE 1963 The relationship between Rose Comb and reproduction in the domestic fowl. Can J Genet Cytol 5 89 95
19. WehrhahnCFCrawfordRD 1965 Comb dimorphism in Wyandotte domestic fowl. II Population genetics of the Rose Comb gene. Can J Genet Cytol 7 651 657
20. TanabeYWilliamCJessellTM 1998 Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95 67 80
21. WrightDBoijeHMeadowsJRSBed'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
22. SomesRGJ 1973 Linkage relationships in the fowl. J Hered 64 217 221
23. DorshorstBOkimotoRAshwellC 2010 Genomic regions associated with dermal hyperpigmentation, polydactyly and other morphological traits in the Silkie chicken. J Hered 101 339 350
24. GroenenMAWahlbergPFoglioMChengHHMegensH-J 2009 A high-density SNP based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 19 510 519
25. GroenenMAMegensHJZareYWarrenWCHillierLW 2011 The development and characterization of a 60K SNP chip for chicken. BMC Genomics 12 274
26. WilliamCMTanabeYJessellTM 2003 Regulation of motor neuron subtype identity by repressor activity of Mnx class homeodomain proteins. Development 130 1523 1536
27. MészárZFelszeghySVeressGMateszKSzékelyG 2008 Hyaluronan accumulates around differentiating neurons in spinal cord of chicken embryos. Brain Res Bull 75 414 418
28. LawrenceIEJ 1963 An experimental analysis of comb development in the chick. J Exp Zool 152 205 218
29. LawrenceIEJ 1968 Regional influences on development of the single comb primordium. J Exp Zool 167 263 273
30. LawrenceIEJ 1971 Timed reciprocal dermal-epidermal interactions between comb, mid-dorsal, and tarsometatarsal. J Exp Zool 178 195 209
31. MarklundSKijasJRodriguez-MartinezHRönnstrandLFunaK 1998 Molecular basis for the dominant white phenotype in the domestic pig. Genome Res 8 826 833
32. KijasJMHMollerMPlastowGAnderssonL 2001 A frameshift mutation in MC1R and a high frequency of somatic reversions cause black spotting in pigs. Genetics 158 779 785
33. AnderssonL 2011 How selective sweeps in domestic animals provides new insight about biological mechanisms. Journal of Internal Medicine In press
34. DorshorstBMolinA-MJohanssonAStrömstedtLPhamM-H 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
35. HastingsPLupskiJRRosenbergSIraG 2009 Mechanisms of change in gene copy number. Nature Reviews Genetics 10 551 564
36. ZhangFCarvalhoCLupskiJR 2009 Complex human chromosomal and genomic rearrangements. Trends in Genetics 25 298 307
37. AltshulerDDalyMJLanderES 2008 Genetic mapping in human disease. Science 322 881 888
38. ShimaJEMcLeanDJMcCarreyJRGriswoldMD 2004 The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 71 319 330
39. PazourGJAgrinNLeszykJWitmanGB 2005 Proteomic analysis of a eukaryotic cilium. Journal of Cell Biology 170 103 113
40. NakanoTImaiSKogaTSimJS 1997 Light microscopic histochemical and immunohistochemical localisation of sulphated glycoseaminoglycans in the rooster comb and wattle tissues. J Anat 189 643 650
41. LefebvreVLiPde CrombruggheB 1998 A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 17 5718 5733
42. StoltCCSchlierfALommesPHillgärtnerSWernerT 2006 SoxD proteins influence multiple stages of oligodendrocyte development and modulate SoxE protein function. Dev Cell 11 697 709
43. HillelJGroenenMAMTixier-BoichardMKorolABDavidL 2003 Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet Sel Evol 35 533 557
44. GreenPFallsKCrookS 1990 Documentation for CRI-MAP, version 2.4. St Louis, MO: Washington University School of Medicine
45. CrooijmansRVrebalovJDijkhofRvan der PoelJGroenenM 2000 Two-dimensional screening of the Wageningen chicken BAC library. Mammalian Genome 11 360 363
46. YerleMGalmanOLahbib-MansaisYGellinJ 1992 Localization of the pig luteinizing hormone/choriogonadotropin receptor gene (LHCGR) by radioactive and nonradioactive in situ hybridization. Cytogenet Cell Genet 59 48 51
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 6
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Rumors of Its Disassembly Have Been Greatly Exaggerated: The Secret Life of the Synaptonemal Complex at the Centromeres
- The NSL Complex Regulates Housekeeping Genes in
- Tipping the Balance in the Powerhouse of the Cell to “Protect” Colorectal Cancer
- Interplay between Synaptonemal Complex, Homologous Recombination, and Centromeres during Mammalian Meiosis