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

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.

The earliest allopolyploidization in tracheophytes revealed by phylotranscriptomics and morphology of Selaginellaceae

“…This position was suggested by plasome-based phylogeny when considering RNA editing events (Du et al, 2020) and the mitogenome-based phylogeny (Tang et al, 2023). There are pervasive RNA editing in the Selaginellaceae organelle genomes to restore the accelerated mutations caused by the improper DNA repair system (Kang et al, 2020, 2022; Zhang et al, 2020; Xiang et al, 2022). The consensus position of the pulvinata group, achieved by the plastome-based phylogeny considering RNA editing, the mitogenome-based phylogeny, and the large-scale nuclear phylogenies, demonstrate the power of integrating the evidence from different genomes and the deep understanding of the data.…”

Evolution of the Araliaceae family involved rapid diversification of the Asian Palmate group and Hydrocotyle specific mutational pressure

“…Hydrocotyle species, including the three species in this study, usually grow in places that are marshy, boggy, and wet, but can even survive under water [57][58][59] . Accelerated nucleotide substitution rates in some species or clades exhibiting distinct environments and growth habitats have been reported [60][61][62] , and associated www.nature.com/scientificreports/ mutation rates among the plastome, mitogenome, and nuclear genome were discussed in previous studies 56,[63][64][65][66] .…”

“…Mutational pressure and gene conversion affect the nucleotide landscape of the genome, and these two factors are known as non-adaptive mechanisms 52 . Owing to the influence of AT-biased mutational pressure in non-coding regions, the majority of land plants have AT-rich plastomes 53 ; conversely, genic regions appear to be under GC-biased mutational pressure, referred to as GC-biased gene conversion [52][53][54][55][56] . The Araliaceae species in this study have AT-rich plastomes with a GC content of approximately 38%, suggesting that the Araliaceae plastomes are under AT-biased mutational pressure similar to other land plant plastomes.…”

“…3), implying that accelerated substitution rates occurred at least in plastome and nrDNA. The accelerated substitution rates in the three genome compartments may have been influenced by generation time, plant height, the replication mechanism of organelle genomes, and an improper organelle DNA repair system 56,[60][61][62][63][64][65][66] . Therefore, we speculate that the accelerated substitution rate in the Hydrocotyle genus occurred not only in their plastome but also in their mitogenome and nuclear genomes as a consequence of their evolutionary history and environmental adaptation.…”