The pentatricopeptide repeat protein <scp>EMP</scp>9 is required for mitochondrial <i>ccmB</i> and <i>rps4</i> transcript editing, mitochondrial complex biogenesis and seed development in maize

Yang, Yan‐Zhuo; Ding, Shuo; Wang, Hongchun; Sun, Feng; Huang, Wenlong; Song, Shu; Xu, Chunhui; Tan, Bin

doi:10.1111/nph.14424

Cited by 67 publications

(71 citation statements)

References 71 publications

(118 reference statements)

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“…Thus, we detected partial editing of the cox2 ‐449 site in the emp18‐2 mutant (Fig. a), which is consistent with the previous report that disruption of the E+ domain in EMP5 and EMP9 does not abolish the RNA editing (Liu et al ., ; Yang et al ., ). Another possibility may be that the partner proteins for EMP18 are different in the editing of atp6 ‐635 and cox2 ‐449, and the mutation in emp18‐2 has more severe impact on the interaction with the protein functioning in atp6 ‐635 editing than the protein functioning in cox2 ‐449 editing.…”

Section: Discussionmentioning

confidence: 97%

“…Apart from DYW-PPR proteins, several E-PPR proteins have also been considered to be related to RNA editing at one or several sites in plant mitochondrial transcripts (Takenaka et al, 2010;Hammani et al, 2011;Murayama et al, 2012;Yuan & Liu, 2012;Zhu et al, 2012;Li et al, 2014;Sun F. et al, 2015). These RNA editing sites are mostly located in transcripts encoding proteins of complex I, III or IV of the mitochondrial respiratory chain, and their editing defects often result in partially or completely deficient function of these complexes, and lead to abnormal plant growth or seed development (Kim et al, 2009;Liu et al, 2013;Li et al, 2014;Sun F. et al, 2015;Yang et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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EMP18 functions in mitochondrial atp6 and cox2 transcript editing and is essential to seed development in maize

Huang

Yang

et al. 2018

New Phytologist

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RNA editing plays an important role in organellar gene expression in plants, and pentatricopeptide repeat (PPR) proteins are involved in this function. Because of its large family size, many PPR proteins are not known for their function and roles in plant growth and development. Through genetic and molecular analyses of the empty pericarp18 (emp18) mutant in maize (Zea mays), we cloned the Emp18 gene, revealed its molecular function, and defined its role in the mitochondrial complex assembly and seed development. Emp18 encodes a mitochondrial-localized DYW-PPR protein. Null mutation of Emp18 arrests embryo and endosperm development at an early stage in maize, resulting in embryo lethality. Mutants are deficient in the cytidine (C)-to-uridine (U) editing at atp6-635 and cox2-449, which converts a Leu to Pro in ATP6 and a Met to Thr in Cox2. The atp6 gene encodes the subunit a of F F -ATPase. The Leu to Pro alteration disrupts an α-helix of subunit a, resulting in a dramatic reduction in assembly and activity of F F -ATPase holoenzyme and an accumulation of free F -subcomplex. These results demonstrate that EMP18 functions in the C-to-U editing of atp6 and cox2, and is essential to mitochondrial biogenesis and seed development in maize.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

EMP18 functions in mitochondrial atp6 and cox2 transcript editing and is essential to seed development in maize

Huang

Yang

et al. 2018

New Phytologist

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“…In general, editing events restore evolutionarily conserved amino acids, which is crucial for proper protein expression, function and regulation. (Chen et al ., ; Wang et al ., ; Yang et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation

Xiao

Líu

et al. 2018

New Phytologist

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RNA editing is a post-transcriptional maturation process affecting organelle transcripts in land plants. However, the molecular functions and physiological roles of RNA editing are still poorly understood. Using high-throughput sequencing, we identified 692 RNA editing sites in the Gossypium hirsutum mitochondrial genome. A total of 422 editing sites were found in the coding regions and all the edits are cytidine (C) to uridine (U) conversions. Comparative analysis showed that two editing sites in Ghatp1, C1292 and C1415, had a prominent difference in editing efficiency between fiber and ovule. Biochemical and genetic analyses revealed that the two vital editing sites were important for the interaction between the α and β subunits of ATP synthase, which resulted in ATP accumulation and promoted cell growth in yeast. Ectopic expression of C1292, C1415, or doubly edited Ghatp1 in Arabidopsis caused a significant increase in the number of trichomes in leaves and root length. Our results indicate that editing at C1292 and C1415 sites in Ghatp1 is crucial for ATP synthase to produce sufficient ATP for cotton fiber cell elongation. This work extends our understanding of RNA editing in atp1 and ATP synthesis, and provides insights into the function of mitochondrial edited Atp1 protein in higher plants.

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“…Although with sequence similarity among the PPR motifs, PPRs exhibit functional distinction and non‐redundancy in assisting the organelle expression and evolutional diversity between monocots and eudicots (Fujii and Small, ; Barkan and Small, ; Manna, ). The PLS (repeat P–L–S motif)‐subfamily PPRs predominantly assist in RNA editing (Takenaka et al ., ; Barkan and Small, ; Li et al ., ; Sun et al ., ; Qi et al ., ; Wang et al ., ; Yang et al ., ) and RNA splicing (Chateigner‐Boutin et al ., ; Ichinose et al ., ), whereas the P subfamily PPRs have been functionally characterized in mitochondrial intron splicing (Brown et al ., ; Colas des Francs‐Small and Small, ; Colas des Francs‐Small et al ., ; Hsu et al ., ; Hsieh et al ., ; Chen et al ., ; Xiu et al ., ; Cai et al ., ; Qi et al ., ; Ren et al ., ; Dai et al ., ), transcript stabilization (Colas des Francs‐Small and Small, ; Lee et al ., ; Wang et al ., ; Zhang et al ., ), cleavage and translation (Colas des Francs‐Small and Small, ; Haïli et al ., ). Nonetheless, the number of characterized mitochondrial PPRs involved in the splicing of group II introns is very few, especially for the case of mutations leading to embryo lethality which often negates genetic and molecular studies (Barkan and Small, ; Colas des Francs‐Small and Small, ).…”

Section: Introductionmentioning

confidence: 99%

The pentatricopeptide repeat protein EMPTY PERICARP8 is required for the splicing of three mitochondrial introns and seed development in maize

et al. 2018

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Splicing of plant organellar group II introns is under accurate nuclear control that employs many nucleus-encoded protein cofactors from various families. For mitochondrial introns, only a few splicing factors have been characterized because disruption of their functions often causes embryo lethality. Here, we report the function of Empty Pericarp8 (Emp8) in the splicing of three group II introns in mitochondria, complex I biogenesis, and seed development in maize. Emp8 encodes a P subfamily pentatricopeptide repeat protein that localizes in mitochondria. The loss-of-function mutants of Emp8 are embryo lethal, showing severely arrested embryo and endosperm development in maize. The respiration rate in the emp8 mutants is reduced with substantially enhanced expression of alternative oxidases. Transcript analysis indicated that the trans-splicing of nad1 intron 4 and cis-splicing of nad4 intron 1 are abolished, and the cis-splicing of nad2 intron 1 is severely impaired in the emp8 mutants. These defects consequently lead to the disassembly of mitochondrial complex I and a dramatic reduction in its activity. Together, these results suggest that Emp8 is required for the trans-splicing of nad1 intron 4 and cis-splicing of nad4 intron 1 and nad2 intron 1, which is essential to mitochondrial complex I assembly and hence to embryogenesis and endosperm development in maize.

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The pentatricopeptide repeat protein EMP9 is required for mitochondrial ccmB and rps4 transcript editing, mitochondrial complex biogenesis and seed development in maize

Cited by 67 publications

References 71 publications

EMP18 functions in mitochondrial atp6 and cox2 transcript editing and is essential to seed development in maize

EMP18 functions in mitochondrial atp6 and cox2 transcript editing and is essential to seed development in maize

Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation

The pentatricopeptide repeat protein EMPTY PERICARP8 is required for the splicing of three mitochondrial introns and seed development in maize

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