Chloroplast C-to-U RNA editing in vascular plants is adaptive due to its restorative effect: testing the restorative hypothesis

Abstract

The adaptiveness of nonsynonymous RNA editing (recoding) could be conferred by the flexibility of the temporal-spatially controllable proteomic diversity, or by its restorative effect which fixes unfavorable genomic mutations at the RNA level. These two complementary hypotheses, namely, the diversifying hypothesis and the restorative hypothesis, have distinct predictions on the landscape of RNA editing sites. We collected the chloroplast C-to-U RNA editomes of 21 vascular plants (11 angiosperms, four gymnosperms, and six ferns) from a previous study, aiming to testify whether the plant editomes typically conform to the restorative hypothesis. All predictions made by the restorative hypothesis are verified: (i) nonsynonymous editing sites are more frequent and have higher editing levels than synonymous sites; (ii) nonsynonymous editing levels are extremely high and show weak tissue-specificity in plants; (iii) on the inferred genomic sites with recent T-to-C mutations, nonsynonymous sites but not synonymous sites are compensated by C-to-U RNA editing. In conclusion, nonsynonymous C-to-U RNA editing in plants is adaptive due to its restorative effects. The recoding levels are high and are constantly required across the whole plant so that the recoding events could perfectly mimic DNA mutations. The evolutionary significance of plant RNA editing is systematically demonstrated at the genome-wide level.

The occurrence, characteristics, and adaptation of A-to-I RNA editing in bacteria: A review

“…As previously stated, the final effect may be an A to G reverse mutation, but the entire process does not improve the organism’s adaptation ( Jiang and Zhang, 2019 ). Additionally, a recent study found that nonsynonymous C-to-U RNA editing is adaptive due to its restorative effects in plants ( Duan et al, 2023 ). On the other hand, some researchers believe that editing is adaptive because it has been discovered that even restored editing events are less prone to mutation than other A sites, which implies that it is evolutionarily deliberate to keep these events rather than reverting to their original state ( Liu et al, 2017 ; Shoshan et al, 2021 ).…”

Adaptation of A-to-I RNA editing in bacteria, fungi, and animals

“…ancestral DNA, then it is apparent that the editing mechanism still increases the fitness of the uneditable allele ( Figure 1D ). Under this scenario, this action/process of restorative RNA editing is adaptive (Duan et al, 2023 ).…”

“…On the other hand, the restorative hypothesis requires the ancestral sequence of editing sites to be the post-edited version and that the editing level should be high. Restorative RNA editing typically takes place in plants (Duan et al, 2023 ) and whether it exists in animals is still under debate (Jiang and Zhang, 2019 ; Shoshan et al, 2021 ).…”

Retrospect of the Two-Year Debate: What Fuels the Evolution of SARS-CoV-2: RNA Editing or Replication Error?

“…In contrast, when replication errors (or SNPs) in SARS-CoV-2 are excluded, the remaining SNVs (if any) should belong to RNA editing events. A typical SNV profile of RNA editing should significantly skew to a particular type of mutation, such as A-to-G or C-to-T [ 11 – 13 ]. Amazingly, even with a symmetric SNV profile in hand, the Di Giorgio et al paper concluded that what they found were RNA editing events.…”