Organellar tRNAs in parasitic plant species

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.

真核生物核基因组通常编码不同组的蛋白质翻译机器（protein translation machinery），以分别在胞质溶胶与细胞器（线粒体及质体）中发挥功能。这一现象引发了若干问题：为何尽管多套翻译系统具备相似功能却仍被保留？它们的演化是否因所处亚细胞区室的不同而存在差异？这些问题在陆生植物中尤为引人关注，因为其翻译机器（包括氨酰-tRNA合成酶（aminoacyl-tRNA synthetases, aaRS））常被双重靶向至质体与线粒体。这两种细胞器的代谢特征差异显著，质体中的翻译速率远高于线粒体，以合成光合作用所需的大量快速周转蛋白。此前研究表明，与无质体的其他真核生物中线粒体aaRS相比，植物细胞器aaRS的演化速率更慢。因此，我们在广泛取样的被子植物中（包括质体基因表达速率降低的非光合（异养）植物物种），研究了核编码的细胞器及胞质翻译机器的演化，旨在验证以下假说：与光合作用相关的翻译需求会限制参与细胞器tRNA代谢的类细菌酶的演化。值得注意的是，尽管异养植物的线粒体与质体中仍存在翻译过程，但其大量细胞器靶向的aaRS及其他酶却发生了整体丢失。这些丢失常伴随胞质酶与tRNA向细胞器的明显重靶向——有时保留了aaRS-tRNA氨酰化关系，有时却导致胞质aaRS与线粒体tRNA底物间出现意外错配。我们的研究结果表明，光合质体的存在推动了细胞器tRNA代谢专用系统的保留。