4.8 Article

Rapid Shifts in Mitochondrial tRNA Import in a Plant Line; e with Extensive Mitochondrial tRNA Gene Loss

Journal

MOLECULAR BIOLOGY AND EVOLUTION
Volume 38, Issue 12, Pages 5735-5751

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/molbev/msab255

Keywords

tRNA import; tRNA-seq; mitochondrial tRNAs; plants; angiosperms

Funding

  1. NSF [MCB-2048407]
  2. Chateaubriand Fellowship from the Embassy of France in the United States
  3. NSF GAUSSI graduate research fellowship [DGE-1450032]
  4. Centre National de la Recherche Scientifique (CNRS)
  5. Initiative d'Excellence [MITOCROSS ANR-11-LABX-0057]

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Research on mitochondrial genomes of Silene plants reveals the process of tRNA gene loss and replacement, as well as the import of nuclear-encoded tRNAs. Even in systems with recent mitochondrial tRNA gene loss, nuclear-encoded counterparts may likely replace mitochondrial tRNAs, providing insight into the evolutionary history of plant mitochondrial genomes.
In most eukaryotes, transfer RNAs (tRNAs) are one of the very few classes of genes remaining in the mitochondrial genome, but some mitochondria have lost these vestiges of their prokaryotic ancestry. Sequencing of mitogenomes from the flowering plant genus Silene previously revealed a large range in tRNA gene content, suggesting rapid and ongoing gene loss/replacement. Here, we use this system to test longstanding hypotheses about how mitochondrial tRNA genes are replaced by importing nuclear-encoded tRNAs. We traced the evolutionary history of these gene loss events by sequencing mitochondrial genomes from key outgroups (Agrostemma githago and Silene [=Lychnis] chalcedonica). We then performed the first global sequencing of purified plant mitochondrial tRNA populations to characterize the expression of mitochondrial-encoded tRNAs and the identity of imported nuclear-encoded tRNAs. We also confirmed the utility of high-throughput sequencing methods for the detection of tRNA import by sequencing mitochondrial tRNA populations in a species (Solanum tuberosum) with known tRNA trafficking patterns. Mitochondrial tRNA sequencing in Silene revealed substantial shifts in the abundance of some nuclear-encoded tRNAs in conjunction with their recent history of mt-tRNA gene loss and surprising cases where tRNAs with anticodons still encoded in the mitochondrial genome also appeared to be imported. These data suggest that nuclear-encoded counterparts are likely replacing mitochondrial tRNAs even in systems with recent mitochondrial tRNA gene loss, and the redundant import of a nuclear-encoded tRNA may provide a mechanism for functional replacement between translation systems separated by billions of years of evolutionary divergence.

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