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In this study, we deleted the mitochondrial t6A37-modifying enzyme OSGEPL1 in HEK293T cells. OSGEPL1 is dispensable for cell viability. t6A37 hypomodification selectively stimulated N1-methyladenosine at A9 (m1A9) and N2-methylguanosine at G10 (m2G10) modifications and caused a substantial reduction in the aminoacylation of mitochondrial tRNAThr and tRNALys, resulting in impaired translation efficiency. Multiple types of amino acid misincorporation due to the misreading of near-cognate codons by t6A37-unmodified tRNAs were detected, indicating a triggered translational infidelity. Accordingly, the alterations in mitochondrial structure, function, and the activated mitochondrial unfolded protein response were observed. Mitochondrial function was efficiently restored by wild-type, but not by tRNA-binding-defective OSGEPL1. Lastly, in Osgepl1 deletion mice, disruption to mitochondrial translation was evident but resulted in no observable deficiency under physiological conditions in heart, which displays the highest Osgepl1 expression. Taken together, our data delineate the multifaceted roles of mitochondrial t6A37 modification in translation efficiency and quality control in mitochondria.<\/jats:p>","DOI":"10.1093\/nar\/gkae013","type":"journal-article","created":{"date-parts":[[2024,1,16]],"date-time":"2024-01-16T13:08:24Z","timestamp":1705410504000},"page":"3213-3233","source":"Crossref","is-referenced-by-count":20,"title":["Multifaceted roles of t6A biogenesis in efficiency and fidelity of mitochondrial gene expression"],"prefix":"10.1093","volume":"52","author":[{"given":"Yong","family":"Zhang","sequence":"first","affiliation":[{"name":"Key Laboratory of RNA Science and Engineering, State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences , 320 Yue Yang Road , Shanghai\u00a0200031, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7889-3089","authenticated-orcid":false,"given":"Jing-Bo","family":"Zhou","sequence":"additional","affiliation":[{"name":"Key Laboratory of RNA Science and Engineering, State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences , 320 Yue Yang Road , Shanghai\u00a0200031, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yue","family":"Yin","sequence":"additional","affiliation":[{"name":"National Facility for Protein Science in Shanghai, Shanghai Advanced Research Institute, Chinese Academy of Science , 333 Haike Road , Shanghai\u00a0201210, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"En-Duo","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of RNA Science and Engineering, State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences , 320 Yue Yang Road , Shanghai\u00a0200031, China"},{"name":"School of Life Science and Technology, ShanghaiTech University , 393 Middle Huaxia Road , Shanghai\u00a0201210,\u00a0 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3701-5965","authenticated-orcid":false,"given":"Xiao-Long","family":"Zhou","sequence":"additional","affiliation":[{"name":"Key Laboratory of RNA Science and Engineering, State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences , 320 Yue Yang Road , Shanghai\u00a0200031, China"},{"name":"Key Laboratory of Systems Health Science of Zhejiang Province, School of Life Science, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences , Hangzhou\u00a0 310024 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,1,16]]},"reference":[{"key":"2024041217033991900_B1","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1038\/s41580-021-00342-0","article-title":"The expanding world of tRNA modifications and their disease relevance","volume":"22","author":"Suzuki","year":"2021","journal-title":"Nat. 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