FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
PloS one2011; 6(7); e21374; doi: 10.1371/journal.pone.0021374

A gene catalogue of the euchromatic male-specific region of the horse Y chromosome: comparison with human and other mammals.

Abstract: Studies of the Y chromosome in primates, rodents and carnivores provide compelling evidence that the male specific region of Y (MSY) contains functional genes, many of which have specialized roles in spermatogenesis and male-fertility. Little similarity, however, has been found between the gene content and sequence of MSY in different species. This hinders the discovery of species-specific male fertility genes and limits our understanding about MSY evolution in mammals. Here, a detailed MSY gene catalogue was developed for the horse--an odd-toed ungulate. Using direct cDNA selection from horse testis, and sequence analysis of Y-specific BAC clones, 37 horse MSY genes/transcripts were identified. The genes were mapped to the MSY BAC contig map, characterized for copy number, analyzed for transcriptional profiles by RT-PCR, examined for the presence of ORFs, and compared to other mammalian orthologs. We demonstrate that the horse MSY harbors 20 X-degenerate genes with known orthologs in other eutherian species. The remaining 17 genes are acquired or novel and have so far been identified only in the horse or donkey Y chromosomes. Notably, 3 transcripts were found in the heterochromatic part of the Y. We show that despite substantial differences between the sequence, gene content and organization of horse and other mammalian Y chromosomes, the functions of MSY genes are predominantly related to testis and spermatogenesis. Altogether, 10 multicopy genes with testis-specific expression were identified in the horse MSY, and considered likely candidate genes for stallion fertility. The findings establish an important foundation for the study of Y-linked genetic factors governing fertility in stallions, and improve our knowledge about the evolutionary processes that have shaped Y chromosomes in different mammalian lineages.
Get Full Text
Publication Date: 2011-07-25 PubMed ID: 21799735PubMed Central: PMC3143126DOI: 10.1371/journal.pone.0021374Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Comparative Study
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper reports a detailed study about the unique genes identified within the male-specific region of Y (MSY) chromosome in horses, noting that despite structural differences between horse and other mammalian Y chromosomes, the functions of the genes are predominantly related to male fertility.

Research Background and Aim

  • The researchers were intrigued by the evidence gathered from previous studies on primates, rodents, and carnivores that showed the presence of functional genes within the MSY, which are crucial for male fertility and spermatogenesis.
  • However, they recognized a difficulty in pinpointing species-specific male fertility genes due to the lack of similarity in the gene content and sequence of MSY across different species.
  • This study aimed to create a comprehensive gene catalogue for the horse’s MSY, improve the understanding of MSY evolution in mammals, and perhaps give a lead for the discovery of species-specific male fertility genes.

Methods

  • The scientists employed cDNA selection directly from horse testis and conducted sequence analysis of Y-specific BAC clones to identify MSY genes/transcripts in horses.
  • They characterized the identified 37 horse MSY genes. This involved mapping the genes to the MSY BAC contig map, characterizing them for copy number, analyzing the transcriptional profiles using RT-PCR, checking for the presence of Open Reading Frames (ORFs), and comparing with other mammalian orthologs.

Findings

  • The researchers are claiming to have found 20 X-degenerate genes on horse MSY that have known orthologs in other eutherian species.
  • They also managed to identify a unique category of 17 genes that, so far, have only been found in the horse or donkey Y chromosomes. Out of these, 3 transcripts were discovered in the heterochromatic part of the Y.
  • The results point to a primary role of these genes in the horse MSY in relation to testis functions and spermatogenesis, regardless of the remarkable differences in sequence, gene content, and organization compared with other mammalian Y chromosomes.
  • Remarkably, they found 10 multicopy genes with testis-specific expression in the horse MSY, potentially linked to stallion fertility.

Conclusion

  • The findings of this research set an important groundwork for future research into Y-linked genetic factors affecting fertility in stallions.
  • Further, the catalogued horse MSY genes enhance the understanding of the evolutionary processes that have influenced the formation and organization of Y chromosomes across different mammalian lineages.

Cite This Article

APA
Paria N, Raudsepp T, Pearks Wilkerson AJ, O'Brien PC, Ferguson-Smith MA, Love CC, Arnold C, Rakestraw P, Murphy WJ, Chowdhary BP. (2011). A gene catalogue of the euchromatic male-specific region of the horse Y chromosome: comparison with human and other mammals. PLoS One, 6(7), e21374. https://doi.org/10.1371/journal.pone.0021374

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 6
Issue: 7
Pages: e21374
PII: e21374

Researcher Affiliations

Paria, Nandina
  • Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas, United States of America.
Raudsepp, Terje
    Pearks Wilkerson, Alison J
      O'Brien, Patricia C M
        Ferguson-Smith, Malcom A
          Love, Charles C
            Arnold, Carolyn
              Rakestraw, Peter
                Murphy, William J
                  Chowdhary, Bhanu P

                    MeSH Terms

                    • Animals
                    • Cats
                    • Cattle
                    • Contig Mapping
                    • DNA, Complementary / genetics
                    • Euchromatin / genetics
                    • Evolution, Molecular
                    • Female
                    • Fertility / genetics
                    • Gene Dosage / genetics
                    • Horses / genetics
                    • Horses / physiology
                    • Humans
                    • Male
                    • Mice
                    • Open Reading Frames / genetics
                    • RNA, Messenger / genetics
                    • Sex Characteristics
                    • Testis / metabolism
                    • X Chromosome / genetics
                    • Y Chromosome / genetics

                    Conflict of Interest Statement

                    The authors have declared that no competing interests exist.

                    References

                    This article includes 89 references

                    Citations

                    This article has been cited 35 times.
                    1. Cardinali I, Giontella A, Tommasi A, Silvestrelli M, Lancioni H. Unlocking Horse Y Chromosome Diversity. Genes (Basel) 2022 Dec 2;13(12).
                      doi: 10.3390/genes13122272pubmed: 36553539google scholar: lookup
                    2. Castaneda C, Radović L, Felkel S, Juras R, Davis BW, Cothran EG, Wallner B, Raudsepp T. Copy number variation of horse Y chromosome genes in normal equine populations and in horses with abnormal sex development and subfertility: relationship of copy number variations with Y haplogroups. G3 (Bethesda) 2022 Dec 1;12(12).
                      doi: 10.1093/g3journal/jkac278pubmed: 36227030google scholar: lookup
                    3. Rossetti C, Genualdo V, Incarnato D, Mottola F, Perucatti A, Pauciullo A. State of the art on the physical mapping of the Y-chromosome in the Bovidae and comparison with other species - A review. Anim Biosci 2022 Sep;35(9):1289-1302.
                      doi: 10.5713/ab.21.0480pubmed: 35240029google scholar: lookup
                    4. Naftaly AS, Pau S, White MA. Long-read RNA sequencing reveals widespread sex-specific alternative splicing in threespine stickleback fish. Genome Res 2021 Aug;31(8):1486-1497.
                      doi: 10.1101/gr.274282.120pubmed: 34131005google scholar: lookup
                    5. Jevit MJ, Davis BW, Castaneda C, Hillhouse A, Juras R, Trifonov VA, Tibary A, Pereira JC, Ferguson-Smith MA, Raudsepp T. An 8.22 Mb Assembly and Annotation of the Alpaca (Vicugna pacos) Y Chromosome. Genes (Basel) 2021 Jan 16;12(1).
                      doi: 10.3390/genes12010105pubmed: 33467186google scholar: lookup
                    6. Peichel CL, McCann SR, Ross JA, Naftaly AFS, Urton JR, Cech JN, Grimwood J, Schmutz J, Myers RM, Kingsley DM, White MA. Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution. Genome Biol 2020 Jul 19;21(1):177.
                      doi: 10.1186/s13059-020-02097-xpubmed: 32684159google scholar: lookup
                    7. Han H, Chen Q, Gao Y, Li J, Li W, Dang R, Lei C. Comparative Transcriptomics Analysis of Testicular miRNA from Cryptorchid and Normal Horses. Animals (Basel) 2020 Feb 21;10(2).
                      doi: 10.3390/ani10020338pubmed: 32098036google scholar: lookup
                    8. Villagomez DAF, Welsford EG, King WA, Revay T. Androgen Receptor Gene Variants in New Cases of Equine Androgen Insensitivity Syndrome. Genes (Basel) 2020 Jan 10;11(1).
                      doi: 10.3390/genes11010078pubmed: 31936796google scholar: lookup
                    9. Han H, Dong H, Chen Q, Gao Y, Li J, Li W, Dang R, Lei C. Transcriptomic Analysis of Testicular Gene Expression in Normal and Cryptorchid Horses. Animals (Basel) 2020 Jan 8;10(1).
                      doi: 10.3390/ani10010102pubmed: 31936283google scholar: lookup
                    10. Sun T, Hanif Q, Chen H, Lei C, Dang R. Copy Number Variations of Four Y-Linked Genes in Swamp Buffaloes. Animals (Basel) 2019 Dec 22;10(1).
                      doi: 10.3390/ani10010031pubmed: 31877875google scholar: lookup
                    11. Jacobs SAH, Gart E, Vreeken D, Franx BAA, Wekking L, Verweij VGM, Worms N, Schoemaker MH, Gross G, Morrison MC, Kleemann R, Arnoldussen IAC, Kiliaan AJ. Sex-Specific Differences in Fat Storage, Development of Non-Alcoholic Fatty Liver Disease and Brain Structure in Juvenile HFD-Induced Obese Ldlr-/-.Leiden Mice. Nutrients 2019 Aug 10;11(8).
                      doi: 10.3390/nᄈ1861pubmed: 31405127google scholar: lookup
                    12. Das PP, Krishnan G, Doley J, Biswas TK, Paul V, Chakravarty P, Mohan Deb S, Das PJ. Identification and expression profiling of MSY genes of yak for bull fertility. J Genet 2019 Jun;98(2).
                      pubmed: 31204701
                    13. Rando HM, Wadlington WH, Johnson JL, Stutchman JT, Trut LN, Farré M, Kukekova AV. The Red Fox Y-Chromosome in Comparative Context. Genes (Basel) 2019 May 28;10(6).
                      doi: 10.3390/genes10060409pubmed: 31142040google scholar: lookup
                    14. Felkel S, Vogl C, Rigler D, Dobretsberger V, Chowdhary BP, Distl O, Fries R, Jagannathan V, Janečka JE, Leeb T, Lindgren G, McCue M, Metzger J, Neuditschko M, Rattei T, Raudsepp T, Rieder S, Rubin CJ, Schaefer R, Schlötterer C, Thaller G, Tetens J, Velie B, Brem G, Wallner B. The horse Y chromosome as an informative marker for tracing sire lines. Sci Rep 2019 Apr 15;9(1):6095.
                      doi: 10.1038/s41598-019-42640-wpubmed: 30988347google scholar: lookup
                    15. Brashear WA, Raudsepp T, Murphy WJ. Evolutionary conservation of Y Chromosome ampliconic gene families despite extensive structural variation. Genome Res 2018 Dec;28(12):1841-1851.
                      doi: 10.1101/gr.237586.118pubmed: 30381290google scholar: lookup
                    16. Janečka JE, Davis BW, Ghosh S, Paria N, Das PJ, Orlando L, Schubert M, Nielsen MK, Stout TAE, Brashear W, Li G, Johnson CD, Metz RP, Zadjali AMA, Love CC, Varner DD, Bellott DW, Murphy WJ, Chowdhary BP, Raudsepp T. Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes. Nat Commun 2018 Jul 27;9(1):2945.
                      doi: 10.1038/s41467-018-05290-6pubmed: 30054462google scholar: lookup
                    17. Chen H, Ren Z, Zhao J, Zhang C, Yang X. Y-chromosome polymorphisms of the domestic Bactrian camel in China. J Genet 2018 Mar;97(1):3-10.
                      pubmed: 29666320
                    18. Oluwole OA, Mahboubi K, Favetta LA, Revay T, Kroetsch T, King WA. Highly dynamic temporal changes of TSPY gene copy number in aging bulls. PLoS One 2017;12(5):e0178558.
                      doi: 10.1371/journal.pone.0178558pubmed: 28552978google scholar: lookup
                    19. Hallast P, Jobling MA. The Y chromosomes of the great apes. Hum Genet 2017 May;136(5):511-528.
                      doi: 10.1007/s00439-017-1769-8pubmed: 28265767google scholar: lookup
                    20. Murata C, Kuroki Y, Imoto I, Kuroiwa A. Ancestral Y-linked genes were maintained by translocation to the X and Y chromosomes fused to an autosomal pair in the Okinawa spiny rat Tokudaia muenninki. Chromosome Res 2016 Sep;24(3):407-19.
                      doi: 10.1007/s10577-016-9531-ypubmed: 27333765google scholar: lookup
                    21. Skinner BM, Sargent CA, Churcher C, Hunt T, Herrero J, Loveland JE, Dunn M, Louzada S, Fu B, Chow W, Gilbert J, Austin-Guest S, Beal K, Carvalho-Silva D, Cheng W, Gordon D, Grafham D, Hardy M, Harley J, Hauser H, Howden P, Howe K, Lachani K, Ellis PJ, Kelly D, Kerry G, Kerwin J, Ng BL, Threadgold G, Wileman T, Wood JM, Yang F, Harrow J, Affara NA, Tyler-Smith C. The pig X and Y Chromosomes: structure, sequence, and evolution. Genome Res 2016 Jan;26(1):130-9.
                      doi: 10.1101/gr.188839.114pubmed: 26560630google scholar: lookup
                    22. Quach AT, Oluwole O, King WA, Revay T. The Porcine TSPY Gene Is Tricopy but Not a Copy Number Variant. PLoS One 2015;10(7):e0131745.
                      doi: 10.1371/journal.pone.0131745pubmed: 26133983google scholar: lookup
                    23. Han H, Zhang Q, Gao K, Yue X, Zhang T, Dang R, Lan X, Chen H, Lei C. Y-Single Nucleotide Polymorphisms Diversity in Chinese Indigenous Horse. Asian-Australas J Anim Sci 2015 Aug;28(8):1066-74.
                      doi: 10.5713/ajas.14.0784pubmed: 26104513google scholar: lookup
                    24. Soh YQ, Alföldi J, Pyntikova T, Brown LG, Graves T, Minx PJ, Fulton RS, Kremitzki C, Koutseva N, Mueller JL, Rozen S, Hughes JF, Owens E, Womack JE, Murphy WJ, Cao Q, de Jong P, Warren WC, Wilson RK, Skaletsky H, Page DC. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 2014 Nov 6;159(4):800-13.
                      doi: 10.1016/j.cell.2014.09.052pubmed: 25417157google scholar: lookup
                    25. Ghosh S, Qu Z, Das PJ, Fang E, Juras R, Cothran EG, McDonell S, Kenney DG, Lear TL, Adelson DL, Chowdhary BP, Raudsepp T. Copy number variation in the horse genome. PLoS Genet 2014 Oct;10(10):e1004712.
                      doi: 10.1371/journal.pgen.1004712pubmed: 25340504google scholar: lookup
                    26. Chang TC, Yang Y, Retzel EF, Liu WS. Male-specific region of the bovine Y chromosome is gene rich with a high transcriptomic activity in testis development. Proc Natl Acad Sci U S A 2013 Jul 23;110(30):12373-8.
                      doi: 10.1073/pnas.1221104110pubmed: 23842086google scholar: lookup
                    27. Wallner B, Vogl C, Shukla P, Burgstaller JP, Druml T, Brem G. Identification of genetic variation on the horse y chromosome and the tracing of male founder lineages in modern breeds. PLoS One 2013;8(4):e60015.
                      doi: 10.1371/journal.pone.0060015pubmed: 23573227google scholar: lookup
                    28. Mukherjee A, Dass G, G JM, Gohain M, Brahma B, Datta TK, De S. Absolute copy number differences of Y chromosomal genes between crossbred (Bos taurus × Bos indicus) and Indicine bulls. J Anim Sci Biotechnol 2013 Apr 4;4(1):15.
                      doi: 10.1186/2049-1891-4-15pubmed: 23556478google scholar: lookup
                    29. Das PJ, McCarthy F, Vishnoi M, Paria N, Gresham C, Li G, Kachroo P, Sudderth AK, Teague S, Love CC, Varner DD, Chowdhary BP, Raudsepp T. Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq. PLoS One 2013;8(2):e56535.
                      doi: 10.1371/journal.pone.0056535pubmed: 23409192google scholar: lookup
                    30. Skinner BM, Lachani K, Sargent CA, Affara NA. Regions of XY homology in the pig X chromosome and the boundary of the pseudoautosomal region. BMC Genet 2013 Jan 15;14:3.
                      doi: 10.1186/1471-2156-14-3pubmed: 23320497google scholar: lookup
                    31. Raudsepp T, McCue ME, Das PJ, Dobson L, Vishnoi M, Fritz KL, Schaefer R, Rendahl AK, Derr JN, Love CC, Varner DD, Chowdhary BP. Genome-wide association study implicates testis-sperm specific FKBP6 as a susceptibility locus for impaired acrosome reaction in stallions. PLoS Genet 2012;8(12):e1003139.
                      doi: 10.1371/journal.pgen.1003139pubmed: 23284302google scholar: lookup
                    32. Betrán E, Demuth JP, Williford A. Why chromosome palindromes?. Int J Evol Biol 2012;2012:207958.
                      doi: 10.1155/2012/207958pubmed: 22844637google scholar: lookup
                    33. Bellott DW, Skaletsky H, Hughes JF, Brown LG, Pyntikova T, Cho TJ, Koutseva N, Zaghlul S, Kizghin D, Mendoza M, Raudsepp T, Dugan S, Khan Z, Wang Q, Watt J, Worley KC, Scherer S, Muzny DM, Gibbs RA, Page DC. The SHR/Akr Y chromosome reveals repeated turnover of the rat pseudoautosomal region. bioRxiv 2025 Jun 1;.
                      doi: 10.1101/2025.05.28.656580pubmed: 40501880google scholar: lookup
                    34. Olagunju TA, Rosen BD, Neibergs HL, Becker GM, Davenport KM, Elsik CG, Hadfield TS, Koren S, Kuhn KL, Rhie A, Shira KA, Skibiel AL, Stegemiller MR, Thorne JW, Villamediana P, Cockett NE, Murdoch BM, Smith TPL. Telomere-to-telomere assemblies of cattle and sheep Y-chromosomes uncover divergent structure and gene content. Nat Commun 2024 Sep 27;15(1):8277.
                      doi: 10.1038/s41467-024-52384-5pubmed: 39333471google scholar: lookup
                    35. Smith T, Olagunju T, Rosen B, Neibergs H, Becker G, Davenport K, Elsik C, Hadfield T, Koren S, Kuhn K, Rhie A, Shira K, Skibiel A, Stegemiller M, Thorne J, Villamediana P, Cockett N, Murdoch B. The first complete T2T Assemblies of Cattle and Sheep Y-Chromosomes uncover remarkable divergence in structure and gene content. Res Sq 2024 Apr 3;.
                      doi: 10.21203/rs.3.rs-4033388/v1pubmed: 38712074google scholar: lookup
                    Subscribe to our newsletter
                    Join 99,658 horse owners like you who receive our email updates on horse health and nutrition.