Abstract
BackgroundMitochondrial 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.MethodsHere, 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.ResultsIn 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.ConclusionsAOX expression in Drosophila thus has effects that are deleterious to male reproductive function. Our results imply that AOX therapy must be developed with caution.
Highlights
Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them
Males expressing alternative oxidase (AOX) are defective in sperm-competition assays In Drosophila, as in many species, females typically mate with a succession of males, storing sperm inside the female body to fertilize oocytes as they mature [14]
We demonstrate that transgenic AOX expression in Drosophila under the α-tubulin promoter does cause a clear detriment to male reproductive success, using a stringent sperm-competition assay
Summary
Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. 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. When the AOX gene from the tunicate Ciona intestinalis (Ascidiacea) was expressed in cultured human cells, it promoted resistance to inhibitors of complexes III and IV [4] and compensated for the growth defects and oxidant-sensitivity of complex IV-deficient cell-lines [5]. It conferred resistance to otherwise lethal levels of complexes III and IV inhibitors [6], mitigated locomotor defects in the dj-1β Parkinson’s disease model [6] and
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