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Plant mitochondrial genomes (mitogenomes) experience remarkable levels of horizontal gene transfer, including the recent discovery that orchids anciently acquired DNA from fungal mitogenomes. Thus far, however, there is no evidence that any of the genes from this interkingdom horizontal gene transfer are functional in orchid mitogenomes. Here, we applied a specialized sequencing approach to the orchid Corallorhiza maculata and found that some fungal-derived tRNA genes in the transferred region are transcribed, post-transcriptionally modified, and aminoacylated. In contrast, all the transferred protein-coding sequences appear to be pseudogenes. These findings show that fungal horizontal gene transfer has altered the composition of the orchid mitochondrial tRNA pool and suggest that these foreign tRNAs function in translation. The exceptional capacity of tRNAs for horizontal gene transfer and functional replacement is further illustrated by the diversity of tRNA genes in the C. maculata mitogenome, which also include genes of plastid and bacterial origin in addition to their native mitochondrial counterparts. 

Eukaryotic nuclear genomes often encode distinct sets of translation machinery for function in the cytosol vs. organelles (mitochondria and plastids). This raises questions about why multiple translation systems are maintained even though they are capable of comparable functions and whether they evolve differently depending on the compartment where they operate. These questions are particularly interesting in plants because translation machinery, including aminoacyl-transfer RNA (tRNA) synthetases (aaRS), is often dual-targeted to the plastids and mitochondria. These organelles have different functions, with much higher rates of translation in plastids to supply the abundant, rapid-turnover proteins required for photosynthesis. Previous studies have indicated that plant organellar aaRS evolve more slowly compared to mitochondrial aaRS in eukaryotes that lack plastids. Thus, we investigated the evolution of nuclear-encoded organellar and cytosolic aaRS and tRNA maturation enzymes across a broad sampling of angiosperms, including nonphotosynthetic (heterotrophic) plant species with reduced plastid gene expression, to test the hypothesis that translational demands associated with photosynthesis constrain the evolution of enzymes involved in organellar tRNA metabolism. Remarkably, heterotrophic plants exhibited wholesale loss of many organelle-targeted aaRS and other enzymes, even though translation still occurs in their mitochondria and plastids. These losses were often accompanied by apparent retargeting of cytosolic enzymes and tRNAs to the organelles, sometimes preserving aaRS–tRNA charging relationships but other times creating surprising mismatches between cytosolic aaRS and mitochondrial tRNA substrates. Our findings indicate that the presence of a photosynthetic plastid drives the retention of specialized systems for organellar tRNA metabolism.