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Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians

During embryonic development in mammals, the testicles generally descend into the scrotum, making the testicular temperature 2–4 °C lower than the core temperature via heat exchange and clearance, and thus more beneficial for normal spermatogenesis. Failure to descend, known as cryptorchidism, carri...

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Autores principales: Ding, Xiaoyue, Cao, Li, Zheng, Yu, Zhou, Xu, He, Xiaofang, Xu, Shixia, Ren, Wenhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8620446/
https://www.ncbi.nlm.nih.gov/pubmed/34828386
http://dx.doi.org/10.3390/genes12111780
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author Ding, Xiaoyue
Cao, Li
Zheng, Yu
Zhou, Xu
He, Xiaofang
Xu, Shixia
Ren, Wenhua
author_facet Ding, Xiaoyue
Cao, Li
Zheng, Yu
Zhou, Xu
He, Xiaofang
Xu, Shixia
Ren, Wenhua
author_sort Ding, Xiaoyue
collection PubMed
description During embryonic development in mammals, the testicles generally descend into the scrotum, making the testicular temperature 2–4 °C lower than the core temperature via heat exchange and clearance, and thus more beneficial for normal spermatogenesis. Failure to descend, known as cryptorchidism, carries a series of risks such as infertility and testicular cancer. However, some mammals have evolved abdominal testes while maintaining healthy reproduction. To explore the underlying molecular mechanism, we conducted comparative genomic analyses and functional assays on the spermatogenesis-related ubiquitin–proteasome system (UPS) genes essential to sperm formation in representative laurasiatherians. Here, positive selection and rapid evolution of spermatogenesis-related UPS genes were identified in the abdominal testicular laurasiatherians. Moreover, potential convergent amino acids were found between distantly related species with similar abdominal testicles and functional analyses showed RNF8 (V437I) in abdominal testicular species (437I) has a stronger ubiquitination ability, which suggests that the mammals with abdominal testes might exhibit enhanced sperm cell histone clearance to maintain sperm formation. This evidence implies that, in response to “cryptorchidism injury”, spermatogenesis-related UPS genes in the abdominal testicular species might have undergone adaptive evolution to stabilize sperm formation. Thus, our study could provide some novel insights into the reproductive adaptation in abdominal testicular mammals.
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spelling pubmed-86204462021-11-27 Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians Ding, Xiaoyue Cao, Li Zheng, Yu Zhou, Xu He, Xiaofang Xu, Shixia Ren, Wenhua Genes (Basel) Article During embryonic development in mammals, the testicles generally descend into the scrotum, making the testicular temperature 2–4 °C lower than the core temperature via heat exchange and clearance, and thus more beneficial for normal spermatogenesis. Failure to descend, known as cryptorchidism, carries a series of risks such as infertility and testicular cancer. However, some mammals have evolved abdominal testes while maintaining healthy reproduction. To explore the underlying molecular mechanism, we conducted comparative genomic analyses and functional assays on the spermatogenesis-related ubiquitin–proteasome system (UPS) genes essential to sperm formation in representative laurasiatherians. Here, positive selection and rapid evolution of spermatogenesis-related UPS genes were identified in the abdominal testicular laurasiatherians. Moreover, potential convergent amino acids were found between distantly related species with similar abdominal testicles and functional analyses showed RNF8 (V437I) in abdominal testicular species (437I) has a stronger ubiquitination ability, which suggests that the mammals with abdominal testes might exhibit enhanced sperm cell histone clearance to maintain sperm formation. This evidence implies that, in response to “cryptorchidism injury”, spermatogenesis-related UPS genes in the abdominal testicular species might have undergone adaptive evolution to stabilize sperm formation. Thus, our study could provide some novel insights into the reproductive adaptation in abdominal testicular mammals. MDPI 2021-11-10 /pmc/articles/PMC8620446/ /pubmed/34828386 http://dx.doi.org/10.3390/genes12111780 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Ding, Xiaoyue
Cao, Li
Zheng, Yu
Zhou, Xu
He, Xiaofang
Xu, Shixia
Ren, Wenhua
Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians
title Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians
title_full Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians
title_fullStr Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians
title_full_unstemmed Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians
title_short Insights into the Evolution of Spermatogenesis-Related Ubiquitin–Proteasome System Genes in Abdominal Testicular Laurasiatherians
title_sort insights into the evolution of spermatogenesis-related ubiquitin–proteasome system genes in abdominal testicular laurasiatherians
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8620446/
https://www.ncbi.nlm.nih.gov/pubmed/34828386
http://dx.doi.org/10.3390/genes12111780
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