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.
Similar content being viewed by others
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.
References
Barbrook AC, Howe CJ, Kurniawan DP, Tarr SJ (2010) Organization and expression of organellar genomes. Philos Trans Roy Soc London B Biol Sci 365:785–797. https://doi.org/10.1098/rstb.2009.0250
Brenner WG, Mader M, Muller NA, Hoenicka H, Schroeder H, Zorn I, Fladung M, Kersten B (2019) High level of conservation of mitochondrial RNA editing sites among four populus species. Genes Genom Genet 9:709–717. https://doi.org/10.1534/g3.118.200763
Covello PS, Gray MW (1989) Rna editing in plant-mitochondria. Nature 341:662–666. https://doi.org/10.1038/341662a0
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190. https://doi.org/10.1101/gr.849004
Danecek P, McCarthy SA (2017) BCFtools/csq: haplotype-aware variant consequences. Bioinformatics 33:2037–2039. https://doi.org/10.1093/bioinformatics/btx100
Edera AA, Sanchez-Puerta MV (2021) Computational detection of plant RNA editing events. Meth Molec Biol 2181:13–34. https://doi.org/10.1007/978-1-0716-0787-9_2
Edera AA, Gandini CL, Sanchez-Puerta MV (2018) Towards a comprehensive picture of C-to-U RNA editing sites in angiosperm mitochondria. Pl Molec Biol 97:215–231. https://doi.org/10.1007/s11103-018-0734-9
Fang J, Jiang XH, Wang TF, Deng ZY, Zhang AD, Zhang XJ (2021a) Dynamic landscape of mitochondrial Cytidine-to-Uridine RNA editing in tobacco (Nicotiana tabacum) shows its tissue specificity. Pl Cell Tiss Org 148:363–376. https://doi.org/10.1007/s11240-021-02194-0
Fang J, Jiang XH, Wang TF, Zhang XJ, Zhang AD (2021b) Tissue-specificity of RNA editing in plant: analysis of transcripts from three tobacco (Nicotiana tabacum) varieties. Pl Biotechnol Rep 15:471–482. https://doi.org/10.1007/s11816-021-00692-3
Farre JC, Aknin C, Araya A, Castandet B (2012) RNA editing in mitochondrial trans-introns is required for splicing. PLoS ONE 7:e52644. https://doi.org/10.1371/journal.pone.0052644
Fauskee BD, Sigel EM, Pryer KM, Grusz AL (2021) Variation in frequency of plastid RNA editing within Adiantum implies rapid evolution in fern plastomes. Amer J Bot 108:820–827. https://doi.org/10.1002/ajb2.1649
Gerke P, Szovenyi P, Neubauer A, Lenz H, Gutmann B, McDowell R, Small I, Schallenberg-Rudinger M, Knoop V (2020) Towards a plant model for enigmatic U-to-C RNA editing: the organelle genomes, transcriptomes, editomes and candidate RNA editing factors in the hornwort Anthoceros agrestis. New Phytol 225:1974–1992. https://doi.org/10.1111/nph.16297
Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341:660–662. https://doi.org/10.1038/341660a0
Hoch B, Maier RM, Appel K, Igloi GL, Kossel H (1991) Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353:178–180. https://doi.org/10.1038/353178a0
Ichinose M, Sugita M (2017) RNA editing and its molecular mechanism in plant organelles. Genes (Basel) 8:5. https://doi.org/10.3390/genes8010005
Ichinose M, Sugita M (2021) Substitutional RNA editing in plant organelles. Meth Molec Biol 2181:1–12. https://doi.org/10.1007/978-1-0716-0787-9_1
Ishibashi K, Small I, Shikanai T (2019) Evolutionary model of plastidial RNA editing in angiosperms presumed from genome-wide analysis of Amborella trichopoda. Pl Cell Physiol 60:2141–2151. https://doi.org/10.1093/pcp/pcz111
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Meth 12:357–360. https://doi.org/10.1038/nmeth.3317
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molec Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lenz H, Knoop V (2013) PREPACT 2.0: Predicting C-to-U and U-to-C RNA Editing in organelle genome sequences with multiple references and curated RNA editing annotation. Bioinform Biol Insights 7:1–19. https://doi.org/10.4137/BBI.S11059
Lenz H, Hein A, Knoop V (2018) Plant organelle RNA editing and its specificity factors: enhancements of analyses and new database features in PREPACT 3.0. BMC Bioinf 19:255. https://doi.org/10.1186/s12859-018-2244-9
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome S, Genome Project Data Processing (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Lo Giudice C, Pesole G, Picardi E (2018) REDIdb 3.0: a comprehensive collection of RNA editing events in plant organellar genomes. Frontiers Pl Sci 9:482. https://doi.org/10.3389/fpls.2018.00482
Lo Giudice C, Hernandez I, Ceci LR, Pesole G, Picardi E (2019) RNA editing in plants: a comprehensive survey of bioinformatics tools and databases. Pl Physiol Biochem 137:53–61. https://doi.org/10.1016/j.plaphy.2019.02.001
Miyata Y, Sugita M (2004) Tissue- and stage-specific RNA editing of rps 14 transcripts in moss (Physcomitrella patens) chloroplasts. J Pl Physiol 161:113–115. https://doi.org/10.1078/0176-1617-01220
Mower JP, Palmer JD (2006) Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Molec Genet Genomics 276:285–293. https://doi.org/10.1007/s00438-006-0139-3
Oldenkott B, Burger M, Hein AC, Jorg A, Senkler J, Braun HP, Knoop V, Takenaka M, Schallenberg-Rudinger M (2020) One C-to-U RNA editing site and two independently evolved editing factors: testing reciprocal complementation with DYW-type PPR Proteins from the Moss Physcomitrium (Physcomitrella) patens and the Flowering Plants Macadamia integrifolia and Arabidopsis. Pl Cell 32:2997–3018. https://doi.org/10.1105/tpc.20.00311
Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7:e30619. https://doi.org/10.1371/journal.pone.0030619
Rodrigues NF, da Fonseca GC, Kulcheski FR, Margis R (2017) Salt stress affects mRNA editing in soybean chloroplasts. Genet Molec Biol 40:200–208. https://doi.org/10.1590/1678-4685-Gmb-2016-0055
Ruchika C, Okudaira MS, Tsukahara T (2021) Genome-wide identification of U-To-C RNA editing events for nuclear genes in Arabidopsis thaliana. Cells 10:635. https://doi.org/10.3390/cells10030635
Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM (2005) Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase alpha-subunit mRNA. Pl Cell 17:1815–1828. https://doi.org/10.1105/tpc.105.032474
Shikanai T (2015) RNA editing in plants: machinery and flexibility of site recognition. Bba-Bioenergetics 1847:779–785. https://doi.org/10.1016/j.bbabio.2014.12.010
Shtratnikova VY, Schelkunov MI, Penin AA, Logacheva MD (2020) Mitochondrial genome of the nonphotosynthetic mycoheterotrophic plant Hypopitys monotropa, its structure, gene expression and RNA editing. PeerJ 8:e9309. https://doi.org/10.7717/peerj.9309
Small ID, Schallenberg-Rudinger M, Takenaka M, Mireau H, Ostersetzer-Biran O (2020) Plant organellar RNA editing: what 30 years of research has revealed. Pl J 101:1040–1056. https://doi.org/10.1111/tpj.14578
Smith DR (2020) Unparalleled variation in RNA editing among Selaginella Plastomes. Pl Physiol 182:12–14. https://doi.org/10.1104/pp.19.00904
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Sun Y, Li X, Wu D, Pan Q, Ji Y, Ren H, Ding K (2016) RED: a Java-MySQL software for identifying and visualizing RNA editing sites using rule-based and statistical filters. PLoS ONE 11:e0150465. https://doi.org/10.1371/journal.pone.0150465
Takenaka M, Zehrmann A, Verbitskiy D, Hartel B, Brennicke A (2013) RNA editing in plants and its evolution. Annual Rev Genet 47:335–352. https://doi.org/10.1146/annurev-genet-111212-133519
Takenaka M, Zehrmann A, Verbitskiy D, Glass F, Brehme N, Brennicke A (2014) The world of RNA editing in mitochondria and chloroplasts in plants. Biocell 38:58–59
Tang W, Luo C (2018) Molecular and functional diversity of RNA editing in plant mitochondria. Molec Biotechnol 60:935–945. https://doi.org/10.1007/s12033-018-0126-z
Walkley CR, Li JB (2017) Rewriting the transcriptome: adenosine-to-inosine RNA editing by ADARs. Genome Biol 18:205. https://doi.org/10.1186/s13059-017-1347-3
Wang Z, Lian J, Li Q, Zhang P, Zhou Y, Zhan X, Zhang G (2016) RES-Scanner: a software package for genome-wide identification of RNA-editing sites. Gigascience 5:37. https://doi.org/10.1186/s13742-016-0143-4
Wu S, Liu W, Aljohi HA, Alromaih SA, Alanazi IO, Lin Q, Yu J, Hu S (2018) REDO: rna editing detection in plant organelles based on variant calling results. J Comput Biol 25:509–516. https://doi.org/10.1089/cmb.2017.0214
Xiong J, Tao T, Luo Z, Yan S, Liu Y, Yu X, Liu G, Xia H, Luo L (2017) RNA editing responses to oxidative stress between a wild abortive type male-sterile line and its maintainer line. Frontiers Pl Sci 8:2023. https://doi.org/10.3389/fpls.2017.02023
Xiong Y, Fang J, Jiang X, Wang T, Liu K, Peng H, Zhang X, Zhang A (2022) Genome-wide analysis of multiple Organellar RNA editing factor (MORF) Family in Kiwifruit (Actinidia chinensis) reveals its roles in chloroplast rna editing and pathogens stress. Plants (Basel) 11:146. https://doi.org/10.3390/plants11020146
Yagi Y, Tachikawa M, Noguchi H, Satoh S, Obokata J, Nakamura T (2013) Pentatricopeptide repeat proteins involved in plant organellar RNA editing. RNA Biol 10:1419–1425. https://doi.org/10.4161/rna.24908
Yan J, Zhang Q, Yin P (2018) RNA editing machinery in plant organelles. Sci China Life Sci 61:162–169. https://doi.org/10.1007/s11427-017-9170-3
Zahn LM (2017) The evolution of edited RNA transcripts. Science 355:1278–1279. https://doi.org/10.1126/science.355.6331.1278-d
Zhang F, Lu Y, Yan S, Xing Q, Tian W (2017) SPRINT: an SNP-free toolkit for identifying RNA editing sites. Bioinformatics 33:3538–3548. https://doi.org/10.1093/bioinformatics/btx473
Zhang A, Jiang X, Zhang F, Wang T, Zhang X (2020) Dynamic response of RNA editing to temperature in grape by RNA deep sequencing. Funct Integr Genomics 20:421–432. https://doi.org/10.1007/s10142-019-00727-7
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).
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Consent for publication
All authors have consented to publishing this work.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Julien Boutte.
Supplementary Information
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
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 aleuticum. c 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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-023-01849-z