Cytonuclear Coadaptation in Drosophila: Disruption of Cytochrome C Oxidase Activity in Backcross Genotypes

Abstract

The cytochrome c oxidase enzyme (COX) is comprised of 10 nuclear-encoded subunits and three mitochondrial-encoded subunits in close physical association in the inner mitochondrial membrane. COX passes electrons from cytochrome c to molecular oxygen and pumps protons into the inner mitochondrial space for ATP production. Selection on nuclear-mitochondrial interactions within species should lead to coadaptation of the proteins comprising this important enzyme. Under this model, there should be relatively little disruption of COX activity when mitochondrial genomes are crossed among strains within species. A more pronounced disruption of activity is expected when the mitochondrial genome is expressed in the nuclear background of a different species. We test these hypotheses in Drosophila using hybridization and backcrossing among lines of D. simulans and D. mauritiana. Disrupted cytonuclear genotypes were constructed using backcrosses between two lines of D. simulans (siI and siII) that introduced each divergent mitochondrial DNA (mtDNA) into each nuclear background due to maternal inheritance of mtDNA. Similar crosses were used to introduce each D. simulans mtDNA into the D. mauritiana maI nuclear background. Reconstituted cytonuclear control genotypes were constructed by backcrossing the initial F1 females to males of the maternal genotype. COX enzyme activities were compared among these disrupted and reconstituted backcross genotypes within and between species. The disruption effect on COX activity was restricted to males of interspecific genotypes. These data support the coadaptation hypothesis and are consistent with predictions that the evolution of modifiers of male mitochondrial dysfunction is hindered by the maternal inheritance of mtDNA. New sequence data for nuclear encoded subunits of COX identified amino acids that may play a role in the disruption effect.

Mitonuclear interactions: evolutionary consequences over multiple biological scales

“…This specific incompatibility decreases the activity of mETS complexes I, II and IV, compromises bristle formation, delays development and decreases fecundity [90]. A similar decline in OXPHOS capacity was previously documented in backcrosses of D. simulans and Drosophila mauritiana [91], and decreased fertility, fecundity and offspring viability, ultimately leading to hybrid breakdown in parasitoid wasps [92][93][94], and extensive mitonuclear epistatic interaction in the fruit fly [95].…”

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

“…Nuclear-mitochondrial coadaptation: The coadaptation hypothesis predicts that disrupted mitonuclear genotypes (e.g., Dmel nuclear chromosomes with Dsim mtDNA) should have reduced performance, and there is compelling evidence for this in a variety of systems (Edmands and Burton 1999;Rawson and Burton 2002;McKenzie et al 2003;Sackton et al 2003). It might follow that such genotypes would have reduced longevity due to disrupted OXPHOS functions, possibly resulting in elevated ROS production.…”

Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule

“…In angiosperms, hybrid male sterility is thought to result frequently from negative epistatic interactions between cytoplasmic (most probably mitochondrial) and nuclear genes in interspecific hybrids (Frank 1989;Schnable and Wise 1998). Negative cytonuclear interactions are also known to contribute to reproductive isolation between animal species and even populations, where they have been identified as the genetic basis of both hybrid inviability and infertility ½e.g., Tigriopus (Willett and Burton 2001;Harrison and Burton 2006) and Drosophila (Rand et al 2001;Sackton et al 2003). Assuming uniparental inheritance of the relevant organelle, cytonuclear interactions involve interactions between a cytoplasmic genome from one parent (usually maternal, Grun 1976) and the genes in the hybrid nuclear genome derived from the second parent.…”