J Syst Evol ›› 2023, Vol. 61 ›› Issue (5): 890-905.DOI: 10.1111/jse.12927

• Research Articles • Previous Articles     Next Articles

The associated evolution among the extensive RNA editing, GC-biased mutation, and PPR family expansion in the organelle genomes of Selaginellaceae

Jong-Soo Kang1, Jigao Yu1,2, Xian-Chun Zhang1, and Qiao-Ping Xiang1*   

  1. 1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China;
    2 University of Chinese Academy of Sciences, Beijing 100049, China
    *Author or correspondence. E-mail:qpxiang@ibcas.ac.cn
  • Received:2022-07-22 Accepted:2022-10-28 Online:2022-11-03 Published:2023-09-01

Abstract: Extensive C-to-U editing has been reported from plastid genomes (plastomes) and mitochondrial genomes (mitogenomes) of spikemoss. While “reverse” U-to-C editing was recorded in other seed-free plants such as hornworts, quillworts, and ferns, it was not observed in spikemosses. However, no comprehensive study on the association between RNA editing and other genomic features was conducted for the organelle genomes of spikemosses. Here, we report thousands of C-to-U editing sites from plastomes and mitogenomes of two species: 1767 and 2394 edits in Selaginella remotifolia, and 4091 and 2786 edits in Selaginella nipponica, respectively. Comparative analyses revealed two different editing frequencies among plastomes, but one similar frequency in mitogenomes. The different editing frequency in the Selaginella organelle genomes is related to the nonsynonymous substitution rate and the genome structural complexity. The high guanine and cytosine (GC) content caused by GC-biased mutations in organelle genomes might be related to the absence of U-to-C editing in Selaginellaceae. Using RNA-seq and whole-genome data, we screened the pentatricopeptide repeat (PPR) family and discovered that the number of aspartic acid-tyrosine-tryptophan (DYW) domain-containing PPR proteins corresponded roughly to the editing abundance in the Selaginella organelle genomes. Consequently, we hypothesize that associated evolution among RNA editing, GC-biased mutation in organelle genomes, and the PPR protein family encoded in the nuclear genome, is probably triggered by the aberrant DNA repair system in Selaginellaceae. Our study provides new insights into the association between organelle and nuclear genomes in Selaginellaceae, which would contribute to understanding the evolution of post-transcriptional modifications of organelle genomes in land plants.

Key words: GC-biased mutation, mitochondrial genome (mitogenome), pentatricopeptide repeat (PPR) protein, plastid genome (plastome), RNA editing, Selaginellaceae