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Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution

BACKGROUND: Heteromorphic sex chromosomes have evolved repeatedly across diverse species. Suppression of recombination between X and Y chromosomes leads to degeneration of the Y chromosome. The progression of degeneration is not well understood, as complete sequence assemblies of heteromorphic Y chr...

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Autores principales: Peichel, Catherine L., McCann, Shaugnessy R., Ross, Joseph A., Naftaly, Alice F. S., Urton, James R., Cech, Jennifer N., Grimwood, Jane, Schmutz, Jeremy, Myers, Richard M., Kingsley, David M., White, Michael A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7368989/
https://www.ncbi.nlm.nih.gov/pubmed/32684159
http://dx.doi.org/10.1186/s13059-020-02097-x
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author Peichel, Catherine L.
McCann, Shaugnessy R.
Ross, Joseph A.
Naftaly, Alice F. S.
Urton, James R.
Cech, Jennifer N.
Grimwood, Jane
Schmutz, Jeremy
Myers, Richard M.
Kingsley, David M.
White, Michael A.
author_facet Peichel, Catherine L.
McCann, Shaugnessy R.
Ross, Joseph A.
Naftaly, Alice F. S.
Urton, James R.
Cech, Jennifer N.
Grimwood, Jane
Schmutz, Jeremy
Myers, Richard M.
Kingsley, David M.
White, Michael A.
author_sort Peichel, Catherine L.
collection PubMed
description BACKGROUND: Heteromorphic sex chromosomes have evolved repeatedly across diverse species. Suppression of recombination between X and Y chromosomes leads to degeneration of the Y chromosome. The progression of degeneration is not well understood, as complete sequence assemblies of heteromorphic Y chromosomes have only been generated across a handful of taxa with highly degenerate sex chromosomes. Here, we describe the assembly of the threespine stickleback (Gasterosteus aculeatus) Y chromosome, which is less than 26 million years old and at an intermediate stage of degeneration. Our previous work identified that the non-recombining region between the X and the Y spans approximately 17.5 Mb on the X chromosome. RESULTS: We combine long-read sequencing with a Hi-C-based proximity guided assembly to generate a 15.87 Mb assembly of the Y chromosome. Our assembly is concordant with cytogenetic maps and Sanger sequences of over 90 Y chromosome BAC clones. We find three evolutionary strata on the Y chromosome, consistent with the three inversions identified by our previous cytogenetic analyses. The threespine stickleback Y shows convergence with more degenerate sex chromosomes in the retention of haploinsufficient genes and the accumulation of genes with testis-biased expression, many of which are recent duplicates. However, we find no evidence for large amplicons identified in other sex chromosome systems. We also report an excellent candidate for the master sex-determination gene: a translocated copy of Amh (Amhy). CONCLUSIONS: Together, our work shows that the evolutionary forces shaping sex chromosomes can cause relatively rapid changes in the overall genetic architecture of Y chromosomes.
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spelling pubmed-73689892020-07-21 Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution Peichel, Catherine L. McCann, Shaugnessy R. Ross, Joseph A. Naftaly, Alice F. S. Urton, James R. Cech, Jennifer N. Grimwood, Jane Schmutz, Jeremy Myers, Richard M. Kingsley, David M. White, Michael A. Genome Biol Research BACKGROUND: Heteromorphic sex chromosomes have evolved repeatedly across diverse species. Suppression of recombination between X and Y chromosomes leads to degeneration of the Y chromosome. The progression of degeneration is not well understood, as complete sequence assemblies of heteromorphic Y chromosomes have only been generated across a handful of taxa with highly degenerate sex chromosomes. Here, we describe the assembly of the threespine stickleback (Gasterosteus aculeatus) Y chromosome, which is less than 26 million years old and at an intermediate stage of degeneration. Our previous work identified that the non-recombining region between the X and the Y spans approximately 17.5 Mb on the X chromosome. RESULTS: We combine long-read sequencing with a Hi-C-based proximity guided assembly to generate a 15.87 Mb assembly of the Y chromosome. Our assembly is concordant with cytogenetic maps and Sanger sequences of over 90 Y chromosome BAC clones. We find three evolutionary strata on the Y chromosome, consistent with the three inversions identified by our previous cytogenetic analyses. The threespine stickleback Y shows convergence with more degenerate sex chromosomes in the retention of haploinsufficient genes and the accumulation of genes with testis-biased expression, many of which are recent duplicates. However, we find no evidence for large amplicons identified in other sex chromosome systems. We also report an excellent candidate for the master sex-determination gene: a translocated copy of Amh (Amhy). CONCLUSIONS: Together, our work shows that the evolutionary forces shaping sex chromosomes can cause relatively rapid changes in the overall genetic architecture of Y chromosomes. BioMed Central 2020-07-19 /pmc/articles/PMC7368989/ /pubmed/32684159 http://dx.doi.org/10.1186/s13059-020-02097-x Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Peichel, Catherine L.
McCann, Shaugnessy R.
Ross, Joseph A.
Naftaly, Alice F. S.
Urton, James R.
Cech, Jennifer N.
Grimwood, Jane
Schmutz, Jeremy
Myers, Richard M.
Kingsley, David M.
White, Michael A.
Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution
title Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution
title_full Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution
title_fullStr Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution
title_full_unstemmed Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution
title_short Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution
title_sort assembly of the threespine stickleback y chromosome reveals convergent signatures of sex chromosome evolution
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7368989/
https://www.ncbi.nlm.nih.gov/pubmed/32684159
http://dx.doi.org/10.1186/s13059-020-02097-x
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