Interchangeable parts: The evolutionarily dynamic tRNA population in plant mitochondria

Abstract

Transfer RNAs (tRNAs) remain one of the very few classes of genes still encoded in the mitochondrial genome. These key components of the protein translation system must interact with a large enzymatic network of nuclear-encoded gene products to maintain mitochondrial function. Plants have an evolutionarily dynamic mitochondrial tRNA population, including ongoing tRNA gene loss and replacement by both horizontal gene transfer from diverse sources and import of nuclear-expressed tRNAs from the cytosol. Thus, plant mitochondria represent an excellent model for understanding how anciently divergent genes can act as "interchangeable parts" during the evolution of complex molecular systems. In particular, understanding the integration of the mitochondrial translation system with elements of the corresponding machinery used in cytosolic protein synthesis is a key area for eukaryotic cellular evolution. Here, we review the increasingly detailed phylogenetic data about the evolutionary history of mitochondrial tRNA gene loss, transfer, and functional replacement that has created extreme variation in mitochondrial tRNA populations across plant species. We describe emerging tRNA-seq methods with promise for refining our understanding of the expression and subcellular localization of tRNAs. Finally, we summarize current evidence and identify open questions related to coevolutionary changes in nuclear-encoded enzymes that have accompanied turnover in mitochondrial tRNA populations.

Keywords: Enzyme/tRNA coevolution; Horizontal gene transfer; Mitochondrial tRNAs; Plant mitochondria; tRNA-seq.