Evolutionary rate analysis of aminoacyl tRNA synthetases

Eukaryotic nuclear genomes often encode distinct sets of protein
translation machinery for function in the cytosol vs. organelles
(mitochondria and plastids). This phenomenon 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 land plants because translation machinery, including
aminoacyl-tRNA synthetases (aaRS), is often dual-targeted to both the
plastids and mitochondria. These two organelles have quite different
metabolisms, 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 other eukaryotes that lack
plastids. Thus, we investigated the evolution of nuclear-encoded
organellar and cytosolic translation machinery across a broad sampling of
angiosperms, including non-photosynthetic (heterotrophic) plant species
with reduced rates of plastid gene expression to test the hypothesis that
translational demands associated with photosynthesis constrain the
evolution of bacterial-like 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.