Dek35 Encodes a PPR Protein that Affects cis -Splicing of Mitochondrial nad4 Intron 1 and Seed Development in Maize

Chen, Xinze; Feng, Fan; Qi, Weiwei; Xu, Liming; Yao, Dongsheng; Wang, Qun; Song, Rentao

doi:10.1016/j.molp.2016.08.008

Cited by 114 publications

(134 citation statements)

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“…More transcripts containing unspliced nad4 introns 1 and 3 are present in dek43 than in the WT, but splicing is not abolished (Figure A–D). Similarly, the cis ‐splicing of nad4 intron 1 occurs in dek35 (Chen et al 2017); however, it is abolished in emp8 (Figure ) (Sun et al 2018). Thus, DEK35, EMP8, EMP602, and DEK43 are required for the splicing of nad4 intron 1 (Figure ) (Chen et al 2017; Sun et al 2018), whereas EMP602 and DEK43 are required for the splicing of nad4 intron 3 (Ren et al 2019) (Figure ).…”

Section: Discussionmentioning

confidence: 97%

“…EMP10 and DEK37 are involved in the cis ‐splicing of mitochondrial nad2 intron 1 (Cai et al 2017; Dai et al 2018). DEK35 is a PPR protein that affects the cis ‐splicing of mitochondrial nad4 intron 1 (Chen et al 2017), and the PPR protein DEK2 affects the splicing of mitochondrial nad1 intron 1 (Qi et al 2017). EMP11 serves as a splicing factor of mitochondrial nad1 intron (Ren et al 2017), and EMP8 is required for the splicing of three mitochondrial introns ( nad1 intron 4, nad2 intron 1, nad4 intron 1) (Sun et al 2018).…”

Section: Introductionmentioning

confidence: 99%

“…The splicing of nad4 intron 1 involves NMS1, DEK35, and EMP8 (Brangeon et al 2000; Chen et al 2017; Sun et al 2018). In Arabidopsis , nMAT1, a nucleus‐encoded maturase, functions in nad4 intron 2 cis ‐splicing (Brangeon et al 2000; Chen et al 2017; Sun et al 2018). EMP602 is responsible for the cis ‐splicing of nad4 introns 1 and 3 (Ren et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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DEK43 is a P‐type pentatricopeptide repeat (PPR) protein responsible for the Cis‐splicing of nad4 in maize mitochondria

Ren

Wang

Zhang

et al. 2019

JIPB

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Mitochondria, the main energy transducers in plant cells, require the proper assembly of respiratory chain complexes I–V for their function. The NADH dehydrogenase 4 (nad4) gene encodes mitochondrial respiratory chain complex I subunit IV, but the mechanism underlying nad4 transcript splicing is unclear. Here, we report that the P‐type pentatricopeptide repeat (PPR) protein DEFECTIVE KERNEL 43 (DEK43) is responsible for cis‐splicing of the nad4 transcript in maize. We demonstrate that DEK43 localizes to both the nucleus and mitochondria. The mutation of Dek43 resulted in embryo‐lethal and light‐colored defective kernels. Among the 22 mitochondrial group II introns, the splicing efficiency of nad4 introns 1 and 3 was reduced by up to 50% compared to the wild type. The levels of complex I and supercomplex I+III2 were also reduced in dek43. Furthermore, in‐gel NADH dehydrogenase assays indicated that the activities of these complexes were significantly reduced in dek43. Further, the mitochondrial ultrastructure was altered in the mutant. Together, our findings indicate that DEK43, a dual‐localized PPR protein, plays an important role in maintaining mitochondrial function and maize kernel development.

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Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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DEK43 is a P‐type pentatricopeptide repeat (PPR) protein responsible for the Cis‐splicing of nad4 in maize mitochondria

Ren

Wang

Zhang

et al. 2019

JIPB

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“…The two DNA samples were hybridized and sequenced using the maize SNP3072 chip (Tian et al ). The genotype data from each sample were analyzed by the Illumina Genome Studio Genotyping Module according to the manufacturer's instructions (Chen et al ).…”

Section: Methodsmentioning

confidence: 99%

“…Mu tag isolation was performed according to a previously described protocol (Chen et al ) and adapted as follows. Genomic DNA was extracted with the same protocol as the SNP genotyping array.…”

Section: Methodsmentioning

confidence: 99%

Dek42 encodes an RNA‐binding protein that affects alternative pre‐mRNA splicing and maize kernel development

Zuo

Feng

et al. 2019

JIPB

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RNA‐binding proteins (RBPs) play an important role in post‐transcriptional gene regulation. However, the functions of RBPs in plants remain poorly understood. Maize kernel mutant dek42 has small defective kernels and lethal seedlings. Dek42 was cloned by Mutator tag isolation and further confirmed by an independent mutant allele and clustered regularly interspaced short palindromic repeats (CRISPR)‐CRISPR‐associated protein 9 materials. Dek42 encodes an RRM_RBM48 type RNA‐binding protein that localizes to the nucleus. Dek42 is constitutively expressed in various maize tissues. The dek42 mutation caused a significant reduction in the accumulation of DEK42 protein in mutant kernels. RNA‐seq analysis showed that the dek42 mutation significantly disturbed the expression of thousands of genes during maize kernel development. Sequence analysis also showed that the dek42 mutation significantly changed alternative splicing in expressed genes, which were especially enriched for the U12‐type intron‐retained type. Yeast two‐hybrid screening identified SF3a1 as a DEK42‐interacting protein. DEK42 also interacts with the spliceosome component U1‐70K. These results suggested that DEK42 participates in the regulation of pre‐messenger RNA splicing through its interaction with other spliceosome components. This study showed the function of a newly identified RBP and provided insights into alternative splicing regulation during maize kernel development.

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OsPPR939, a nad5 splicing factor, is essential for plant growth and pollen development in rice

Peng

Liu

et al. 2021

Theor Appl Genet

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Key message P-subfamily PPR protein OsPPR939, which can be phosphorylated by OsS6K1, regulates plant growth and pollen development by involving in the splicing of mitochondrial nad5 introns 1, 2, and 3. Abstract In land plants, pentatricopeptide repeat (PPR) proteins play key roles in mitochondrial group II intron splicing, but how these nucleus-encoded proteins are imported into mitochondria is unknown. To date, a few PPR proteins have been characterized in rice (Oryza sativa). Here, we demonstrate that the mitochondrion-localized P-subfamily PPR protein OsPPR939 is required for the splicing of nad5 introns 1, 2, and 3 in rice. Complete knockout or partial disruption of OsPPR939 function resulted in different degrees of growth retardation and pollen sterility. The dramatically reduced splicing efficiency of these introns in osppr939-4 and osppr939-5 led to reduced mitochondrial complex I abundance and activity and enhanced expression of alternative respiratory pathway genes. Complementation with OsPPR939 rescued the defective plant morphology of osppr939-4 and restored its decreased splicing efficiency of nad5 introns 1, 2, and 3. Therefore, OsPPR939 plays crucial roles in plant growth and pollen development by splicing mitochondrial nad5 introns 1, 2, and 3. More importantly, the 12th amino acid Ser in the N-terminal targeting sequence of OsPPR939 is phosphorylated by OsS6K1, and truncated OsPPR939 with a non-phosphorylatable S12A mutation in its presequence could not be imported into mitochondria, suggesting that phosphorylation of this amino acid plays an important role in the mitochondrial import of OsPPR939. To our knowledge, the 12th residue Ser on OsPPR939 is the first experimentally proven phosphorylation site in PPR proteins. Our results provide a basis for investigating the regulatory mechanism of PPR proteins at the post-translational level.

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Dek35 Encodes a PPR Protein that Affects cis -Splicing of Mitochondrial nad4 Intron 1 and Seed Development in Maize

Cited by 114 publications

References 71 publications

DEK43 is a P‐type pentatricopeptide repeat (PPR) protein responsible for the Cis‐splicing of nad4 in maize mitochondria

DEK43 is a P‐type pentatricopeptide repeat (PPR) protein responsible for the Cis‐splicing of nad4 in maize mitochondria

Dek42 encodes an RNA‐binding protein that affects alternative pre‐mRNA splicing and maize kernel development

OsPPR939, a nad5 splicing factor, is essential for plant growth and pollen development in rice

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