The involvement of a PPR protein of the P subfamily in partial RNA editing of an Arabidopsis mitochondrial transcript

Abstract C-to-U RNA editing in plant mitochondria requires the participation of many nucleus-encoded factors, most of which are pentatricopeptide repeat (PPR) proteins. There is a large number of PPR proteins and the functions many of them are unknown. Here, we report a mitochondrion-localized DYW-subgroup PPR protein, PPR27, which functions in the editing of multiple mitochondrial transcripts in maize. The ppr27 mutant is completely deficient in C-to-U editing at the ccmFN-1357 and rps3-707 sites, and editing at six other sites is substantially reduced. The lack of editing at ccmFN-1357 causes a deficiency of CcmFN protein. As CcmFN functions in the maturation pathway of cytochrome proteins that are subunits of mitochondrial complex III, its deficiency results in an absence of cytochrome c1 and cytochrome c proteins. Consequently, the assembly of mitochondrial complex III and super-complex I+III2 is decreased, which impairs the electron transport chain and respiration, leading to arrests in embryogenesis and endosperm development in ppr27. In addition, PPR27 was found to physically interact with ZmMORF1, which interacts with ZmMORF8, suggesting that these three proteins may facilitate C-to-U RNA editing via the formation of a complex in maize mitochondria. This RNA editing is essential for complex III assembly and seed development in maize.

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Novel DYW-type pentatricopeptide repeat (PPR) protein BLX controls mitochondrial RNA editing and splicing essential for early seed development of Arabidopsis

Journal of Genetics and Genomics ◽

10.1016/j.jgg.2018.01.006 ◽

2018 ◽

Vol 45 (3) ◽

pp. 155-168 ◽

Cited By ~ 9

Author(s):

Yan Sun ◽

Jiaying Huang ◽

Sheng Zhong ◽

Hongya Gu ◽

Shan He ◽

...

Keyword(s):

Rna Editing ◽

Seed Development ◽

Mitochondrial Rna ◽

Pentatricopeptide Repeat ◽

Ppr Protein ◽

Early Seed Development

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The novel E-subgroup pentatricopeptide repeat protein DEK55 is responsible for RNA editing at multiple sites and for the splicing of nad1 and nad4 in maize

BMC Plant Biology ◽

10.1186/s12870-020-02765-x ◽

2020 ◽

Vol 20 (1) ◽

Author(s):

Ru Chang Ren ◽

Xu Wei Yan ◽

Ya Jie Zhao ◽

Yi Ming Wei ◽

Xiaoduo Lu ◽

...

Keyword(s):

Rna Editing ◽

Rna Processing ◽

Mitochondrial Gene ◽

Endosperm Development ◽

Molecular Evidence ◽

Pentatricopeptide Repeat ◽

Reading Frame ◽

Maize Kernel ◽

Ppr Protein ◽

Ppr Proteins

Abstract Background Pentatricopeptide repeat (PPR) proteins compose a large protein family whose members are involved in both RNA processing in organelles and plant growth. Previous reports have shown that E-subgroup PPR proteins are involved in RNA editing. However, the additional functions and roles of the E-subgroup PPR proteins are unknown. Results In this study, we developed and identified a new maize kernel mutant with arrested embryo and endosperm development, i.e., defective kernel (dek) 55 (dek55). Genetic and molecular evidence suggested that the defective kernels resulted from a mononucleotide alteration (C to T) at + 449 bp within the open reading frame (ORF) of Zm00001d014471 (hereafter referred to as DEK55). DEK55 encodes an E-subgroup PPR protein within the mitochondria. Molecular analyses showed that the editing percentage of 24 RNA editing sites decreased and that of seven RNA editing sites increased in dek55 kernels, the sites of which were distributed across 14 mitochondrial gene transcripts. Moreover, the splicing efficiency of nad1 introns 1 and 4 and nad4 intron 1 significantly decreased in dek55 compared with the wild type (WT). These results indicate that DEK55 plays a crucial role in RNA editing at multiple sites as well as in the splicing of nad1 and nad4 introns. Mutation in the DEK55 gene led to the dysfunction of mitochondrial complex I. Moreover, yeast two-hybrid assays showed that DEK55 interacts with two multiple organellar RNA-editing factors (MORFs), i.e., ZmMORF1 (Zm00001d049043) and ZmMORF8 (Zm00001d048291). Conclusions Our results demonstrated that a mutation in the DEK55 gene affects the mitochondrial function essential for maize kernel development. Our results also provide novel insight into the molecular functions of E-subgroup PPR proteins involved in plant organellar RNA processing.

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Maize pentatricopeptide repeat protein DEK53 is required for mitochondrial RNA editing at multiple sites and seed development

Journal of Experimental Botany ◽

10.1093/jxb/eraa348 ◽

2020 ◽

Vol 71 (20) ◽

pp. 6246-6261 ◽

Cited By ~ 2

Author(s):

Dawei Dai ◽

Lifang Jin ◽

Zhenzhen Huo ◽

Shumei Yan ◽

Zeyang Ma ◽

...

Keyword(s):

Rna Editing ◽

Protein Complexes ◽

Plant Mitochondria ◽

Mitochondrial Protein ◽

Electron Microscopic Examination ◽

Complex Iii ◽

Mitochondrial Rna ◽

Pentatricopeptide Repeat ◽

Electron Microscopic ◽

Ppr Protein

Abstract Pentatricopeptide repeat (PPR) proteins were identified as site-specific recognition factors for RNA editing in plant mitochondria and plastids. In this study, we characterized maize (Zea mays) kernel mutant defective kernel 53 (dek53), which has an embryo lethal and collapsed endosperm phenotype. Dek53 encodes an E-subgroup PPR protein, which possesses a short PLS repeat region of only seven repeats. Subcellular localization analysis indicated that DEK53 is localized in the mitochondrion. Strand- and transcript-specific RNA-seq analysis showed that the dek53 mutation affected C-to-U RNA editing at more than 60 mitochondrial C targets. Biochemical analysis of mitochondrial protein complexes revealed a significant reduction in the assembly of mitochondrial complex III in dek53. Transmission electron microscopic examination showed severe morphological defects of mitochondria in dek53 endosperm cells. In addition, yeast two-hybrid and luciferase complementation imaging assays indicated that DEK53 can interact with the mitochondrion-targeted non-PPR RNA editing factor ZmMORF1, suggesting that DEK53 might be a functional component of the organellar RNA editosome.

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The DYW-E-PPR protein MEF14 is required for RNA editing at site matR -1895 in mitochondria of Arabidopsis thaliana

FEBS Letters ◽

10.1016/j.febslet.2011.01.037 ◽

2011 ◽

Vol 585 (4) ◽

pp. 700-704 ◽

Cited By ~ 23

Author(s):

Daniil Verbitskiy ◽

Barbara Härtel ◽

Anja Zehrmann ◽

Axel Brennicke ◽

Mizuki Takenaka

Keyword(s):

Arabidopsis Thaliana ◽

Rna Editing ◽

Ppr Protein

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Non-canonical Features of Pentatricopeptide Repeat Protein-Facilitated RNA Editing in Arabidopsis Chloroplasts

10.1101/544486 ◽

2019 ◽

Author(s):

Yueming Kelly Sun ◽

Bernard Gutmann ◽

Ian Small

Keyword(s):

Rna Editing ◽

Plant Mitochondria ◽

Pentatricopeptide Repeat ◽

Site Specific ◽

Ppr Protein ◽

Sequence Variations ◽

Ppr Proteins ◽

Editing Activity ◽

Chloroplast Rna ◽

Plant Organelles

AbstractCytosine (C) to uracil (U) RNA editing in plant mitochondria and chloroplasts is facilitated by site-specific pentatricopeptide repeat (PPR) editing factors. PPR editing factors contain multiple types of PPR motifs, and PPR motifs of the same type also show sequence variations. Therefore, no PPR motifs are invariant within a PPR protein or between different PPR proteins. This work evaluates the functional diversity of PPR motifs in CHLOROPLAST RNA EDITING FACTOR 3 (CREF3). The results indicate that previously overlooked features of PPR editing factors could also contribute to RNA editing activity. In particular, the N-terminal degenerated PPR motifs and the two L1-type PPR motifs in CREF3 are functionally indispensable. Furthermore, PPR motifs of the same type in CREF3 are not interchangeable. These non-canonical features of CREF3 have important implications on the understanding of PPR-facilitated RNA editing in plant organelles.

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The Amount of RNA Editing Sites in Liverwort Organellar Genes Is Correlated with GC Content and Nuclear PPR Protein Diversity

Genome Biology and Evolution ◽

10.1093/gbe/evz232 ◽

2019 ◽

Vol 11 (11) ◽

pp. 3233-3239 ◽

Cited By ~ 3

Author(s):

Shanshan Dong ◽

Chaoxian Zhao ◽

Shouzhou Zhang ◽

Hong Wu ◽

Weixue Mu ◽

...

Keyword(s):

Rna Editing ◽

Phylogenetic Diversity ◽

Gc Content ◽

Pentatricopeptide Repeat ◽

Protein Coding ◽

Protein Diversity ◽

Ppr Protein ◽

Ppr Proteins ◽

Codon Positions ◽

Positive Correlations

Abstract RNA editing occurs in the organellar mRNAs of all land plants but the marchantioid liverworts, making liverworts a perfect group for studying the evolution of RNA editing. Here, we profiled the RNA editing of 42 exemplars spanning the ordinal phylogenetic diversity of liverworts, and screened for the nuclear-encoded pentatricopeptide repeat (PPR) proteins in the transcriptome assemblies of these taxa. We identified 7,428 RNA editing sites in 128 organellar genes from 31 non-marchantioid liverwort species, and characterized 25,059 PPR protein sequences. The abundance of organellar RNA editing sites varies greatly among liverwort lineages, genes, and codon positions, and shows strong positive correlations with the GC content of protein-coding genes, and the diversity of the PLS class of nuclear PPR proteins.

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