PacBio full-length transcriptome analysis reveals the role of tRNA-like structures in RNA processing

• Published in: Cellular signalling 2025-01, Vol.125, p.111515, Article 111515
• Main Authors: Hu, Yanping, Yan, Shuangyong, Yan, Haohao, Su, Jingping, Cui, Zhongqiu, Li, Junling, Wang, Shengjun, Sun, Yue, Li, Wenjing, Gao, Shan
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - metabolism; DNA, Mitochondrial - genetics; DNA, Mitochondrial - metabolism; Gene Expression Profiling; Inverted repeat; Mitochondria - genetics; Mitochondria - metabolism; Nucleic Acid Conformation; polyA-like site; RNA Processing, Post-Transcriptional; RNA, Mitochondrial - genetics; RNA, Mitochondrial - metabolism; RNA, Plant - genetics; RNA, Plant - metabolism; RNA, Transfer - genetics; RNA, Transfer - metabolism; TIS; Transcriptome; tRNA-like site; TTS
• ISSN: 0898-6568; 1873-3913; 1873-3913
• DOI: 10.1016/j.cellsig.2024.111515

Mitochondrial DNA (mtDNA) and chloroplast DNA (cpDNA) are distinct from nuclear DNA (nuDNA) in a eukaryotic cell. Animal mitochondria transcribe a single primary transcript that carries all genes from a DNA strand; In contrast, plant mitochondria and chloroplasts produce multiple primary transcripts, with each transcript carrying several genes. How primary transcripts of plant mtDNA and cpDNA are processed into mature RNAs is still unknown. In the present study, we employed PacBio's full-length transcriptome data to characterize the transcription of Arabidopsis thaliana mtDNA, providing a more comprehensive and precise understanding. The primary findings included 20 novel mitochondrial (mt) RNAs of A. thaliana, transcripts carrying single introns or exons, long mt and chloroplast (cp) tRNAs with intricate secondary structures, and the role of tRNA-like structures in RNA processing. The gene of No. 20 novel mt RNA and its paralog on chromosome 2 of A. thaliana were assigned locus IDs ATMG01335 and AT2G07811. According to our upgraded “mitochondrial cleavage” model, tRNA-like structures serve as “punctuation” marks for RNA processing, akin to the role of tRNAs. Both tRNA-like structures and tRNAs collaborate for RNA processing in plant mitochondria and chloroplasts. •tRNA-like Structures play a crucial role in RNA processing, similar to tRNAs.•Both tRNA-like structures and tRNAs collaborate for RNA processing in plant mitochondria and chloroplasts.•The role in RNA processing is an ancient function of tRNAs or their evolutionary precursors, existing prior to the endosymbiotic events.•The gene for a novel mt RNA and its paralog on chromosome 2 of A. thaliana were assigned locus IDs ATMG01335 and AT2G07811, respectively.