Variation in frequency of plastid RNA editing within <i>Adiantum</i> implies rapid evolution in fern plastomes

Fauskee, Blake D.; Sigel, Erin M.; Pryer, Kathleen M.; Grusz, Amanda L.

doi:10.1002/ajb2.1649

Cited by 9 publications

(11 citation statements)

References 46 publications

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“…We became interested in the taxon given the apparently dynamic evolution of mitochondrial introns and RNA editing 22 . Likewise, a striking diversity of chloroplast RNA editing has been reported in the genus Adiantum 41 .…”

Section: Resultsmentioning

confidence: 96%

Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis

2023

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Plant mitochondrial genomes can be complex owing to highly recombinant structures, lack of gene syntenies, heavy RNA editing and invasion of chloroplast, nuclear or even foreign DNA by horizontal gene transfer (HGT). Leptosporangiate ferns remained the last major plant clade without an assembled mitogenome, likely owing to a demanding combination of the above. We here present both organelle genomes now for Haplopteris ensiformis. More than 1,400 events of C-to-U RNA editing and over 500 events of reverse U-to-C edits affect its organelle transcriptomes. The Haplopteris mtDNA is gene-rich, lacking only the ccm gene suite present in ancestral land plant mitogenomes, but is highly unorthodox, indicating extraordinary recombinogenic activity. Although eleven group II introns known in disrupted trans-splicing states in seed plants exist in conventional cis-arrangements, a particularly complex structure is found for the mitochondrial rrnL gene, which is split into two parts needing reassembly on RNA level by a trans-splicing group I intron. Aside from ca. 80 chloroplast DNA inserts that complicated the mitogenome assembly, the Haplopteris mtDNA features as an idiosyncrasy 30 variably degenerated protein coding regions from Rickettiales bacteria indicative of heavy bacterial HGT on top of tRNA genes of chlamydial origin.

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Section: Resultsmentioning

confidence: 96%

Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis

2023

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“…The frequency of RNA editing sites varies from zero to hundreds across the plant kingdom, among land plants (Takenaka, Zehrmann et al 2013, Smith 2020). The unparalleled variation in RNA editing among fern plastomes was demonstrated in several recent studies (Smith 2020, Fauskee, Sigel et al 2021). Yet, variation in the frequency and editing level among gymnosperms and angiosperms remains unclear.…”

Section: Introductionmentioning

confidence: 85%

Diversity of RNA Editing in Chloroplast Transcripts across Three Main Plant Clades

Zhang

Fang

Zhang

2022

Preprint

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RNA editing is a post-transcriptional modification of an RNA nucleotide sequence. Until now, different RNA editing systems were found in the major eukaryotic clades. In the plant kingdom, RNA editing was mainly documented in the mitochondria and chloroplast genomes. However, variation among large taxonomic groups and the evolutionary trajectory in terms of intra- and inter- clades remains unclear. To gain a better understanding of RNA editing evolution, in this study, based on publicly available RNA-seq data across three clades (fern, gymnosperm, and angiosperm), we provided a detailed analysis of chloroplast RNA editing events and discussed its evolution in land plants. A total of 5,205 editing sites were determined across 21 species after rigorous screening. We found that the clustering relations of RNA editing sites across 21 species agreed with the phylogenetic tree based on protein sequences approximately, and more editing sites occurred in early-diverging lineages for all the three clades, implying they shared similar evolutionary trajectories of editing loss. We observed that the average RNA editing level varied among species as well as genes, a lowest RNA editing level (~0.42) was detected in Selaginella moellendorffii; the highest editing level (~0.88) was detected in atpA gene. The reduction of cytosine content with evolution detected in our study further suggested that the substitution of the genomic sequence was the significant driver of loss of editing for later-branching plants. Many of the identified sites in our study have not been previously reported and provided a valuable data set for the future research community. Our findings also provide valuable information for the evolution of RNA editing in plants.

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“…We became particularly interested in the taxon given the apparently dynamic evolution of mitochondrial introns and RNA editing 22 . Likewise, a striking diversity of chloroplast RNA editing has been reported in the genus Adiantum 40 .…”

Section: A First Leptosporangiate Fern Mitogenome Assemblymentioning

confidence: 96%

Rickettsial DNA invasions and a scrambled rRNA cluster with a trans-splicing group I intron: The highly unorthodox mitogenome of the fern Haplopteris ensiformis

Zumkeller

Polsakiewicz

Knoop

2022

Preprint

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Plant mitochondrial genomes can be complex owing to highly recombinant structures, lack of gene syntenies, heavy RNA editing and invasion of chloroplast, nuclear or even foreign DNA by horizontal gene transfer (HGT). Leptosporangiate ferns remained the last major plant clade without an assembled mitogenome, likely owing to a demanding combination of the above. We here present both organelle genomes of Haplopteris ensiformis as a first leptosporangiate fern. More than 1,400 events of C-to-U RNA editing and over 500 events of reverse U-to-C edits affect its organelle transcriptomes. The Haplopteris mitogenome has a rich gene complement lacking only the ccm gene suite but is highly unorthodox, indicating extraordinary recombinogenic activity. Although eleven group II introns known in disrupted trans-splicing states in seed plants exist in conventional cis-arrangements, a particularly complex structure is found for the mitochondrial rrnL gene, which is split into two parts needing reassembly on RNA level by a novel trans-splicing group I intron. Finally, and aside from ca. 80 chloroplast DNA inserts that complicated the mitogenome assembly, the Haplopteris mtDNA features as an unparalleled idiosyncrasy 30 variably degenerated protein coding regions from Rickettiales bacteria indicative of heavy bacterial HGT on top of tRNA genes of chlamydial origin.

show abstract

Variation in frequency of plastid RNA editing within Adiantum implies rapid evolution in fern plastomes

Cited by 9 publications

References 46 publications

Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis

Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis

Diversity of RNA Editing in Chloroplast Transcripts across Three Main Plant Clades

Rickettsial DNA invasions and a scrambled rRNA cluster with a trans-splicing group I intron: The highly unorthodox mitogenome of the fern Haplopteris ensiformis

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