Does mitochondrial DNA evolution in metazoa drive the origin of new mitochondrial proteins?

Most eukaryotic cells contain mitochondria with a genome that evolved from their α-proteobacterial ancestor. In the course of eukaryotic evolution, the mitochondrial genome underwent a dramatic reduction in size, caused by the loss and translocation of genes. This required adjustments in mitochondrial gene expression mechanisms and resulted in a complex collaborative system of mitochondrially encoded transfer RNAs and ribosomal RNAs with nuclear encoded proteins to express the mitochondrial encoded oxidative phosphorylation (OXPHOS) proteins. In this review, we examine mitochondrial gene expression from an evolutionary point of view: to what extent can we correlate changes in the mitochondrial genome in the evolutionary lineage leading to human with the origin of new nuclear encoded proteins. We dated the evolutionary origin of mitochondrial proteins that interact with mitochondrial DNA or its RNA and/or protein products in a systematic manner and compared them with documented changes in the mitochondrial DNA. We find anecdotal but accumulating evidence that metazoan RNA-interacting proteins arose in conjunction with changes of the mitochondrial DNA. We find no substantial evidence for such compensatory evolution in new OXPHOS proteins, which appear to be constrained by the ability to form supercomplexes. © 2018 IUBMB Life, 70(12):1240-1250, 2018.