DeTar Rachael A, Chustecki Joanna M, Martinez-Hottovy Ana, Ceriotti Luis Federico, Broz Amanda K, Lou Xiaorui, Sanchez-Puerta M Virginia, Elowsky Christian, Christensen Alan C, Sloan Daniel B
Department of Biology, Colorado State University, Fort Collins, CO 80523.
School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE 68588.
Proc Natl Acad Sci U S A. 2024 Dec 24;121(52):e2421485121. doi: 10.1073/pnas.2421485121. Epub 2024 Dec 18.
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.
真核生物的核基因组通常编码不同的翻译机制，分别用于细胞质与细胞器（线粒体和质体）中的功能。这就引发了一些问题，即为什么即使多个翻译系统具有可比的功能，它们仍被保留下来，以及它们是否会根据其运作的区室而有不同的进化方式。这些问题在植物中尤其有趣，因为包括氨酰 - 转移RNA（tRNA）合成酶（aaRS）在内的翻译机制常常双靶向于质体和线粒体。这些细胞器具有不同的功能，质体中的翻译速率要高得多，以供应光合作用所需的大量快速周转的蛋白质。先前的研究表明，与缺乏质体的真核生物中的线粒体aaRS相比，植物细胞器aaRS的进化更为缓慢。因此，我们在广泛采样的被子植物中研究了核编码的细胞器和细胞质aaRS以及tRNA成熟酶的进化，包括质体基因表达减少的非光合（异养）植物物种，以检验与光合作用相关的翻译需求限制了参与细胞器tRNA代谢的酶的进化这一假设。值得注意的是，异养植物表现出许多靶向细胞器的aaRS和其他酶的全面丧失，尽管它们的线粒体和质体中仍发生翻译。这些丧失往往伴随着细胞质酶和tRNA明显重新靶向到细胞器，有时保留aaRS - tRNA的充电关系，但有时会在细胞质aaRS和线粒体tRNA底物之间产生惊人的错配。我们的研究结果表明，光合质体的存在驱动了细胞器tRNA代谢专门系统的保留。
