Convergent Evolution of Fern-Specific Mitochondrial Group II Intron atp1i361g2 and Its Ancient Source Paralogue rps3i249g2 and Independent Losses of Intron and RNA Editing among Pteridaceae

Abstract

Mitochondrial intron patterns are highly divergent between the major land plant clades. An intron in the atp1 gene, atp1i361g2, is an example for a group II intron specific to monilophytes (ferns). Here, we report that atp1i361g2 is lost independently at least 4 times in the fern family Pteridaceae. Such plant organelle intron losses have previously been found to be accompanied by loss of RNA editing sites in the flanking exon regions as a consequence of genomic recombination of mature cDNA. Instead, we now observe that RNA editing events in both directions of pyrimidine exchange (C-to-U and U-to-C) are retained in atp1 exons after loss of the intron in Pteris argyraea/biaurita and in Actiniopteris and Onychium. We find that atp1i361g2 has significant similarity with intron rps3i249g2 present in lycophytes and gymnosperms, which we now also find highly conserved in ferns. We conclude that atp1i361g2 may have originated from the more ancestral rps3i249g2 paralogue by a reverse splicing copy event early in the evolution of monilophytes. Secondary structure elements of the two introns, most characteristically their domains III, show strikingly convergent evolution in the monilophytes. Moreover, the intron paralogue rps3i249g2 reveals relaxed evolution in taxa where the atp1i361g2 paralogue is lost. Our findings may reflect convergent evolution of the two related mitochondrial introns exerted by co-evolution with an intron-binding protein simultaneously acting on the two paralogues.

Towards a plant model for enigmatic U‐to‐C RNA editing: the organelle genomes, transcriptomes, editomes and candidate RNA editing factors in the hornwort Anthoceros agrestis

“…Comparing plant lifestyles gives no reasonable clues as to why some plant lineages (like the Selaginellales) have lost reverse RNA editing altogether, may have never possessed it in the first place (possibly mosses and liverworts, depending on the ultimately true phylogeny of the bryophyte clades), or why U-to-C editing may even dominate over C-to-U editing in other lineages . Based on the working hypotheses presented here, the experimental approaches outlined herein will hopefully help to answer that puzzling evolutionary question or, for example, also why RNA editing evolves so dramatically fast in at least some genera, like Amaranthus or Silene among the angiosperms (Sloan et al, 2010;Hein et al, 2019), Selaginella among the lycophytes (Smith, 2019), Adiantum among ferns (Zumkeller et al, 2016), or, as also demonstrated here for U-to-C editing, in Anthoceros among the hornworts.…”

Comparative Analysis of Four Calypogeia Species Revealed Unexpected Change in Evolutionarily-Stable Liverwort Mitogenomes

“…As a result, introns are removed, but editing sites remain [ 10 , 18 ]. The loss of introns without concurrent loss of flanking editing sites has recently been reported in ferns [ 62 ]. Edited sites from the intron-missing genes of Calypogeia may also not be removed because they are crucial for the excision of the remaining introns [ 10 ].…”

The complete mitochondrial genome of Taxus cuspidata (Taxaceae): eight protein-coding genes have transferred to the nuclear genome

“…This discrepancy could be caused by a partially processed cDNA undergoing conversion with the native intron-bearing gene. As a result, although introns are removed, some RNA editing sites still remain [71]. Another possibility is that the full-length cDNA molecules have partially recombined with the native gene.…”