A mitochondrial DNA hypomorph of cytochrome oxidase specifically impairs male fertility in Drosophila melanogaster.

Maulik R Patel,Harmit S Malik,Yukiko M Yamashita,Leo J Pallanck,Ganesh K Miriyala,Aimee J Littleton,Kien Trinh,Heiko Yang,Janet M Young,Scott R Kennedy

doi:10.7554/elife.16923

Abstract

Due to their strict maternal inheritance in most animals and plants, mitochondrial genomes are predicted to accumulate mutations that are beneficial or neutral in females but harmful in males. Although a few male-harming mtDNA mutations have been identified, consistent with this 'Mother's Curse', their effect on females has been largely unexplored. Here, we identify COII(G177S), a mtDNA hypomorph of cytochrome oxidase II, which specifically impairs male fertility due to defects in sperm development and function without impairing other male or female functions. COII(G177S) represents one of the clearest examples of a 'male-harming' mtDNA mutation in animals and suggest that the hypomorphic mtDNA mutations like COII(G177S) might specifically impair male gametogenesis. Intriguingly, some D. melanogaster nuclear genetic backgrounds can fully rescue COII(G177S) -associated sterility, consistent with previously proposed models that nuclear genomes can regulate the phenotypic manifestation of mtDNA mutations.

Highlights

The acquisition of the mitochondria by the ancestral eukaryote is one of the most remarkable instances of symbiosis in biology (Sagan, 1967; Schwartz and Dayhoff, 1978)
Continuous replacement of a large fraction of the nuclear genome every generation via crosses to external males practically eliminates the likelihood of evolution of nuclear suppressors during the course of the experiment
Our analyses revealed an approximately 20% decrease in C oxidase (COX) enzymatic activity in COIIG177S mutants grown at 29 ̊C in both male and female flies (Figure 5B)

Summary

Introduction

The acquisition of the mitochondria by the ancestral eukaryote is one of the most remarkable instances of symbiosis in biology (Sagan, 1967; Schwartz and Dayhoff, 1978). This symbiosis gave the eukaryotic cell the ability to perform oxidative phosphorylation (Williams et al, 2013). Despite the appearance of a symbiotic relationship, the evolutionary interests of mitochondria can be in conflict with those of nuclear genomes (Partridge and Hurst, 1998). This conflict arises from the differences in transmission between the two genomes. There are elaborate mechanisms to prevent the inheritance of sperm mitochondria

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Conclusion