Photosynthetic demands on translational machinery drive retention of redundant tRNA metabolism in plant organelles

• 成果类型: Article
• 署名作者: 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.
• 署名单位: Colorado State University System; Colorado State University Fort Collins; University of Nebraska System; University of Nebraska Lincoln; University Nacional Cuyo Mendoza; Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET); University Nacional Cuyo Mendoza; University of Nebraska System; University of Nebraska Lincoln
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9026
• DOI: 10.1073/pnas.2421485121
• 发表日期: 2024-12-24
• 关键词: protein import; plastid genomes; gene-transfer; mitochondrial; arabidopsis; EVOLUTION; synthetases; chloroplast; expression; biology

摘要

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 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.