Evolution of mitochondrial RNA editing in extant gymnosperms

Abstract

To unveil the evolution of mitochondrial RNA editing in gymnosperms, we characterized mitochondrial genomes (mitogenomes), plastid genomes, RNA editing sites, and pentatricopeptide repeat (PPR) proteins from 10 key taxa representing four of the five extant gymnosperm clades. The assembled mitogenomes vary in gene content due to massive gene losses in Gnetum and Conifer II clades. Mitochondrial gene expression levels also vary according to protein function, with the most highly expressed genes involved in the respiratory complex. We identified 9132 mitochondrial C-to-U editing sites, as well as 2846 P-class and 8530 PLS-class PPR proteins. Regains of editing sites were demonstrated in Conifer II rps3 transcripts whose corresponding mitogenomic sequences lack introns due to retroprocessing. Our analyses reveal that non-synonymous editing is efficient and results in more codons encoding hydrophobic amino acids. In contrast, synonymous editing, although performed with variable efficiency, can increase the number of U-ending codons that are preferentially utilized in gymnosperm mitochondria. The inferred loss-to-gain ratio of mitochondrial editing sites in gymnosperms is 2.1:1, of which losses of non-synonymous editing are mainly due to genomic C-to-T substitutions. However, such substitutions only explain a small fraction of synonymous editing site losses, indicating distinct evolutionary mechanisms. We show that gymnosperms have experienced multiple lineage-specific duplications in PLS-class PPR proteins. These duplications likely contribute to accumulated RNA editing sites, as a mechanistic correlation between RNA editing and PLS-class PPR proteins is statistically supported.

Characterization of RNA editing profiles in rice endosperm development

“…Studies have shown that RNA editing is functionally important by affecting amino acid biochemical properties [40–42]. In our study, among these 214 CDS- recoding sites, we find that 88 (41.12%) and 126 (58.88%) are located at the first and second codon positions, respectively.…”

“…Although, as known to all, CDS- synonymous editing events do not cause amino acid alterations, some of them, such as cob -1119, cob -564, and ccmFn -372, present relatively higher editing frequencies (Table S1), suggesting that synonymous RNA editing does play an important role in rice endosperm development. As previously reported, synonymous mutations created by RNA editing likely stabilize RNA molecules [62] and affect translation efficiency based on changing synonymous codon types [40].…”

Organellar-genome analyses from the lycophyte genus Isoetes L. show one of the highest frequencies of RNA editing in land plants

“…Among gymnosperms, edits in the plastome can vary from a complete absence in Welwitschia mirabilis Hook. f. (Fan et al, 2019) to 255 editing sites in Ginkgo biloba L (He et al, 2016), while the mitogenome range from 99 in W. mirabilis (Fan et al, 2019) to an impressive number of 1,240 sites in Dioon Lindl (Wu and Chaw, 2022). Notably, seed-free plants exhibit an even wider range of variation in RNA-editing sites.…”

Complete organelle genomes of Korean fir, Abies koreana and phylogenomics of the gymnosperm genus Abies using nuclear and cytoplasmic DNA sequence data

“…The sizes of the mitogenomes are also variable, ranging from 346.5 kb in G. biloba 21 to 11.69 Mb in L. sibirica 23 from Pinophyta and contain 29–41 protein-coding genes, 28–35 tRNA genes, and three rRNA genes. They show various features, including mitochondrial DNA of plastid (MIPTs) and nuclear (MINCs) origin, repeats, and RNA editing 19 , 22 , 28 , 29 .…”