In silico subcellular targeting predictions for cytosolic aminoacyl tRNA-synthetases (aaRS) in parasitic plants

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的蛋白质翻译机器，以分别在胞质溶胶与细胞器（线粒体和质体）中发挥功能。这一现象引发了诸多问题：为何即便多种翻译系统具备相似功能仍被保留？它们的演化是否会因所处区室的不同而存在差异？这些问题在陆生植物中尤为有趣，因为包括氨酰-tRNA合成酶（aminoacyl-tRNA synthetases，aaRS）在内的翻译机器常被双重靶向至质体和线粒体。这两种细胞器的代谢模式差异显著，质体的翻译速率远高于线粒体，以供应光合作用所需的大量快速周转蛋白。此前研究表明，与缺乏质体的其他真核生物中的线粒体aaRS相比，植物细胞器aaRS的演化更为缓慢。因此，我们对被子植物的广泛样本进行了核编码细胞器及胞质翻译机器的演化分析，其中包括质体基因表达速率降低的非光合型（异养型）植物物种，旨在验证以下假设：与光合作用相关的翻译需求限制了参与细胞器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和质体中仍存在翻译过程，但它们却出现了许多细胞器靶向aaRS及其他酶的整体性丢失。这些丢失现象常伴随胞质酶和tRNA向细胞器的明显重靶向，有时会保留aaRS-tRNA氨酰化关系，有时则会在胞质aaRS与线粒体tRNA底物之间产生意外的错配。我们的研究结果表明，光合型质体的存在推动了细胞器tRNA代谢特化系统的保留。