The pig X and Y Chromosomes: structure, sequence, and evolution.

Benjamin M Skinner, Carole A Sargent, Carol Churcher, Toby Hunt, Javier Herrero, Jane E Loveland, Matt Dunn, Sandra Louzada, Beiyuan Fu, William Chow, James Gilbert, Siobhan Austin-Guest, Kathryn Beal, Denise Carvalho-Silva, William Cheng, Daria Gordon, Darren Grafham, Matt Hardy, Jo Harley, Heidi Hauser, Philip Howden, Kerstin Howe, Kim Lachani, Peter J I Ellis, Daniel Kelly, Giselle Kerry, James Kerwin, Bee Ling Ng, Glen Threadgold, Thomas Wileman, Jonathan M D Wood, Fengtang Yang, Jen Harrow, Nabeel A Affara, Chris Tyler-Smith
Author Information
  1. Benjamin M Skinner: Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom;
  2. Carole A Sargent: Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom;
  3. Carol Churcher: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  4. Toby Hunt: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  5. Javier Herrero: European Molecular Biology Laboratory, European Bioinformatics Institute, Hinxton, Cambridge CB10 1SD, United Kingdom; Bill Lyons Informatics Centre, UCL Cancer Institute, University College London, London WC1E 6BT, United Kingdom.
  6. Jane E Loveland: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  7. Matt Dunn: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  8. Sandra Louzada: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  9. Beiyuan Fu: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  10. William Chow: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  11. James Gilbert: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  12. Siobhan Austin-Guest: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  13. Kathryn Beal: European Molecular Biology Laboratory, European Bioinformatics Institute, Hinxton, Cambridge CB10 1SD, United Kingdom;
  14. Denise Carvalho-Silva: European Molecular Biology Laboratory, European Bioinformatics Institute, Hinxton, Cambridge CB10 1SD, United Kingdom;
  15. William Cheng: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  16. Daria Gordon: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  17. Darren Grafham: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  18. Matt Hardy: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  19. Jo Harley: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  20. Heidi Hauser: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  21. Philip Howden: Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom; Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  22. Kerstin Howe: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  23. Kim Lachani: Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom;
  24. Peter J I Ellis: Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom;
  25. Daniel Kelly: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  26. Giselle Kerry: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  27. James Kerwin: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  28. Bee Ling Ng: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  29. Glen Threadgold: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  30. Thomas Wileman: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  31. Jonathan M D Wood: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  32. Fengtang Yang: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  33. Jen Harrow: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  34. Nabeel A Affara: Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom;
  35. Chris Tyler-Smith: Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;

Abstract

We have generated an improved assembly and gene annotation of the pig X Chromosome, and a first draft assembly of the pig Y Chromosome, by sequencing BAC and fosmid clones from Duroc animals and incorporating information from optical mapping and fiber-FISH. The X Chromosome carries 1033 annotated genes, 690 of which are protein coding. Gene order closely matches that found in primates (including humans) and carnivores (including cats and dogs), which is inferred to be ancestral. Nevertheless, several protein-coding genes present on the human X Chromosome were absent from the pig, and 38 pig-specific X-chromosomal genes were annotated, 22 of which were olfactory receptors. The pig Y-specific Chromosome sequence generated here comprises 30 megabases (Mb). A 15-Mb subset of this sequence was assembled, revealing two clusters of male-specific low copy number genes, separated by an ampliconic region including the HSFY gene family, which together make up most of the short arm. Both clusters contain palindromes with high sequence identity, presumably maintained by gene conversion. Many of the ancestral X-related genes previously reported in at least one mammalian Y Chromosome are represented either as active genes or partial sequences. This sequencing project has allowed us to identify genes--both single copy and amplified--on the pig Y Chromosome, to compare the pig X and Y Chromosomes for homologous sequences, and thereby to reveal mechanisms underlying pig X and Y Chromosome evolution.

References

  1. Nat Genet. 2013 Sep;45(9):1083-7 [PMID: 23872635]
  2. Cytogenet Genome Res. 2013;141(1):26-36 [PMID: 23735614]
  3. Cold Spring Harb Symp Quant Biol. 2009;74:345-53 [PMID: 20508063]
  4. Nature. 2012 Nov 15;491(7424):393-8 [PMID: 23151582]
  5. BMC Genet. 2013;14:3 [PMID: 23320497]
  6. Nat Genet. 2013 Dec;45(12):1431-8 [PMID: 24162736]
  7. Clin Genet. 2013 Jul;84(1):86-90 [PMID: 23036093]
  8. Biol Reprod. 1996 Jul;55(1):47-53 [PMID: 8793057]
  9. Genome Res. 2004 May;14(5):963-70 [PMID: 15123593]
  10. PLoS Genet. 2013;9(7):e1003666 [PMID: 23935520]
  11. Anim Genet. 1998 Apr;29(2):157-8 [PMID: 9699287]
  12. Genome Res. 2012 Mar;22(3):498-507 [PMID: 22128133]
  13. Cell. 2014 Nov 6;159(4):800-13 [PMID: 25417157]
  14. PLoS One. 2011;6(7):e21374 [PMID: 21799735]
  15. Genome Res. 2004 Oct;14(10A):1861-9 [PMID: 15466286]
  16. Nat Rev Genet. 2013 Feb;14(2):113-24 [PMID: 23329112]
  17. PLoS One. 2011;6(10):e26195 [PMID: 22022562]
  18. Cold Spring Harb Symp Quant Biol. 2009;74:355-62 [PMID: 19717539]
  19. Mol Biol Evol. 2014 Sep;31(9):2365-75 [PMID: 24916032]
  20. Sex Dev. 2012;6(5):231-9 [PMID: 22688524]
  21. Hum Mol Genet. 2011 Aug 1;20(15):3010-21 [PMID: 21551453]
  22. Mol Biol Evol. 2011 Oct;28(10):2731-9 [PMID: 21546353]
  23. BMC Genomics. 2012;13:584 [PMID: 23153364]
  24. Nature. 2010 Jan 28;463(7280):536-9 [PMID: 20072128]
  25. Genome Res. 2013 Sep;23(9):1486-95 [PMID: 23788650]
  26. Database (Oxford). 2012;2012:bas009 [PMID: 22434843]
  27. Bioessays. 2004 Feb;26(2):159-69 [PMID: 14745834]
  28. Genome Res. 2002 Jan;12(1):26-36 [PMID: 11779828]
  29. Nucleic Acids Res. 1988 Nov 11;16(21):10389 [PMID: 3194222]
  30. Nature. 2003 Jun 19;423(6942):825-37 [PMID: 12815422]
  31. Science. 1997 Sep 5;277(5331):1518-23 [PMID: 9278517]
  32. Nucleic Acids Res. 2011 Jan;39(Database issue):D514-9 [PMID: 20929869]
  33. Genes (Basel). 2011 Jan 10;2(1):36-47 [PMID: 24710137]
  34. Cytogenet Cell Genet. 1999;84(3-4):150-5 [PMID: 10393417]
  35. Organogenesis. 2014 Jan 1;10(1):62-8 [PMID: 24743231]
  36. Genomics. 1996 Feb 1;31(3):367-72 [PMID: 8838319]
  37. Nucleic Acids Res. 1988 Dec 23;16(24):11842 [PMID: 3211765]
  38. Genome Res. 2009 May;19(5):770-7 [PMID: 19342477]
  39. BMC Genomics. 2013;14:332 [PMID: 23676093]
  40. Nature. 2014 Apr 24;508(7497):494-9 [PMID: 24759411]
  41. Genome Res. 2012 Sep;22(9):1760-74 [PMID: 22955987]
  42. J Biol Chem. 2005 Apr 15;280(15):14755-64 [PMID: 15671038]
  43. BMC Genomics. 2015;16:442 [PMID: 26055083]
  44. Science. 2013 Dec 20;342(6165):1518-21 [PMID: 24357321]
  45. Nature. 2002 Dec 5;420(6915):520-62 [PMID: 12466850]
  46. Cytogenet Cell Genet. 1992;61(2):152-4 [PMID: 1395727]
  47. Heredity (Edinb). 2012 Jan;108(1):37-41 [PMID: 22045382]
  48. Placenta. 2010 Mar;31 Suppl:S27-32 [PMID: 20163856]
  49. J Dent Res. 1996 Oct;75(10):1735-41 [PMID: 8955667]
  50. Am J Hum Genet. 2007 Feb;80(2):345-52 [PMID: 17236139]
  51. BMC Genomics. 2013;14:792 [PMID: 24228692]
  52. Mamm Genome. 2002 Oct;13(10):588-94 [PMID: 12420137]
  53. Nature. 2005 Mar 17;434(7031):325-37 [PMID: 15772651]
  54. Nature. 2014 Apr 24;508(7497):488-93 [PMID: 24759410]
  55. Genome Res. 2004 Feb;14(2):267-72 [PMID: 14762062]
  56. J Mol Evol. 1997 Jul;45(1):60-5 [PMID: 9211735]
  57. Mol Biol Evol. 2010 Nov;27(11):2437-40 [PMID: 20525900]
  58. Nature. 2003 Jun 19;423(6942):873-6 [PMID: 12815433]
  59. Bioessays. 2012 Dec;34(12):1035-44 [PMID: 23055411]
  60. Mol Biol Evol. 1986 Sep;3(5):418-26 [PMID: 3444411]
  61. PLoS One. 2013;8(4):e60482 [PMID: 23596509]
  62. Chromosome Res. 2010 Sep;18(6):623-34 [PMID: 20574822]
  63. Heredity (Edinb). 2012 Jan;108(1):50-8 [PMID: 22086077]
  64. Science. 2009 Apr 24;324(5926):522-8 [PMID: 19390049]
  65. Int J Androl. 2008 Aug;31(4):376-82 [PMID: 18399979]
  66. Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12373-8 [PMID: 23842086]
  67. Trends Genet. 2011 Sep;27(9):358-67 [PMID: 21962971]
  68. Hum Mol Genet. 2007 Apr 1;16(7):763-73 [PMID: 17327269]

Grants

  1. BB/I025506/1/Biotechnology and Biological Sciences Research Council
  2. WT098051/Wellcome Trust
  3. U41 HG007234/NHGRI NIH HHS
  4. BB/F021372/1/Biotechnology and Biological Sciences Research Council
  5. 095908/Wellcome Trust
  6. /Wellcome Trust

MeSH Term

Animals
Base Sequence
Cats
Chromosomes, Mammalian
Dogs
Evolution, Molecular
Female
Gene Conversion
Gene Expression
Gene Library
Gene Order
Humans
Male
Molecular Sequence Data
Sequence Alignment
Sequence Analysis, DNA
Swine
X Chromosome
Y Chromosome

Word Cloud

Created with Highcharts 10.0.0pigChromosomeXYgenessequencegeneincludinggeneratedassemblysequencingannotatedancestralclusterscopysequencesevolutionimprovedannotationfirstdraftBACfosmidclonesDurocanimalsincorporatinginformationopticalmappingfiber-FISHcarries1033690proteincodingGeneordercloselymatchesfoundprimateshumanscarnivorescatsdogsinferredNeverthelessseveralprotein-codingpresenthumanabsent38pig-specificX-chromosomal22olfactoryreceptorsY-specificcomprises30megabasesMb15-Mbsubsetassembledrevealingtwomale-specificlownumberseparatedampliconicregionHSFYfamilytogethermakeshortarmcontainpalindromeshighidentitypresumablymaintainedconversionManyX-relatedpreviouslyreportedleastonemammalianrepresentedeitheractivepartialprojectallowedusidentifygenes--bothsingleamplified--oncompareChromosomeshomologoustherebyrevealmechanismsunderlyingChromosomes:structure

Similar Articles

Cited By