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Towards a comprehensive picture of C-to-U RNA editing sites in angiosperm mitochondria

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Abstract

Key message

Our understanding of the dynamic and evolution of RNA editing in angiosperms is in part limited by the few editing sites identified to date. This study identified 10,217 editing sites from 17 diverse angiosperms. Our analyses confirmed the universality of certain features of RNA editing, and offer new evidence behind the loss of editing sites in angiosperms.

Abstract

RNA editing is a post-transcriptional process that substitutes cytidines (C) for uridines (U) in organellar transcripts of angiosperms. These substitutions mostly take place in mitochondrial messenger RNAs at specific positions called editing sites. By means of publicly available RNA-seq data, this study identified 10,217 editing sites in mitochondrial protein-coding genes of 17 diverse angiosperms. Even though other types of mismatches were also identified, we did not find evidence of non-canonical editing processes. The results showed an uneven distribution of editing sites among species, genes, and codon positions. The analyses revealed that editing sites were conserved across angiosperms but there were some species-specific sites. Non-synonymous editing sites were particularly highly conserved (~ 80%) across the plant species and were efficiently edited (80% editing extent). In contrast, editing sites at third codon positions were poorly conserved (~ 30%) and only partially edited (~ 40% editing extent). We found that the loss of editing sites along angiosperm evolution is mainly occurring by replacing editing sites with thymidines, instead of a degradation of the editing recognition motif around editing sites. Consecutive and highly conserved editing sites had been replaced by thymidines as result of retroprocessing, by which edited transcripts are reverse transcribed to cDNA and then integrated into the genome by homologous recombination. This phenomenon was more pronounced in eudicots, and in the gene cox1. These results suggest that retroprocessing is a widespread driving force underlying the loss of editing sites in angiosperm mitochondria.

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Notes

  1. https://www.ncbi.nlm.nih.gov/genome/organelle.

  2. https://www.ncbi.nlm.nih.gov/sra.

  3. Data harvested January 2018.

  4. https://github.com/genome/bam-readcount.

  5. http://broadinstitute.github.io/picard.

  6. http://www.evolution.rdg.ac.uk/BayesTraitsV3.0.1/BayesTraitsV3.0.1.html.

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Acknowledgements

This work was funded by the National Scientific and Technical Research Council (CONICET) in Argentina.

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Authors and Affiliations

  1. IBAM, Facultad de Ciencias Agrarias, CONICET, Universidad Nacional de Cuyo, M5528AHB, Chacras de Coria, Argentina

    Alejandro A. Edera, Carolina L. Gandini & M. Virginia Sanchez-Puerta

  2. Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, 5500, Mendoza, Argentina

    M. Virginia Sanchez-Puerta

Authors
  1. Alejandro A. Edera
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  2. Carolina L. Gandini
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  3. M. Virginia Sanchez-Puerta
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Contributions

MVSP and AAE conceived and designed the experiments. AAE and CLG designed the editing site annotation pipeline. AAE implemented computational scripts, and performed the experiments. CLG performed experiments of ancestral state reconstruction. MVSP and AAE analyzed the data. AAE prepared figures and supplementary materials. AAE, MVSP, and CLG wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Alejandro A. Edera.

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11103_2018_734_MOESM3_ESM.gz

ESM3: CDS sequences used for identifying all the editing sites, and nucleotide alignments of the 24 protein-coding genes that were conserved across the 17 angiosperm mitochondrial genomes. Gaps indicate sites with <10 reads, and uppercase C nucleotides depict editing sites. (GZ 200 KB)

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Edera, A.A., Gandini, C.L. & Sanchez-Puerta, M.V. Towards a comprehensive picture of C-to-U RNA editing sites in angiosperm mitochondria. Plant Mol Biol 97, 215–231 (2018). https://doi.org/10.1007/s11103-018-0734-9

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  • DOI: https://doi.org/10.1007/s11103-018-0734-9

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