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Diversity of RNA editing in chloroplast transcripts across three main plant clades

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Abstract

RNA editing is a post-transcriptional modification of an RNA nucleotide sequence. Until now, different RNA editing systems were found in the major eukaryotic clades. In the plant kingdom, RNA editing was mainly documented in the mitochondria and chloroplast genomes. However, variation among large taxonomic groups and the evolutionary trajectory in terms of intra- and inter-clades remains unclear. To gain a better understanding of RNA editing evolution, in this study, based on publicly available RNA-seq data across three clades (fern, gymnosperm, and angiosperm), we provided a detailed analysis of chloroplast RNA editing events and discussed its evolution in land plants. A total of 5203 editing sites were determined across 21 species after rigorous screening. We found that the clustering relations of RNA editing sites across 21 species agreed with the phylogenetic tree based on protein sequences approximately, and more editing sites occurred in early diverging lineages for all three clades, implying they shared similar evolutionary trajectories of editing loss. We observed that the average RNA editing level varied among species as well as genes, a lowest RNA editing level (~ 0.42) was detected in Selaginella moellendorffii; the highest editing level (~ 0.88) was detected in the atpA gene. The reduction of cytosine content with evolution detected in our study further suggested that the substitution of the genomic sequence was the significant driver of loss of editing for later-branching plants. Many of the identified sites in our study have not been previously reported and provided a valuable data set for the future research community. Our findings also provide valuable information for the evolution of RNA editing in plants.

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Data Availability and Material

The datasets analyzed during the current study are available in the NCBI repository (https://www.ncbi.nlm.nih.gov/) and are available as Online Resource 1–6 associated with this manuscript.

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Acknowledgements

We would like to thank the members of Bioinformatics Group of Wuhan Botanical Garden, Chinese Academy of Sciences, China, for the discussion and suggestion to improve the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, Grant Numbers 32070682, the National Science & Technology Innovation Zone Project, grant numbers 1716315XJ00200303 and 1816315XJ00100216, CAS Pioneer Hundred Talents Program, and the Key Research and Development Program of Hubei Province (2022BBA0076).

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Authors

Contributions

ADZ and XJZ designed the experiments. ADZ and JF performed statistical analyses of gene expression data. ADZ performed statistical analyses. ADZ drafted the manuscript. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Xiujun Zhang.

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Supplementary Information

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Information on Electronic Supplementary Material

Online Resource 1. SRA accessions and chloroplast genome for each plant used in the study.

Online Resource 2. The statistical result of RNA editing sites in 21 species.

Online Resource 3. Information of identified RNA editing sites by REDO.

Online Resource 4. Editing sites in 30 genes with most editing sites across 21 species.

Online Resource 5. Cytosines content of shared 50 genes across 21 plants.

Online Resource 6. a Average read depth of RNA-seq data across 21 species used in our study. b The attributes of RNA editing sites in chloroplast illustrated by samples of Adiantum aleuticumc Hierarchical cluster analysis of numbers of RNA editing sites in chloroplast across 21 species. d Hierarchical cluster analysis of numbers of RNA editing sites in chloroplast across 11 angiosperms. e Hierarchical cluster analysis of numbers of RNA editing sites in chloroplast across 6 fern plants. f Hierarchical cluster analysis of numbers of RNA editing sites in chloroplast across 4 gymnosperm plants.

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Zhang, A., Fang, J. & Zhang, X. Diversity of RNA editing in chloroplast transcripts across three main plant clades. Plant Syst Evol 309, 12 (2023). https://doi.org/10.1007/s00606-023-01849-z

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  • DOI: https://doi.org/10.1007/s00606-023-01849-z

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