Selective Homo- and Heteromer Interactions between the Multiple Organellar RNA Editing Factor (MORF) Proteins in Arabidopsis thaliana

Zehrmann, Anja; Härtel, Barbara; Glass, Franziska; Bayer-Császár, Eszter; Obata, Toshihiro; Meyer, Etienne H.; Brennicke, Axel; Takenaka, Mizuki

doi:10.1074/jbc.m114.602086

Cited by 56 publications

(55 citation statements)

References 40 publications

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“…Disruption of single-polypeptide RNA editing factors like in the moss Physcomitrella (Schallenberg-R€ udinger & may have occurred independently or may be yet another synapomorphy of the HT clade. We found no evidence in A. agrestis, however, for additional, non-PPR 'helper' components identified in angiosperms, such as MORFs/RIPs indicative of more complex editosomes (Bentolila et al, 2012;Takenaka et al, 2012;Zehrmann et al, 2015;Bayer-Cs asz ar et al, 2017;Haag et al, 2017).…”

Section: New Phytologistcontrasting

confidence: 79%

“…However, the setup of organelle RNA editing is evidently more complex in flowering plants, where truncated proteins require interactions with DYW domains supplied in trans, frequently mediated by extra helper proteins (e.g. NUWA and multiple organellar RNA editing factor (MORF)/RNA-editing factor interacting protein (RIP) proteins) in much more complex editosomes (Takenaka et al, 2012;Bentolila et al, 2012;Boussardon et al, 2012;Sun et al, 2013Sun et al, , 2015Sun et al, , 2016Zehrmann et al, 2015;Diaz et al, 2017;Bayer-Cs asz ar et al, 2017;Andr es-Col as et al, 2017;Guillaumot et al, 2017;Sandoval et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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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

et al. 2019

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Summary Hornworts are crucial to understand the phylogeny of early land plants. The emergence of ‘reverse’ U‐to‐C RNA editing accompanying the widespread C‐to‐U RNA editing in plant chloroplasts and mitochondria may be a molecular synapomorphy of a hornwort–tracheophyte clade. C‐to‐U RNA editing is well understood after identification of many editing factors in models like Arabidopsis thaliana and Physcomitrella patens, but there is no plant model yet to investigate U‐to‐C RNA editing. The hornwort Anthoceros agrestis is now emerging as such a model system. We report on the assembly and analyses of the A. agrestis chloroplast and mitochondrial genomes, their transcriptomes and editomes, and a large nuclear gene family encoding pentatricopeptide repeat (PPR) proteins likely acting as RNA editing factors. Both organelles in A. agrestis feature high amounts of RNA editing, with altogether > 1100 sites of C‐to‐U and 1300 sites of U‐to‐C editing. The nuclear genome reveals > 1400 genes for PPR proteins with variable carboxyterminal DYW domains. We observe significant variants of the ‘classic’ DYW domain, in the meantime confirmed as the cytidine deaminase for C‐to‐U editing, and discuss the first attractive candidates for reverse editing factors given their excellent matches to U‐to‐C editing targets according to the PPR‐RNA binding code.

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Section: New Phytologistcontrasting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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“…RNA editing in plastids and mitochondria in higher plants requires PPR proteins for site recognition and proteins of the multiple organellar RNA editing factor (MORF) family as cofactors (Zehrmann et al ., ). Our Y2H, BiFC and Co‐IP assays demonstrated that WSP1 (a MORF family member) could interact with DUA1.…”

Section: Discussionmentioning

confidence: 97%

The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice

Cui

Wang

et al. 2018

New Phytologist

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Summary Low temperature stress hinders plant growth and chloroplast development and can limit the geographic range of cultivars. In rice, japonica cultivars have greater chilling tolerance than indica cultivars, but the molecular mechanism underlying chilling tolerance is unclear. Here, we report an RNA‐binding protein, DUA1, cloned from the indica cultivar Dular, which exhibits a deficiency in chloroplast development at an early stage of development under low‐temperature conditions. DUA1 shares high sequence homology with the pentatricopeptide repeat family and functions in plastid RNA editing under low‐temperature conditions. Our data suggest that DUA1 can bind to the plastid‐encoded rps8‐182 transcript and disruption of DUA1 activity impairs editing. The RNA editing cofactor WSP1, a partner of DUA1, also participates in chloroplast development at low temperature. Western blot analysis indicates that WSP1 enhances DUA1 stability under low temperatures. DUA1 sequence analyses of rice core germplasm revealed that three major haplotypes of DUA1 and one haplotype showed substantial differences in chlorophyll content under low‐temperature conditions. Variation at DUA1 may play an important role in the adaptation of rice to different growing regions.

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“…7B). The large overlap of mitochondrial sites controlled by RIP1 and RIP3 is supported by a physical interaction between these two proteins, as demonstrated by yeast two-hybrid (Y2H), pulldown, and bimolecular fluorescence complementation (BiFC) assays (Zehrmann et al, 2015).…”

Section: Orrm4 Interacts With Rip1mentioning

confidence: 99%

RNA Recognition Motif-Containing Protein ORRM4 Broadly Affects Mitochondrial RNA Editing and Impacts Plant Development and Flowering

et al. 2015

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Plant RNA editosomes modify cytidines (C) to uridines (U) at specific sites in plastid and mitochondrial transcripts. Members of the RNA-editing factor interacting protein (RIP) family and Organelle RNA Recognition Motif-containing (ORRM) family are essential components of the Arabidopsis (Arabidopsis thaliana) editosome. ORRM2 and ORRM3 have been recently identified as minor mitochondrial editing factors whose silencing reduces editing efficiency at ;6% of the mitochondrial C targets. Here we report the identification of ORRM4 (for organelle RRM protein 4) as a novel, major mitochondrial editing factor that controls ;44% of the mitochondrial editing sites. C-to-U conversion is reduced, but not eliminated completely, at the affected sites. The orrm4 mutant exhibits slower growth and delayed flowering time. ORRM4 affects editing in a site-specific way, though orrm4 mutation affects editing of the entire transcript of certain genes. ORRM4 contains an RRM domain at the N terminus and a Gly-rich domain at the C terminus. The RRM domain provides the editing activity of ORRM4, whereas the Gly-rich domain is required for its interaction with ORRM3 and with itself. The presence of ORRM4 in the editosome is further supported by its interaction with RIP1 in a bimolecular fluorescence complementation assay. The identification of ORRM4 as a major mitochondrial editing factor further expands our knowledge of the composition of the RNA editosome and reveals that adequate mitochondrial editing is necessary for normal plant development.

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Selective Homo- and Heteromer Interactions between the Multiple Organellar RNA Editing Factor (MORF) Proteins in Arabidopsis thaliana

Cited by 56 publications

References 40 publications

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

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

The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice

RNA Recognition Motif-Containing Protein ORRM4 Broadly Affects Mitochondrial RNA Editing and Impacts Plant Development and Flowering

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