The effects of rapid mitochondrial gene loss on organellar proteomes

Abstract

Mitochondrial genomes retain only a tiny number of genes from their bacterial progenitors, including key components of protein translation machinery. The set of mitochondrially encoded tRNAs and ribosomal subunits is highly variable across angiosperms, with many examples of mitochondrial gene loss, replacement, and/or transfer to the nucleus. This dynamic history suggests large-scale remodeling of mitochondrial translation machinery in some lineages, but such conclusions are largely inferred from genomic sequence and protein targeting predictions. Here, we use proteomic (LC-MS/MS) analysis of purified mitochondria and chloroplasts from angiosperm species with major differences in mitochondrial gene content (Arabidopsis thaliana and Silene conica). Our analysis largely confirms the current understanding of subcellular localization for nuclear-encoded proteins involved in tRNA metabolism and ribosome function in A. thaliana, although some aminoacyl-tRNA synthetases (aaRSs) may have more specialized subcellular roles than previously thought. In contrast, S. conica has undergone extensive mitochondrial gene loss and numerous associated changes in the composition of its mitochondrial proteome, including apparent retargeting of aaRSs, replacement of ribosomal subunits, and loss of the glutamine amidotransferase (GatCAB) complex. Overall, this analysis illustrates how the complex network of molecular interactions necessary for mitochondrial translation are perturbed by gene loss, transfer, and replacement. Significance StatementPlant mitochondrial genomes exhibit exceptional diversity in gene content across species due to ongoing processes of gene loss, transfer, and functional replacement. However, our understanding of the consequences of these genomic changes on the mitochondrial proteome remain limited. Here, we compare organellar (mitochondrial and chloroplast) proteomes across species of flowering plants, revealing a large-scale rewiring of mitochondrial protein synthesis machinery has coincided with loss of tRNA and ribosomal protein genes from the mitochondrial genome.