Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes

Jan E. Janečka; Brian W. Davis; Sharmila Ghosh; Nandina Paria; Pranab J. Das; Ludovic Orlando; Mikkel Schubert; Martin K. Nielsen; Tom A.E. Stout; Wesley Brashear; Gang Li; Charles D. Johnson; Richard P. Metz; Al Muatasim Al Zadjali; Charles C. Love; Dickson D. Varner; Daniel W. Bellott; William J. Murphy; Bhanu P. Chowdhary; Terje Raudsepp

doi:10.1038/s41467-018-05290-6

Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes

Jan E. Janečka
, Brian W. Davis
, Sharmila Ghosh
, Nandina Paria
, Pranab J. Das
, Ludovic Orlando
, Mikkel Schubert
, Martin K. Nielsen
, Tom A.E. Stout
, Wesley Brashear
, Gang Li
, Charles D. Johnson
, Richard P. Metz
, Al Muatasim Al Zadjali
, Charles C. Love
, Dickson D. Varner
, Daniel W. Bellott
, William J. Murphy
, Bhanu P. Chowdhary
, Terje Raudsepp

Veterinary Science

Research output: Contribution to journal › Article › peer-review

72 Scopus citations

Abstract

Dynamic evolutionary processes and complex structure make the Y chromosome among the most diverse and least understood regions in mammalian genomes. Here, we present an annotated assembly of the male specific region of the horse Y chromosome (eMSY), representing the first comprehensive Y assembly in odd-toed ungulates. The eMSY comprises single-copy, equine specific multi-copy, PAR transposed, and novel ampliconic sequence classes. The eMSY gene density approaches that of autosomes with the highest number of retained X–Y gametologs recorded in eutherians, in addition to novel Y-born and transposed genes. Horse, donkey and mule testis RNAseq reveals several candidate genes for stallion fertility. A novel testis-expressed XY ampliconic sequence class, ETSTY7, is shared with the parasite Parascaris genome, providing evidence for eukaryotic horizontal transfer and inter-chromosomal mobility. Our study highlights the dynamic nature of the Y and provides a reference sequence for improved understanding of equine male development and fertility.

Original language	English
Article number	2945
Journal	Nature Communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-05290-6
State	Published - Dec 1 2018

Bibliographical note

Publisher Copyright:
© 2018, The Author(s).

Funding

This work was supported by USDA (grant 2012-67015-19632, BPC, TR, JEJ), LINK Endowment Equine Foundation (BPC, TR), Danish National Research Foundation (grant DNRF94, LO, MS), Initiative d′Excellence Chaires d′attractivité, Université de Toulouse (OURASI, LO), the European Research Council (grant agreement ERC-CoG-2015-681605, LO, MS). We thank Dr. Loren Skow and Dr. François Piumi for providing BAC clones from TAMU and INRA BAC libraries, respectively; Dr. Doug Antzack and Dr. Donald Miller for providing blood samples and fibroblast cell lines from the Thoroughbred stallion Bravo; Elaine Owens for assisting with cell cultures; Dr. Vaishali Katju for providing DNA from C. elegans; Dr. Rytis Juras for the photos of a Parascaris specimen. Special thanks to Dr. James MacLeod from the University of Kentucky for bonding Y chromosome researchers with equine parasitologists.

Funders	Funder number
BPC
OURASI
U.S. Department of Agriculture
US Department of Agriculture National Institute of Food and Agriculture, Agriculture and Food Research Initiative	2012-67015-19632
US Department of Agriculture National Institute of Food and Agriculture, Agriculture and Food Research Initiative
Horizon 2020 Framework Programme	681605
Horizon 2020 Framework Programme
H2020 European Research Council	ERC-CoG-2015-681605
H2020 European Research Council
Danmarks Grundforskningsfond	DNRF94
Danmarks Grundforskningsfond
Université de Toulouse

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General
General Physics and Astronomy

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Cite this

Janečka, J. E., Davis, B. W., Ghosh, S., Paria, N., Das, P. J., Orlando, L., Schubert, M., Nielsen, M. K., Stout, T. A. E., Brashear, W., Li, G., Johnson, C. D., Metz, R. P., Zadjali, A. M. A., Love, C. C., Varner, D. D., Bellott, D. W., Murphy, W. J., Chowdhary, B. P., & Raudsepp, T. (2018). Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes. Nature Communications, 9(1), Article 2945. https://doi.org/10.1038/s41467-018-05290-6

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abstract = "Dynamic evolutionary processes and complex structure make the Y chromosome among the most diverse and least understood regions in mammalian genomes. Here, we present an annotated assembly of the male specific region of the horse Y chromosome (eMSY), representing the first comprehensive Y assembly in odd-toed ungulates. The eMSY comprises single-copy, equine specific multi-copy, PAR transposed, and novel ampliconic sequence classes. The eMSY gene density approaches that of autosomes with the highest number of retained X{\textendash}Y gametologs recorded in eutherians, in addition to novel Y-born and transposed genes. Horse, donkey and mule testis RNAseq reveals several candidate genes for stallion fertility. A novel testis-expressed XY ampliconic sequence class, ETSTY7, is shared with the parasite Parascaris genome, providing evidence for eukaryotic horizontal transfer and inter-chromosomal mobility. Our study highlights the dynamic nature of the Y and provides a reference sequence for improved understanding of equine male development and fertility.",

author = "Jane{\v c}ka, \{Jan E.\} and Davis, \{Brian W.\} and Sharmila Ghosh and Nandina Paria and Das, \{Pranab J.\} and Ludovic Orlando and Mikkel Schubert and Nielsen, \{Martin K.\} and Stout, \{Tom A.E.\} and Wesley Brashear and Gang Li and Johnson, \{Charles D.\} and Metz, \{Richard P.\} and Zadjali, \{Al Muatasim Al\} and Love, \{Charles C.\} and Varner, \{Dickson D.\} and Bellott, \{Daniel W.\} and Murphy, \{William J.\} and Chowdhary, \{Bhanu P.\} and Terje Raudsepp",

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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 2018, 'Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes', Nature Communications, vol. 9, no. 1, 2945. https://doi.org/10.1038/s41467-018-05290-6

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AU - Li, Gang

AU - Johnson, Charles D.

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AU - Zadjali, Al Muatasim Al

AU - Love, Charles C.

AU - Varner, Dickson D.

AU - Bellott, Daniel W.

AU - Murphy, William J.

AU - Chowdhary, Bhanu P.

AU - Raudsepp, Terje

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Horse Y chromosome assembly displays unique evolutionary features and putative stallion fertility genes

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

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