The Unexpected Diversity of Plant Organelle RNA Editosomes

Sun, Tao; Bentolila, Stéphane; Hanson, Maureen R.

doi:10.1016/j.tplants.2016.07.005

Cited by 165 publications

(174 citation statements)

References 88 publications

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“…5), suggesting that ORRM6 may form oligomers. While the stoichiometry of editing factors present in editosomes is not yet known (Sun et al, 2016), our evidence indicates that the RNA editosomes acting on psbF-C77 and accD-C794 contain one or more RIP/MORF proteins, OZ1, ORRM6, and either PPR protein LPA66 or RARE1, respectively.…”

Section: Orrm6 Is a New And Unusual Component Of Particular Arabidopsmentioning

confidence: 79%

“…RNA editing in the coding regions of mRNAs restores conserved codons and is thought to be a correction mechanism for defective genes at the transcript level (Lutz and Maliga, 2001;Schmitz-Linneweber and Barkan, 2007;ChateignerBoutin andSmall, 2010, 2011;Dalby and Bonen, 2013;Takenaka et al, 2013;Börner et al, 2014;Sun et al, 2016). Different plant species vary in their numbers of organelle RNA editing sites (Bock, 1998(Bock, , 2000Tillich et al, 2005;Li-Pook-Than et al, 2007;Robbins et al, 2009;Wang et al, 2015).…”

mentioning

confidence: 99%

“…Four types of proteins have been identified as C-to-U RNA editing factors in the plastid: PLS subfamily pentatricopeptide repeat (PPR) proteins, RNA editing factor interacting proteins/multiple organellar RNA editing factors (RIPs/MORFs), organelle RNA recognition motif-containing proteins (ORRMs), and organelle zinc finger proteins (OZs; Takenaka et al, 2012;Sun et al, 2013Sun et al, , 2015Barkan and Small, 2014;Colas des FrancsSmall and Small, 2014;Shi et al, 2016a). At least one PPR protein, RIP/MORF protein, and ORRM protein are likely to be present in each editosome, which differ in composition in chloroplasts versus mitochondria and between different transcripts in the same organelle (Sun et al, 2016).…”

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confidence: 99%

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An Organelle RNA Recognition Motif Protein is Required for Photosynthetic Subunit psbF Transcript Editing

et al. 2017

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Loss-of-function mutations in ORGANELLE RNA RECOGNITION MOTIF PROTEIN6 (ORRM6) result in the near absence of RNA editing of psbF-C77 and the reduction in accD-C794 editing in Arabidopsis (Arabidopsis thaliana). The orrm6 mutants have decreased levels of photosystem II (PSII) proteins, especially PsbF, lower PSII activity, pale green pigmentation, smaller leaf and plant sizes, and retarded growth. Stable expression of ORRM6 rescues the orrm6 editing defects and mutant phenotype. Unlike ORRM1, the other known ORRM plastid editing factor, ORRM6, does not contain RNA editing interacting protein/multiple organellar RNA editing factor (RIP/MORF) boxes, which are required for ORRM1 to interact with site-specific pentatricopeptide repeat protein editing factors. ORRM6 interacts with RIP1/MORF8, RIP2/MORF2, and RIP9/MORF9, known components of RNA editosomes. While some plastid RRM proteins are involved in other forms of RNA processing and translation, the primary function of ORRM6 is evidently to mediate psbF-C77 editing, like the essential site-specific pentatricopeptide repeat protein LOW PSII ACCUMULATION66. Stable expression in the orrm6 mutants of a nucleus-encoded, plastid-targeted PsbF protein from a psbF gene carrying a T at nucleotide 77 significantly increases leaf and plant sizes, chlorophyll content, and PSII activity. These transformants demonstrate that plastid RNA editing can be bypassed through the expression of nucleus-encoded, edited forms of plastid genes.

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Section: Orrm6 Is a New And Unusual Component Of Particular Arabidopsmentioning

confidence: 79%

mentioning

confidence: 99%

mentioning

confidence: 99%

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An Organelle RNA Recognition Motif Protein is Required for Photosynthetic Subunit psbF Transcript Editing

et al. 2017

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“…Length variants of PPR repeats have been detected however, with repeats that are longer (L) or shorter (S) than the initially-recognized 35-amino-acid (P) motif (11,15). PLS PPR proteins, which contain ordered series of P, L and S motifs, have been almost exclusively associated with RNA editing in both mitochondria and chloroplasts (16,17). In contrast, PPR proteins exclusively composed of P-type repeats were shown to participate in various aspects of organellar RNA expression ranging from gene transcription to mRNA translation (for review see (12,18)).…”

Section: Introductionmentioning

confidence: 99%

The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3΄ end of its 5΄-half intron

Wang

Aubé

Planchard

et al. 2017

Nucleic Acids Research

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RNA expression in plant mitochondria implies a large number of post-transcriptional events in which transcript processing and stabilization are essential. In this study, we analyzed the function of the Arabidopsis mitochondrial stability factor 2 gene (MTSF2) and show that the encoded pentatricopeptide repeat protein is essential for the accumulation of stable nad1 mRNA. The production of mature nad1 requires the assembly of three independent RNA precursors via two trans-splicing reactions. Genetic analyses revealed that the lack of nad1 in mtsf2 mutants results from the specific destabilization of the nad1 exons 2–3 precursor transcript. We further demonstrated that MTSF2 binds to its 3΄ extremity with high affinity, suggesting a protective action by blocking exoribonuclease progression. By defining the 3΄ end of nad1 exons 2–3 precursor, MTSF2 concomitantly determines the 3΄ extremity of the first half of the trans-intron found at the end of the transcript. Therefore, binding of the MTSF2 protein to nad1 exons 2–3 precursor evolved both to stabilize the transcript and to define a 3΄ extremity compatible with the trans-splicing reaction needed to reconstitute mature nad1. We thus reveal that the range of transcripts stabilized by association with protective protein on their 3΄ end concerns also mitochondrial precursor transcripts.

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“…The site specificity of the cytidines to be edited in a plant organelle is determined by a crucial cis -acting regulatory sequence 10–14 and the RNA editosome that will bind to it. The RNA editosome is composed of nuclear-encoded trans -acting factors that recognize the cis -element and perform RNA editing 15 . Recent extensive genetics studies have revealed that these trans -factors enlisted in the RNA editosome include DYW-type pentatricopeptide repeat (PPR) proteins 1 , RNA-Editing Factor Interacting Protein (RIP) family or Multiple Organelle RNA Editing Factor (MORF) family proteins 16, 17 , RNA-recognition motif (RRM)-containing proteins 18–20 , protoporphyrinogen IX oxidase 1 (PPO1) 21 and organelle zinc-finger 1 (OZ1) 22 .…”

Section: Introductionmentioning

confidence: 99%

Functional divergence and origin of the DAG-like gene family in plants

Luo

Cai

Zhang

et al. 2017

Sci Rep

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The nuclear-encoded DAG-like (DAL) gene family plays critical roles in organelle C-to-U RNA editing in Arabidopsis thaliana. However, the origin, diversification and functional divergence of DAL genes remain unclear. Here, we analyzed the genomes of diverse plant species and found that: DAL genes are specific to spermatophytes, all DAL genes share a conserved gene structure and protein similarity with the inhibitor I9 domain of subtilisin genes found in ferns and mosses, suggesting that DAL genes likely arose from I9-containing proproteases via exon shuffling. Based on phylogenetic inference, DAL genes can be divided into five subfamilies, each composed of putatively orthologous and paralogous genes from different species, suggesting that all DAL genes originated from a common ancestor in early seed plants. Significant type I functional divergence was observed in 6 of 10 pairwise comparisons, indicating that shifting functional constraints have contributed to the evolution of DAL genes. This inference is supported by the finding that functionally divergent amino acids between subfamilies are predominantly located in the DAL domain, a critical part of the RNA editosome. Overall, these findings shed light on the origin of DAL genes in spermatophytes and outline functionally important residues involved in the complexity of the RNA editosome.

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The Unexpected Diversity of Plant Organelle RNA Editosomes

Cited by 165 publications

References 88 publications

An Organelle RNA Recognition Motif Protein is Required for Photosynthetic Subunit psbF Transcript Editing

An Organelle RNA Recognition Motif Protein is Required for Photosynthetic Subunit psbF Transcript Editing

The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3΄ end of its 5΄-half intron

Functional divergence and origin of the DAG-like gene family in plants

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