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

Marion Herbette, Xiaolu Wei, Ching-Ho Chang, Amanda M Larracuente, Benjamin Loppin, and Raphaëlle Dubruille (2021)

PLoS Genet, 17(7):e1009662.

Segregation Distorter (SD) is a male meiotic drive system in Drosophilamelanogaster. Males heterozygous for a selfish SD chromosome rarely transmit thehomologous SD+ chromosome. It is well established that distortion results from aninteraction between Sd, the primary distorting locus on the SD chromosome and itstarget, a satellite DNA called Rsp, on the SD+ chromosome. However, the molecularand cellular mechanisms leading to post-meiotic SD+ sperm elimination remainunclear. Here we show that SD/SD+ males of different genotypes but with similarlystrong degrees of distortion have distinct spermiogenic phenotypes. In somegenotypes, SD+ spermatids fail to fully incorporate protamines after the removal ofhistones, and degenerate during the individualization stage of spermiogenesis. Incontrast, in other SD/SD+ genotypes, protamine incorporation appears less disturbed,yet spermatid nuclei are abnormally compacted, and mature sperm nuclei areeventually released in the seminal vesicle. Our analyses of different SD+chromosomes suggest that the severity of the spermiogenic defects associates withthe copy number of the Rsp satellite. We propose that when Rsp copy number is veryhigh (> 2000), spermatid nuclear compaction defects reach a threshold that triggersa checkpoint controlling sperm chromatin quality to eliminate abnormal spermatidsduring individualization.

 
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