Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.

Segregation Distorter (SD) is a male meiotic drive system in Drosophila melanogaster. Males heterozygous for a selfish SD chromosome rarely transmit the homologous SD+ chromosome. It is well established that distortion results from an interaction between Sd, the primary distorting locus on the SD ch...

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Autores principales:	Marion Herbette, Xiaolu Wei, Ching-Ho Chang, Amanda M Larracuente, Benjamin Loppin, Raphaëlle Dubruille
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/34761be6f8de43f3864747c2085ed363
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spelling	oai:doaj.org-article:34761be6f8de43f3864747c2085ed3632021-12-02T20:02:57ZDistinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.1553-73901553-740410.1371/journal.pgen.1009662https://doaj.org/article/34761be6f8de43f3864747c2085ed3632021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009662https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Segregation Distorter (SD) is a male meiotic drive system in Drosophila melanogaster. Males heterozygous for a selfish SD chromosome rarely transmit the homologous SD+ chromosome. It is well established that distortion results from an interaction between Sd, the primary distorting locus on the SD chromosome and its target, a satellite DNA called Rsp, on the SD+ chromosome. However, the molecular and cellular mechanisms leading to post-meiotic SD+ sperm elimination remain unclear. Here we show that SD/SD+ males of different genotypes but with similarly strong degrees of distortion have distinct spermiogenic phenotypes. In some genotypes, SD+ spermatids fail to fully incorporate protamines after the removal of histones, and degenerate during the individualization stage of spermiogenesis. In contrast, in other SD/SD+ genotypes, protamine incorporation appears less disturbed, yet spermatid nuclei are abnormally compacted, and mature sperm nuclei are eventually released in the seminal vesicle. Our analyses of different SD+ chromosomes suggest that the severity of the spermiogenic defects associates with the copy number of the Rsp satellite. We propose that when Rsp copy number is very high (> 2000), spermatid nuclear compaction defects reach a threshold that triggers a checkpoint controlling sperm chromatin quality to eliminate abnormal spermatids during individualization.Marion HerbetteXiaolu WeiChing-Ho ChangAmanda M LarracuenteBenjamin LoppinRaphaëlle DubruillePublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009662 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Marion Herbette Xiaolu Wei Ching-Ho Chang Amanda M Larracuente Benjamin Loppin Raphaëlle Dubruille Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.
description	Segregation Distorter (SD) is a male meiotic drive system in Drosophila melanogaster. Males heterozygous for a selfish SD chromosome rarely transmit the homologous SD+ chromosome. It is well established that distortion results from an interaction between Sd, the primary distorting locus on the SD chromosome and its target, a satellite DNA called Rsp, on the SD+ chromosome. However, the molecular and cellular mechanisms leading to post-meiotic SD+ sperm elimination remain unclear. Here we show that SD/SD+ males of different genotypes but with similarly strong degrees of distortion have distinct spermiogenic phenotypes. In some genotypes, SD+ spermatids fail to fully incorporate protamines after the removal of histones, and degenerate during the individualization stage of spermiogenesis. In contrast, in other SD/SD+ genotypes, protamine incorporation appears less disturbed, yet spermatid nuclei are abnormally compacted, and mature sperm nuclei are eventually released in the seminal vesicle. Our analyses of different SD+ chromosomes suggest that the severity of the spermiogenic defects associates with the copy number of the Rsp satellite. We propose that when Rsp copy number is very high (> 2000), spermatid nuclear compaction defects reach a threshold that triggers a checkpoint controlling sperm chromatin quality to eliminate abnormal spermatids during individualization.
format	article
author	Marion Herbette Xiaolu Wei Ching-Ho Chang Amanda M Larracuente Benjamin Loppin Raphaëlle Dubruille
author_facet	Marion Herbette Xiaolu Wei Ching-Ho Chang Amanda M Larracuente Benjamin Loppin Raphaëlle Dubruille
author_sort	Marion Herbette
title	Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.
title_short	Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.
title_full	Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.
title_fullStr	Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.
title_full_unstemmed	Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.
title_sort	distinct spermiogenic phenotypes underlie sperm elimination in the segregation distorter meiotic drive system.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/34761be6f8de43f3864747c2085ed363
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Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system.

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