Potential of Transcript Editing Across Mitogenomes of Early Land Plants Shows Novel and Familiar Trends

Abstract

RNA editing alters the identity of nucleotides in an RNA sequence so that the mature transcript differs from the template defined in the genome. This process has been observed in chloroplasts and mitochondria of both seed and early land plants. However, the frequency of RNA editing in plant mitochondria ranges from zero to thousands of editing sites. To date, analyses of RNA editing in mitochondria of early land plants have been conducted on a small number of genes or mitochondrial genomes of a single species. This study provides an overview of the mitogenomic RNA editing potential of the main lineages of these two groups of early land plants by predicting the RNA editing sites of 33 mitochondrial genes of 37 species of liverworts and mosses. For the purpose of the research, we newly assembled seven mitochondrial genomes of liverworts. The total number of liverwort genera with known complete mitogenome sequences has doubled and, as a result, the available complete mitogenome sequences now span almost all orders of liverworts. The RNA editing site predictions revealed that C-to-U RNA editing in liverworts and mosses is group-specific. This is especially evident in the case of liverwort lineages. The average level of C-to-U RNA editing appears to be over three times higher in liverworts than in mosses, while the C-to-U editing frequency of the majority of genes seems to be consistent for each gene across bryophytes.

Keywords: RNA editing; early land plants; liverwort; mitochondrial genome; moss.

Figure 1

Phylogenetic relationships of 37 species of liverworts and mosses based on 33 concatenated mitochondrial protein-coding sequences and predicted RNA editing sites. (A) Phylogenetic tree obtained as a result of Bayesian inference analysis of 33 concatenated protein-coding sequences of 37 species. All branches are maximally supported unless otherwise marked. The scale bar indicates the number of substitutions per nucleotide position. (B) Phylogenetic tree obtained as a result of maximum parsimony analysis of binary matrix of predicted C-to-U RNA editing site occurrence within the 33 aforementioned protein-coding sequences of 35 species. The support values are given at the nodes. Two columns in the middle of the graph depict the total number of C-to-U and U-to-C editing sites predicted within the aforementioned species sequences.

Figure 2

Predicted C-to-U editing frequency of liverwort genes. Bar plots depicting mean editing frequency of leafy (n = 8) and simple thalloid (n = 5) liverworts are colored by liverwort group. Genes are sorted in ascending order (left to right) of statistical significance of differences between editing frequencies. The significantly different (p-value < 0.05) editing frequencies are depicted on the left side of vertical dashed line. The bar plot whiskers depict standard error values.

Figure 3

Predicted C-to-U editing frequency of moss genes. Bar plots depicting mean editing frequency of orthotropic (n = 8) and plagiotropic (n = 6) mosses are colored by moss group. Genes are sorted in ascending order (left to right) of statistical significance of differences between editing frequencies. The significantly different (p-value < 0.05) editing frequencies are depicted on the left side of the vertical dashed line. The bar plot whiskers depict standard error values.

Figure 4

Mean C-to-U RNA editing frequency in genes of mosses and liverworts. The means of C-to-U RNA editing frequency of liverworts (orange line) and mosses (black line) are scaled.