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The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract

Unique patterns of inheritance and selection on Y chromosomes lead to the evolution of specialized gene functions. Yet characterizing the function of genes on Y chromosomes is notoriously difficult. We report CRISPR mutants in Drosophila of the Y-linked gene, WDY, which is required for male fertilit...

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Autores principales: Hafezi, Yassi, Omurzakov, Arsen, Carlisle, Jolie A., Caldas, Ian V., Wolfner, Mariana F., Clark, Andrew G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9915733/
https://www.ncbi.nlm.nih.gov/pubmed/36778485
http://dx.doi.org/10.1101/2023.02.02.526876
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author Hafezi, Yassi
Omurzakov, Arsen
Carlisle, Jolie A.
Caldas, Ian V.
Wolfner, Mariana F.
Clark, Andrew G.
author_facet Hafezi, Yassi
Omurzakov, Arsen
Carlisle, Jolie A.
Caldas, Ian V.
Wolfner, Mariana F.
Clark, Andrew G.
author_sort Hafezi, Yassi
collection PubMed
description Unique patterns of inheritance and selection on Y chromosomes lead to the evolution of specialized gene functions. Yet characterizing the function of genes on Y chromosomes is notoriously difficult. We report CRISPR mutants in Drosophila of the Y-linked gene, WDY, which is required for male fertility. WDY mutants produce mature sperm with beating tails that can be transferred to females but fail to enter the female sperm storage organs. We demonstrate that the sperm tails of WDY mutants beat approximately half as fast as wild-type sperm’s and that the mutant sperm do not propel themselves within the male ejaculatory duct or female reproductive tract (RT). These specific motility defects likely cause the sperm storage defect and sterility of the mutants. Regional and genotype-dependent differences in sperm motility suggest that sperm tail beating and propulsion do not always correlate. Furthermore, we find significant differences in the hydrophobicity of key residues of a putative calcium-binding domain between orthologs of WDY that are Y-linked and those that are autosomal. Given that WDY appears to be evolving under positive selection, our results suggest that WDY’s functional evolution coincides with its transition from autosomal to Y-linked in Drosophila melanogaster and its most closely related species. Finally, we show that mutants for another Y-linked gene, PRY, also show a sperm storage defect that may explain their subfertility. In contrast to WDY, PRY mutants do swim in the female RT, suggesting they are defective in yet another mode of motility, navigation, or a necessary interaction with the female RT. Overall, we provide direct evidence for the long-held presumption that protein-coding genes on the Drosophila Y regulate sperm motility.
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spelling pubmed-99157332023-02-11 The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract Hafezi, Yassi Omurzakov, Arsen Carlisle, Jolie A. Caldas, Ian V. Wolfner, Mariana F. Clark, Andrew G. bioRxiv Article Unique patterns of inheritance and selection on Y chromosomes lead to the evolution of specialized gene functions. Yet characterizing the function of genes on Y chromosomes is notoriously difficult. We report CRISPR mutants in Drosophila of the Y-linked gene, WDY, which is required for male fertility. WDY mutants produce mature sperm with beating tails that can be transferred to females but fail to enter the female sperm storage organs. We demonstrate that the sperm tails of WDY mutants beat approximately half as fast as wild-type sperm’s and that the mutant sperm do not propel themselves within the male ejaculatory duct or female reproductive tract (RT). These specific motility defects likely cause the sperm storage defect and sterility of the mutants. Regional and genotype-dependent differences in sperm motility suggest that sperm tail beating and propulsion do not always correlate. Furthermore, we find significant differences in the hydrophobicity of key residues of a putative calcium-binding domain between orthologs of WDY that are Y-linked and those that are autosomal. Given that WDY appears to be evolving under positive selection, our results suggest that WDY’s functional evolution coincides with its transition from autosomal to Y-linked in Drosophila melanogaster and its most closely related species. Finally, we show that mutants for another Y-linked gene, PRY, also show a sperm storage defect that may explain their subfertility. In contrast to WDY, PRY mutants do swim in the female RT, suggesting they are defective in yet another mode of motility, navigation, or a necessary interaction with the female RT. Overall, we provide direct evidence for the long-held presumption that protein-coding genes on the Drosophila Y regulate sperm motility. Cold Spring Harbor Laboratory 2023-02-23 /pmc/articles/PMC9915733/ /pubmed/36778485 http://dx.doi.org/10.1101/2023.02.02.526876 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Hafezi, Yassi
Omurzakov, Arsen
Carlisle, Jolie A.
Caldas, Ian V.
Wolfner, Mariana F.
Clark, Andrew G.
The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract
title The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract
title_full The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract
title_fullStr The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract
title_full_unstemmed The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract
title_short The Drosophila melanogaster Y-linked gene, WDY, is required for sperm to swim in the female reproductive tract
title_sort drosophila melanogaster y-linked gene, wdy, is required for sperm to swim in the female reproductive tract
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9915733/
https://www.ncbi.nlm.nih.gov/pubmed/36778485
http://dx.doi.org/10.1101/2023.02.02.526876
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