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.

中文翻译：

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对翻译机制的光合作用需求推动了植物细胞器中冗余 tRNA 代谢的保留


真核核基因组通常编码不同的翻译机制集，用于在胞质溶胶与细胞器（线粒体和质体）中发挥作用。这就提出了一个问题，即为什么即使多个翻译系统能够具有类似的功能，也要维护它们，以及它们是否会根据它们运行所在的隔间而有所不同。这些问题在植物中特别有趣，因为翻译机制，包括氨酰转移 RNA （tRNA） 合成酶 （aaRS），通常是对质体和线粒体的双重靶向。这些细胞器具有不同的功能，在质体中具有更高的翻译速率，以提供光合作用所需的丰富、快速周转的蛋白质。先前的研究表明，在缺乏质体的真核生物中，与线粒体 aaRS 相比，植物细胞器 aaRS 的进化速度更慢。因此，我们研究了核编码的细胞器和胞质 aaRS 和 tRNA 成熟酶在广泛的被子植物样本中的进化，包括质体基因表达降低的非光合（异养）植物物种，以检验与光合作用相关的翻译需求限制参与细胞器 tRNA 代谢的酶的进化的假设。值得注意的是，异养植物表现出许多细胞器靶向 aaRS 和其他酶的大量丢失，即使翻译仍然发生在它们的线粒体和质体中。这些丢失通常伴随着胞质酶和 tRNA 对细胞器的明显重新定位，有时保留 aaRS-tRNA 充电关系，但有时在胞质 aaRS 和线粒体 tRNA 底物之间产生令人惊讶的错配。 我们的研究结果表明，光合质体的存在推动了细胞器 tRNA 代谢的专门系统的保留。