Distinctive evolutionary pattern of organelle genomes linked to the nuclear genome in Selaginellaceae

Abstract

Plastids and mitochondria are endosymbiotic organelles that store genetic information. The genomes of these organelles generally exhibit contrasting patterns regarding genome architecture and genetic content. However, they have similar genetic features in Selaginellaceae, and little is known about what causes parallel evolution. Here, we document the multipartite plastid genomes (plastomes) and the highly divergent mitochondrial genomes (mitogenomes) from spikemoss obtained by combining short-and long-reads. The 188-kb multipartite plastome has three ribosomal operon copies in the master genomic conformation, creating the alternative subgenomic conformation composed of 110-and 78-kb subgenomes. The long-read data indicated that the two different genomic conformations were present in almost equal proportions in the plastomes of Selaginella nipponica. The mitogenome of S. nipponica was assembled into 27 contigs with a total size of 110 kb. All contigs contained directly arranged repeats at both ends, which introduced multiple conformations. Our results showed that plastomes and mitogenomes share high tRNA losses, GC-biased nucleotides, elevated substitution rates and complicated organization. The exploration of nuclear-encoded organelle DNA replication, recombination and repair proteins indicated that, several single-targeted proteins, particularly plastid-targeted recombinase A1, have been lost in Selaginellaceae; conversely, the dualtargeted proteins remain intact. According to the reported function of recombinase A1, we propose that the plastomes of spikemoss often fail to pair homologous sequences during recombination, and the dual-targeted proteins play a key role in the convergent genetic features of plastomes and mitogenomes. Our results provide a distinctive evolutionary pattern of the organelle genomes in Selaginellaceae and evidence of their convergent evolution.

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

“…So far, two hypotheses have been proposed: one is that disruptions to the nuclear-encoded, organelle-targeted DNA replication, recombination, and repair (DNA-RRR) systems are responsible for the unusual organellar genome evolution; the other is that the number of repetitive elements is positively associated with aberrant organellar genomes. DNA-RRR genes have been regarded as key players in organellar genome evolution (Kang et al, 2020;Weng et al, 2014). This opinion is stimulated mainly by the experiment results using mutants of model organisms (e.g., Arabidopsis and Physcomitrella) and bacteria addressing functions of RecA homologous and other genes of the DNA-RRR system (Cerutti et al, 1992;Cox, 2013;Odahara et al, 2009Odahara et al, , 2015Rowan et al, 2010;Shedge et al, 2007).…”

“…This opinion is stimulated mainly by the experiment results using mutants of model organisms (e.g., Arabidopsis and Physcomitrella) and bacteria addressing functions of RecA homologous and other genes of the DNA-RRR system (Cerutti et al, 1992;Cox, 2013;Odahara et al, 2009Odahara et al, , 2015Rowan et al, 2010;Shedge et al, 2007). Kang et al (2020) reported a deficient DNA-RRR system in wild vascular plants and revealed the convergent evolution of plastome and mitochondrion genome (mitogenome) in Selaginellaceae caused solely by intact, dual-targeted recombinase gene. In studies on bacterial endosymbionts, it was reported that a deficient DNA-RRR system sometimes co-occurred with gene-order conservation (Garcia-Gonzalez et al, 2013;Tamas et al, 2002), or a highly dynamic architecture (Sloan & Moran, 2013).…”

“…In addition to unusual genome organization, the mitogenomes have extremely high GC contents (63-68%), genome-wide C-to-U RNA editing, elevated substitution rates, and no detectable tRNA genes, paralleling some of the trends observed in the plastomes of Selaginella. Kang et al (2020) revealed that the DNA-RRR system of Selaginella organellar genomes encoded by the nuclear genome was deficient. For example, the plastid-targeted RecA1 and mitochondrion-targeted RecA3 are absent, and only dual-targeted RecA2 exists in the Selaginellaceae.…”

Integrative taxonomy of the Selaginella helvetica group based on morphological, molecular and ecological data

“…. Kang & al. (2020) illustrated the potential evolutionary mechanism leading to the unusual architecture and genetic content of chloroplast genomes within several Selaginella plants, which indicated that using chloroplast markers solely in the analysis of Selaginella could be problematic.…”

“…Selaginella pallidissima together with S. helvetica and a few similar species formed a monophyletic group in all molecular phylogenetic studies (Zhou & al., 2015b;Weststrand & Korall, 2016a). However, species delimitation within this group remained unclear, due to insufficient taxonomic sampling and inapplicability of molecular markers from the chloroplast genome, which was revealed to have high GC-biased nucleotide composition, elevated substitution rates, and complicated organization (Kang & al., 2020;. In previous studies, different individuals of the same species of this group clustered in various positions in the phylogeny due to incorrect identification or low differentiation of the markers (Zhou & al., 2015b;Weststrand & Korall, 2016a).…”