Comparative genomics among gymnosperms suggested extensive loss of mitochondrial RNA editing sites from Welwitschia mirabilis based on predictive analysis. However, empirical or transcriptome data to confirm this massive loss event are lacking, and the potential mechanisms of RNA site loss are unclear. By comparing genomic sequences with transcriptomic and reverse-transcription PCR sequencing data, we performed a comprehensive analysis of the pattern of RNA editing in the mitochondrial and plastid genomes (mitogenome and plastome, respectively) of W. mirabilis and a second gymnosperm, Ginkgo biloba. For W. mirabilis, we found only 99 editing sites located in 13 protein-coding genes in the mitogenome and a complete loss of RNA editing from the plastome. The few genes having high editing frequency in the Welwitschia mitogenome showed a strong negative correlation with gene expression level. Comparative analyses with G. biloba, containing 1,405 mitochondrial and 345 plastid editing sites, revealed that the editing loss from W. mirabilis is mainly due to the substitution of editable cytidines to thymidines at the genomic level, which could be caused by retroprocessing. Our result is the first study to uncover massive editing loss from both the mitogenome and plastome in a single genus. Furthermore, our results suggest that gene expression level and retroprocessing both contributed to the evolution of RNA editing in plant organellar genomes.
Keywords: RNA editing; Welwitschia; expression levels; massive loss; organelle genomes.