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

Gerke, Philipp; Szövényi, Péter; Neubauer, Anna; Lenz, H; Gutmann, Bernard; McDowell, Rose; Small, Ian; Schallenberg‐Rüdinger, Mareike; Knoop, Volker

doi:10.1111/nph.16297

Cited by 64 publications

(74 citation statements)

References 93 publications

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“…Previous studies have shown that RNA editing sites can be verified by comparing genomic DNA sequences with cDNA sequences ( Wolf et al., 2004 ; Oldenkott et al., 2014 ), or can be predicted by comparing genomic DNA sequences with verified DNA or amino acid sequences among closely related species ( Lenz et al., 2018 ). Prediction of C-to-U RNA editing in coding regions is relatively reliable because most editing events tend to restore conserved codons ( Oldenkott et al., 2014 ; Lenz et al., 2018 ; Small et al., 2020 ; Gerke et al., 2020 ). In this study, we used Selaginella as a research model to test the effect of extreme plastid RNA editing on phylogenetic reconstruction.…”

Section: Introductionmentioning

confidence: 99%

Extreme plastid RNA editing may confound phylogenetic reconstruction: A case study of Selaginella (lycophytes)

2020

Plant Diversity

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Cytidine-to-uridine (C-to-U) RNA editing is common in coding regions of organellar genomes throughout land plants. In most cases RNA editing alters translated amino acids or creates new start codons, potentially confounds phylogenetic reconstructions. In this study, we used the spike moss genus Selaginella (lycophytes), which has the highest frequency of RNA editing, as a model to test the effects of extreme RNA editing on phylogenetic reconstruction. We predicted the C-to-U RNA editing sites in coding regions of 18 Selaginella plastomes, and reconstructed the phylogenetic relationships within Selaginella based on three data set pairs consisted of plastome or RNA-edited coding sequences, first and second codon positions, and translated amino acid sequences, respectively. We predicted between 400 and 3100 RNA editing sites of 18 Selaginella plastomes. The numbers of RNA editing sites in plastomes were highly correlated with the GC content of first and second codon positions, but not correlated with the GC content of plastomes as a whole. Contrast phylogenetic analyses showed that there were substantial differences (e.g., the placement of clade B in Selaginella ) between the phylogenies generated by the plastome and RNA-edited data sets. This empirical study provides evidence that extreme C-to-U RNA editing in the coding regions of organellar genomes alters the sequences used for phylogenetic reconstruction, and might even confound phylogenetic reconstruction. Therefore, RNA editing sites should be corrected when plastid or mitochondrial genes are used for phylogenetic studies, particularly in those lineages with abundant organellar RNA editing sites, such as hornworts, quillworts, spike mosses, and some seed plants.

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Section: Introductionmentioning

confidence: 99%

Extreme plastid RNA editing may confound phylogenetic reconstruction: A case study of Selaginella (lycophytes)

2020

Plant Diversity

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“…As a consequence, a sense codon can be converted into a more evolutionarily conserved one or a start/stop codon to a sense codon (Tillich et al, 2006). Organelles in A. agrestis feature high amounts of RNA editing with altogether more than 1100 sites of C-to-U and 1300 sites of U-to-C editing (Gerke et al, 2019).…”

Section: Rna Editingmentioning

confidence: 99%

“…PPR proteins are a group of RNA-binding proteins which play critical roles in post-transcriptional gene regulation in plant chloroplasts (Barkan & Small, 2014). Preliminary data suggest that the few land plant lineages capable of reverse editing have evolved special types of PPR proteins, providing strong candidates for future studies (Gerke et al, 2019;Gutmann et al, 2020). A. agrestis provides an exceptional system to study the poorly known mechanisms and the evolution of reverse editing in land plants.…”

Section: Rna Editingmentioning

confidence: 99%

“…This plant is small, easy to propagate, has a small genome size, and sexual reproduction is facilitated in the laboratory because the plants are monoicous (male and female reproductive organs are produced on the same individual) (Proskauer, 1948a,b; Szövényi et al ., 2015). Anthoceros agrestis has been adopted as a plant model by research groups around the world to study biological processes such as the evolution of circadian clocks (Linde et al ., 2017), microbial‐type terpene synthase biochemistry (Xiong et al ., 2018) and RNA editing (Gerke et al ., 2019).…”

Section: The Hornwort Model Species Anthoceros Agrestismentioning

confidence: 99%

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The hornworts: morphology, evolution and development

et al. 2020

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Extant land plants consist of two deeply divergent groups, tracheophytes and bryophytes, which shared a common ancestor some 500 million years ago. While information about vascular plants and the two of the three lineages of bryophytes, the mosses and liverworts, is steadily accumulating, the biology of hornworts remains poorly explored. Yet, as the sister group to liverworts and mosses, hornworts are critical in understanding the evolution of key land plant traits. Until recently, there was no hornwort model species amenable to systematic experimental investigation, which hampered detailed insight into the molecular biology and genetics of this unique group of land plants. The emerging hornwort model species, Anthoceros agrestis, is instrumental in our efforts to better understand not only hornwort biology but also fundamental questions of land plant evolution. To this end, here we provide an overview of hornwort biology and current research on the model plant A. agrestis to highlight its potential in answering key questions of land plant biology and evolution.

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“…RNA editing is a term denoting a type of post-transcriptional modi cation of a transcribed RNA such that it differs from the sequence predicted from the genomic DNA 1 . This process occurs in diverse forms across all kingdoms of life, including the deamination of adenosines to inosines (which are read as guanosines in the mRNA) by ADAR enzymes in animals 2 , the deamination of cytidines to uridines by APOBEC enzymes in animals 3 and by PPR-DYW proteins in plants 4 , and the unknown mechanism of uridine modi cation to cytidine in an as yet unelucidated pathway present in some groups of plants (hornworts, lycophytes and some ferns) 5,6 . Recently, several tools have been developed to perform single nucleotide editing of mRNA 7 .…”

Section: Introductionmentioning

confidence: 99%

A synthetic RNA editing factor edits its target site in chloroplasts and bacteria

Royan

Gutmann

Francs‐Small

et al. 2020

Preprint

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Targeted cytidine to uridine RNA editing is a widespread phenomenon throughout the land plant lineage. Members of the pentatricopeptide repeat (PPR) protein family act as the specificity factors in this process. These proteins consist of helix-turn-helix domains, each of which recognises a single RNA nucleotide following a well-elucidated code. A cytidine deaminase-like domain (present at the C-terminus of some PPR editing factors or provided in trans via protein-protein interactions) is the catalytic domain in the process. The huge expansion of the PPR superfamily in land plants provides the sequence variation required for design of novel consensus-based RNA-binding proteins. We used this approach to construct a synthetic RNA editing factor designed to target one of the two sites in the Arabidopsis chloroplast transcriptome naturally recognised by the RNA editing factor CHLOROPLAST BIOGENESIS 19 (CLB19). We show that this designed editing factor specifically recognises the target sequence in in vitro binding assays and can partially complement a clb19 mutant. The designed factor is specific for the target rpoA site and does not recognise or edit the other site recognised by CLB19 in the clpP1 transcript. We show that the designed editing factor can function equally specifically in the bacterium E. coli, and shows some activity even in the absence of the editing cofactors that are often required for natural editing factor activity in plants. This study serves as a successful pilot into the design and application of programmable RNA editing factors based on plant PPR proteins.

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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

Cited by 64 publications

References 93 publications

Extreme plastid RNA editing may confound phylogenetic reconstruction: A case study of Selaginella (lycophytes)

Extreme plastid RNA editing may confound phylogenetic reconstruction: A case study of Selaginella (lycophytes)

The hornworts: morphology, evolution and development

A synthetic RNA editing factor edits its target site in chloroplasts and bacteria

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