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...

Full description

Bibliographic Details
Main Authors: Sina Saari, Ana Andjelković, Geovana S. Garcia, Howard T. Jacobs, Marcos T. Oliveira
Format: Article
Language:English
Published: BMC 2017-07-01
Series:BMC Developmental Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12861-017-0151-3
id doaj-2bce1b13b16a4feebb093fe59f02ea6b
record_format Article
spelling 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
work_keys_str_mv AT sinasaari expressionofcionaintestinalisaoxcausesmalereproductivedefectsindrosophilamelanogaster
AT anaandjelkovic expressionofcionaintestinalisaoxcausesmalereproductivedefectsindrosophilamelanogaster
AT geovanasgarcia expressionofcionaintestinalisaoxcausesmalereproductivedefectsindrosophilamelanogaster
AT howardtjacobs expressionofcionaintestinalisaoxcausesmalereproductivedefectsindrosophilamelanogaster
AT marcostoliveira expressionofcionaintestinalisaoxcausesmalereproductivedefectsindrosophilamelanogaster
_version_ 1725757619313836032