The Pentatricopeptide Repeat Protein OTP87 Is Essential for RNA Editing of nad7 and atp1 Transcripts in Arabidopsis Mitochondria

Hammani, Kamel; Francs‐Small, Catherine Colas des; Takenaka, Mizuki; Tanz, Sandra K.; Okuda, K; Shikanai, Toshiharu; Brennicke, Axel; Small, Ian

doi:10.1074/jbc.m111.230516

Cited by 80 publications

(70 citation statements)

References 65 publications

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“…Plant site-specific editing factors belong to the PLS subfamily of the PPR protein family (14). Binding of the cis-element and the PPR-PLS trans-factor has been demonstrated in several instances (35)(36)(37). Recent reports have demonstrated that RIPs, another small class of proteins, are also plant organelle editing transfactors (19,20).…”

Section: Discussionmentioning

confidence: 99%

An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize

Sun

Germain

Giloteaux

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Plant RNA editing modifies cytidines (C) to uridines (U) at specific sites in the transcripts of both mitochondria and plastids. Specific targeting of particular Cs is achieved by pentatricopeptide proteins that recognize cis elements upstream of the C that is edited. Members of the RNA-editing factor interacting protein (RIP) family in Arabidopsis have recently been shown to be essential components of the plant editosome. We have identified a gene that contains a pair of truncated RIP domains (RIP-RIP). Unlike any previously described RIP family member, the encoded protein carries an RNA recognition motif (RRM) at its C terminus and has therefore been named Organelle RRM protein 1 (ORRM1). ORRM1 is an essential plastid editing factor; in Arabidopsis and maize mutants, RNA editing is impaired at particular sites, with an almost complete loss of editing for 12 sites in Arabidopsis and 9 sites in maize. Transfection of Arabidopsis orrm1 mutant protoplasts with constructs encoding a region encompassing the RIP-RIP domain or a region spanning the RRM domain of ORRM1 demonstrated that the RRM domain is sufficient for the editing function of ORRM1 in vitro. According to a yeast two-hybrid assay, ORRM1 interacts selectively with pentatricopeptide transfactors via its RIP-RIP domain. Phylogenetic analysis reveals that the RRM in ORRM1 clusters with a clade of RRM proteins that are targeted to organelles. Taken together, these results suggest that other members of the ORRM family may likewise function in RNA editing.

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Section: Discussionmentioning

confidence: 99%

An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize

Sun

Germain

Giloteaux

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

133

185

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“…Recently, OTP87, a PPR-E editing factor, was shown to be dual-targeted to mitochondria and chloroplasts; however, although mutation of OTP87 was shown to affect mitochondrial editing, no effect on chloroplast editing extent in the mutant was reported (29). RIP1 is among about 50 dual-targeted proteins in plants reported to date; 16 of these proteins are amino acyl-tRNA synthetases (reviewed in ref.…”

Section: Discussionmentioning

confidence: 99%

“…CRR4, a PPR-E protein necessary for the editing of the plastid ndhD transcript, directly interacts with the transcript in the area surrounding the targeted C for editing (12). Two other PPR editing trans-factors, the Physcomitrella patens PpPPR_71 and A. thaliana OTP87, have been shown to bind the RNA sequence surrounding their target editing sites (29,51). However, the identity of all the proteins that act in conjunction with PPR proteins to convert C targets to U targets is unknown.…”

Section: Discussionmentioning

confidence: 99%

“…Among the 13 Arabidopsis members of the PLS subfamily reported to be mitochondrial editing factors (22)(23)(24)(25)(26)(27)(28)(29), only 5 members have been observed to control the editing extent at more than one site. MEF1 and MEF11 control the editing of three sites (22,27), whereas REME1, SLO1, and OTP87 control two sites each (23,24,29). Whether 100 PPR proteins are sufficient to recognize the over 500 C targets of editing in Arabidopsis mitochondria is presently unknown.…”

Section: Rip1 Controls the Editing Extent Of Many More Mitochondrial Cmentioning

confidence: 99%

“…The PLS subfamily, which is specific to the plant kingdom, can be further separated into smaller subclasses based on two C-terminal motifs, the E and DYW motifs (14). All of the well-characterized organelle editing factors that are required for editing at specific sites are members of the PLS subfamily of PPR proteins (11,(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29).…”

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RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing

Bentolila¹,

Heller²,

Sun³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

206

266

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Transcripts of plant organelle genes are modified by cytidine-touridine (C-to-U) RNA editing, often changing the encoded amino acid predicted from the DNA sequence. Members of the PLS subclass of the pentatricopeptide repeat (PPR) motif-containing family are site-specific recognition factors for either chloroplast or mitochondrial C targets of editing. However, other than PPR proteins and the cis-elements on the organelle transcripts, no other components of the editing machinery in either organelle have previously been identified. The Arabidopsis chloroplast PPR protein Required for AccD RNA Editing 1 (RARE1) specifies editing of a C in the accD transcript. RARE1 was detected in a complex of >200 kDa. We immunoprecipitated epitope-tagged RARE1, and tandem MS/MS analysis identified a protein of unknown function lacking PPR motifs; we named it RNA-editing factor interacting protein 1 (RIP1). Yeast two-hybrid analysis confirmed RIP1 interaction with RARE1, and RIP1-GFP fusions were found in both chloroplasts and mitochondria. Editing assays for all 34 known Arabidopsis chloroplast targets in a rip1 mutant revealed altered efficiency of 14 editing events. In mitochondria, 266 editing events were found to have reduced efficiency, with major loss of editing at 108 C targets. Virusinduced gene silencing of RIP1 confirmed the altered editing efficiency. Transient introduction of a WT RIP1 allele into rip1 improved the defective RNA editing. The presence of RIP1 in a protein complex along with chloroplast editing factor RARE1 indicates that RIP1 is an important component of the RNA editing apparatus that acts on many chloroplast and mitochondrial C targets.nucleoid | RNA editosome | dual targeting P osttranscriptional C-to-U RNA editing occurs in plastid and plant mitochondrial transcripts. In a typical vascular plant, ∼30 C targets in chloroplasts and over 500 C targets in mitochondria are targeted for editing (1, 2). The majority of the editing events results in encoding of a different amino acid than the one predicted from the genomic sequence. The editing-encoded amino acid is usually more conserved relative to residues present in homologous proteins in other organisms than the genomically encoded amino acid. Because there is presently no known case in which useful genetic variation results from partial editing of a transcript population, the current concept is that editing is a correction mechanism for thymidine-to-cytidine (T-to-C) mutations that have arisen in plant organelle genomes (1,3,4).Little is known about the molecular apparatus that is responsible for recognizing the correct C target for editing and converting it to U, although plant mitochondrial RNA editing was discovered over 20 y ago (5-7). cis-Elements for recognition of editing sites have been identified proximal and 5′ to the nucleotide to be modified (8-10). As few as 22 nt in sequence surrounding the C target is sufficient to specify RNA editing (9). In 2005, a pentatricopeptide repeat (PPR) motif-containing protein termed CRR4 was discovered to ...

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OsNDUFA9 encoding a mitochondrial complex I subunit is essential for embryo development and starch synthesis in rice

Tian

Zhu

et al. 2018

Plant Cell Rep

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Loss of function of a mitochondrial complex I subunit (OsNDUFA9) causes abnormal embryo development and affects starch synthesis by altering the expression of starch synthesis-related genes and proteins. Proton-pumping NADH: ubiquinone oxidoreductase (also called complex I) is thought to be the largest and most complicated enzyme of the mitochondrial respiratory chain. Mutations of complex I subunits have been revealed to link with a number of growth inhibitions in plants. However, the function of complex I subunits in rice remains unclear. Here, we isolated a rice floury endosperm mutant (named flo13) that was embryonic lethal and failed to germinate. Semi-thin sectioning analysis showed that compound starch grain development in the mutant was greatly impaired, leading to significantly compromised starch biosynthesis and decreased 1000-grain weight relative to the wild type. Map-based cloning revealed that FLO13 encodes an accessory subunit of complex I protein (designated as OsNDUFA9). A single nucleotide substitution (G18A) occurred in the first exon of OsNDUFA9, introducing a premature stop codon in the flo13 mutant gene. OsNDUFA9 was ubiquitously expressed in various tissues and the OsNDUFA9 protein was localized to the mitochondria. Quantitative RT-PCR and protein blotting indicated loss of function of OsNDUFA9 altered gene expression and protein accumulation associated with respiratory electron chain complex in the mitochondria. Moreover, transmission electron microscopic analysis showed that the mutant lacked obvious mitochondrial cristae structure in the mitochondria of endosperm cell. Our results demonstrate that the OsNDUFA9 subunit of complex I is essential for embryo development and starch synthesis in rice endosperm.

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The Pentatricopeptide Repeat Protein OTP87 Is Essential for RNA Editing of nad7 and atp1 Transcripts in Arabidopsis Mitochondria

Cited by 80 publications

References 65 publications

An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize

An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize

RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing

OsNDUFA9 encoding a mitochondrial complex I subunit is essential for embryo development and starch synthesis in rice

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