The pentatricopeptide repeat protein <scp>EMPTY PERICARP</scp>8 is required for the splicing of three mitochondrial introns and seed development in maize

Sun, Feng; Zhang, Xiaoyan; Shen, Yun; Wang, Hongchun; Li, Rui; Wang, Xiaomin; Gao, Dahai; Yang, Yan‐Zhuo; Liu, Yiwei; Tan, Bin

doi:10.1111/tpj.14030

Cited by 57 publications

(64 citation statements)

References 77 publications

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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%

“…In the emp8 mutant, the trans ‐splicing of nad1 intron 4 and the cis ‐splicing of nad4 intron 1 are abolished, and the cis ‐splicing of nad2 intron 1 is severely reduced (Figure ). The emp8 progeny exhibit an embryo‐lethal phenotype, with severely arrested embryo and endosperm development (Sun et al 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, the cis-splicing of nad4 intron 1 occurs in dek35 (Chen et al 2017); however, it is abolished in emp8 ( Figure 6) . Thus, DEK35, EMP8, EMP602, and DEK43 are required for the splicing of nad4 intron 1 ( Figure 6) (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 6). Indeed, multiple, independent cis-splicing factors are needed to splice a single intron.…”

Section: Discussionmentioning

confidence: 99%

“…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). EMP12 is involved in the splicing of three nad2 introns including nad2 intron 1, nad2 intron 2, and nad2 intron 4 (Sun et al 2019).…”

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: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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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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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Maize kernel development

Dai

Song

2021

Mol Breeding

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

Cited by 57 publications

References 77 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

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

Maize kernel development

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