The evolution of extremely diverged plastomes in Selaginellaceae (lycophyte) is driven by repeat patterns and the underlying DNA maintenance machinery

Abstract

Two factors are proposed to account for the unusual features of organellar genomes: the disruptions of organelle-targeted DNA replication, repair, and recombination (DNA-RRR) systems in the nuclear genome and repetitive elements in organellar genomes. Little is known about how these factors affect organellar genome evolution. The deep-branching vascular plant family Selaginellaceae is known to have a deficient DNA-RRR system and convergently evolved organellar genomes. However, we found that the plastid genome (plastome) of Selaginella sinensis has extremely accelerated substitution rates, a low GC content, pervasive repeat elements, a dynamic network structure, and it lacks direct or inverted repeats. Unexpectedly, its organelle DNA-RRR system is short of a plastid-targeted Recombinase A1 (RecA1) and a mitochondriontargeted RecA3, in line with other explored Selaginella species. The plastome contains a large collection of short-and medium-sized repeats. Given the absence of RecA1 surveillance, we propose that these repeats trigger illegitimate recombination, accelerated mutation rates, and structural instability. The correlations between repeat quantity and architectural complexity in the Selaginella plastomes support these conclusions. We, therefore, hypothesize that the interplay of the deficient DNA-RRR system and the high repeat content has led to the extraordinary divergence of the S. sinensis plastome. Our study not only sheds new light on the mechanism of plastome divergence by emphasizing the power of cytonuclear integration, but it also reconciles the longstanding contradiction on the effects of DNA-RRR system disruption on genome structure evolution.

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

“…Similar to the sanguinolenta group, the phylogenetic position of the sinensis group remains unclear. The reported plastome from the sinensis group exhibited extraordinary genomic and genetic features, even when compared to other Selaginella species (Xiang et al, 2022), established as the most basal group of Selaginellaceae with a long branch (Zhou et al, 2022). In contrast, its mitochondrial genome features were similar to those of other Selaginella species, and the phylogenetic position of the sinensis group based on the mitogenomes was located within the superclade C (Tang et al, 2023).…”

“…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.…”

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

“…Recently, more and more unconventional structural rearrangements of organelle genomes have been reported in Selaginellaceae (Tsuji et al, 2007; Hecht et al, 2011; Mower et al, 2019; Zhang et al, 2019a; Kang et al, 2020; Xiang et al, 2022). The plastomes in Selaginellaceae exhibit complicated genome architectures; the DR structure contains directly arranged ribosomal operons, the IR structure converts back from DR to IR, and the multipartite plastome with three ribosomal operon copies creates the alternative subgenomic conformation (Tsuji et al, 2007; Hecht et al, 2011; Mower et al, 2019; Zhang et al, 2019a; Kang et al, 2020) (Fig.…”

Phylogeny, character evolution, and classification of Selaginellaceae (lycophytes)

“…Plastome studies ( Tsuji et al., 2007 ; Smith, 2009 ; Wicke et al., 2011 ; Jansen and Ruhlman 2012 ; Ruhlman and Jansen 2018 ; Mower et al., 2019 ; Xu et al., 2018 ; Zhang et al., 2019a , Zhang et al., 2019b ; Kang et al., 2020 ; Xiang et al., 2022 ; Zhou et al., 2022 ) showed that plastomes of Selaginellaceae and their infrafamilial lineages known so far have a number of unique and diverse features: (a) plastomes of most plant lineages are highly conserved with quadripartite structure composed by a large single copy (LSC), a small single copy (SSC), and two inverted repeats (IRa and IRb), whereas plastomes of Selaginellaceae exhibit DR structure (also can be R, DR, IR, or DR-IR coexisting types) with small to medium repeats existed in SC, and plastome conformations ranged from one to 24 ( Zhou et al., 2022 ); (b) plastome sizes in most land plants are 120–160 kb but those in Selaginellaceae are 78–190 kb; (c) a plastome in other vascular plants usually contains approximately 120–130 genes but those of Selaginellaceae contain 36–128 genes; (d) accD/cemA/infA/psaM/rpl20/rpl21/rpl32/rpl33/rps12/rps15/rps16/ycf66/ycf94 and most of the rRNA, tRNA, and introns are generally lost or pseudogenetized in Selaginellaceae; (e) GC content in land plant plastomes ranges from 34% to 40%, but plastomes of Selaginellaceae often are extremely GC-rich (>50%); and (f) overall distinctions of plastomes among subgenera even among sections in Selaginella are much greater than those among orders/families/subfamilies/genera in other vascular plants.…”