Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
Abstract Background Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. However, they have been lost in the evolutionary lineages leading to vertebrates and arthropods, raising the...
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doaj-2bce1b13b16a4feebb093fe59f02ea6b2020-11-24T22:25:27ZengBMCBMC Developmental Biology1471-213X2017-07-0117111110.1186/s12861-017-0151-3Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogasterSina Saari0Ana Andjelković1Geovana S. Garcia2Howard T. Jacobs3Marcos T. Oliveira4Institute of Biosciences and Medical Technology, Tampere University Hospital, University of TampereInstitute of Biosciences and Medical Technology, Tampere University Hospital, University of TampereDepartamento de Tecnologia, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista “Júlio de Mesquita Filho”Institute of Biosciences and Medical Technology, Tampere University Hospital, University of TampereInstitute of Biosciences and Medical Technology, Tampere University Hospital, University of TampereAbstract Background Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. However, they have been lost in the evolutionary lineages leading to vertebrates and arthropods, raising the question as to what survival or reproductive disadvantages they confer. Recent interest in using them in therapy lends a biomedical dimension to this question. Methods Here, we examined the impact of the expression of Ciona intestinalis alternative oxidase, AOX, on the reproductive success of Drosophila melanogaster males. Sperm-competition assays were performed between flies carrying three copies of a ubiquitously expressed AOX construct, driven by the α-tubulin promoter, and wild-type males of the same genetic background. Results In sperm-competition assays, AOX conferred a substantial disadvantage, associated with decreased production of mature sperm. Sperm differentiation appeared to proceed until the last stages, but was spatially deranged, with spermatozoids retained in the testis instead of being released to the seminal vesicle. High AOX expression was detected in the outermost cell-layer of the testis sheath, which we hypothesize may disrupt a signal required for sperm maturation. Conclusions AOX expression in Drosophila thus has effects that are deleterious to male reproductive function. Our results imply that AOX therapy must be developed with caution.http://link.springer.com/article/10.1186/s12861-017-0151-3MitochondriaRespiratory chainSpermatogenesisSperm competition |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Sina Saari Ana Andjelković Geovana S. Garcia Howard T. Jacobs Marcos T. Oliveira |
spellingShingle |
Sina Saari Ana Andjelković Geovana S. Garcia Howard T. Jacobs Marcos T. Oliveira Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster BMC Developmental Biology Mitochondria Respiratory chain Spermatogenesis Sperm competition |
author_facet |
Sina Saari Ana Andjelković Geovana S. Garcia Howard T. Jacobs Marcos T. Oliveira |
author_sort |
Sina Saari |
title |
Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster |
title_short |
Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster |
title_full |
Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster |
title_fullStr |
Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster |
title_full_unstemmed |
Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster |
title_sort |
expression of ciona intestinalis aox causes male reproductive defects in drosophila melanogaster |
publisher |
BMC |
series |
BMC Developmental Biology |
issn |
1471-213X |
publishDate |
2017-07-01 |
description |
Abstract Background Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. However, they have been lost in the evolutionary lineages leading to vertebrates and arthropods, raising the question as to what survival or reproductive disadvantages they confer. Recent interest in using them in therapy lends a biomedical dimension to this question. Methods Here, we examined the impact of the expression of Ciona intestinalis alternative oxidase, AOX, on the reproductive success of Drosophila melanogaster males. Sperm-competition assays were performed between flies carrying three copies of a ubiquitously expressed AOX construct, driven by the α-tubulin promoter, and wild-type males of the same genetic background. Results In sperm-competition assays, AOX conferred a substantial disadvantage, associated with decreased production of mature sperm. Sperm differentiation appeared to proceed until the last stages, but was spatially deranged, with spermatozoids retained in the testis instead of being released to the seminal vesicle. High AOX expression was detected in the outermost cell-layer of the testis sheath, which we hypothesize may disrupt a signal required for sperm maturation. Conclusions AOX expression in Drosophila thus has effects that are deleterious to male reproductive function. Our results imply that AOX therapy must be developed with caution. |
topic |
Mitochondria Respiratory chain Spermatogenesis Sperm competition |
url |
http://link.springer.com/article/10.1186/s12861-017-0151-3 |
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