The mitochondrial pentatricopeptide repeat protein EMP12 is involved in the splicing of three<i>nad2</i>introns and seed development in maize

Sun, Feng; Xiu, Zhihui; Jiang, Ruicheng; Liu, Yiwei; Zhang, Xiaoyan; Yang, Yan‐Zhuo; Li, Xiaojie; Zhang, Xin; Wang, Yong; Tan, Bin

doi:10.1093/jxb/ery432

Cited by 49 publications

(44 citation statements)

References 73 publications

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“…Indeed, multiple, independent cis-splicing factors are needed to splice a single intron. Similarly, EMP8, EMP10, and DEK37 are required for the splicing of nad2 intron 1 ( Figure 6) Dai et al 2018;Sun et al 2018), and EMP16 and EMP12 are required for the splicing of nad2 intron 4 ( Figure 6) (Xiu et al 2016;Sun et al 2019). On the other hand, one splicing factor can be involved in the splicing of multiple introns, as exemplified by EMP11, EMP8, and EMP12 ( Figure 6) Sun et al 2018Sun et al , 2019, indicating that splicing factors exhibit a wide range of specificity for their plant mitochondrial gene transcripts.…”

Section: Discussionmentioning

confidence: 99%

“…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%

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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: 99%

Section: Introductionmentioning

confidence: 99%

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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“…In many cases, PPR genes are responsible for these phenotypes, due to their function in organellar gene expression. Generally, null alleles of PPR genes in previous studies produce kernels that are with obvious development abnormality at early stages and are easily distinguished from normal kernels on self-crossed F 1 ears due to their smaller size, pale pericarp, flat or shrunken appearance (Manavski et al, 2012; Sosso et al, 2012; Li et al, 2014; Sun et al, 2015; Xiu et al, 2016; Cai et al, 2017; Chen et al, 2017; Qi et al, 2017; Ren et al, 2017; Dai et al, 2018; Li et al, 2018; Sun et al, 2019). Unlike these kernel mutants, kernels produced by null allele of qKW9 are similar in appearance and viability although smaller in size comparing to wild type, and kernel weight is determined by genotype of maternal plant rather than kernel genotype.…”

Section: Discussionmentioning

confidence: 99%

“…Several of these maize kernel development genes have been identified. For instance, EMP10 (Cai et al, 2017), EMP11 (Ren et al, 2017), EMP12 (Sun et al, 2019), EMP16 (Xiu et al, 2016), DEK35 (Chen et al, 2017), and DEK37 (Dai et al, 2018) are involved in intron splicing of mitochondrial genes. In contrast, MPPR6 functions in maturation and translation initiation of mitochondrial ribosomal protein subunit mRNA(Manavski et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

qKW9encodes a pentatricopeptide repeat protein affecting photosynthesis and grain filling in maize

Huang

Lü

Liu

et al. 2019

Preprint

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Kernel weight is an important yield component in maize that was selected during domestication. Many kernel weight genes have been identified through mutant analysis, and are mostly involved in the biogenesis and functional maintenance of organelles or other fundamental cellular activities. However, only a limited number of loci underlying quantitative variation in kernel weight have been cloned. Here we characterize a maize kernel weight QTL, qKW9 and find that it encodes a DYW motif pentatricopeptide repeat protein involved in C-to-U editing of NdhB, a subunit of the chloroplast NADH dehydrogenase-like complex. In a null qKW9 background, C-to-U editing of NdhB was abolished, and photosynthesis was reduced, suggesting that qKW9 regulates kernel weight by controling the maternal source of photosynthate for grain filling. Characterization of qKW9 highlights the importance of optimizing photosynthesis on maize grain yield production.

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“…Mutations of the above genes generally lead to delayed germination and retarded growth. Mutations of P-type PPRs in maize usually lead to lethal embryos within defective kernels or empty pericarps, in mutants such as defective kernel2 (dek2) (Qi et al, 2017), dek35 (Chen et al, 2017), dek37 (Dai et al, 2018), dek41/dek43 (Zhu et al, 2019; Ren et al, 2020), empty pericarp8 (emp8) (Sun et al, 2018), emp10 (Cai et al, 2017), emp11 (Ren et al, 2017), emp12 (Sun et al, 2019), emp16 (Xiu et al, 2016), emp602 (Ren et al, 2019) and ppr20 (Yang et al, 2020). In contrast to numerous P-subfamily PPR proteins reported in Arabidopsis and maize, few such proteins are reported in rice although its genome has 477 PPRs (O'Toole et al, 2008).…”

mentioning

confidence: 99%

Rice Floury Shrunken Endosperm5 encodes a putative plant organelle RNA recognition protein that is required for cis-splicing of mitochondrial nad4 intron 1

Wang

Zhang

Liu

et al. 2020

Preprint

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Background: Some important mitochondrial-encoded genes for respiration in higher plants are interrupted by introns. Many nuclear-encoded factors are involved in the splicing of these introns, but the underlying mechanisms remain to be deciphered.Results: Here, we isolated and characterized a rice mutant named floury shrunken endosperm5 (fse5). In addition to floury shrunken endosperm seeds with mutant phenotype either failed to germinate or produced retarded lethal seedlings. The Fse5 encodes a putative plant organelle RNA recognition (PORR) protein targeted to mitochondria. Mutation of Fse5 hindered splicing of the first intron of nad4, that encodes an essential subunit of mitochondrial NADH dehydrogenase Complex I. The assembly and NADH dehydrogenase activity of Complex I were disrupted and the structure of the mitochondria was abnormal in the fse5 mutant. FSE5 protein was shown to interact with Mitochondrial Intron Splicing Factor 68 (MISF68), which is also a splicing factor for nad4 intron 1 identified previously in a yeast two-hybrid assay.Conclusion: Fse5 encoding a PORR protein is essential for splicing of nad4 intron 1, and loss of function affects seed development and seedling growth.

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The mitochondrial pentatricopeptide repeat protein EMP12 is involved in the splicing of threenad2introns and seed development in maize

Abstract: The mitochondrial PPR protein EMP12 is required for the splicing of cis- and trans-introns of nad2, complex I biogenesis, and seed development in maize.

Cited by 49 publications

References 73 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

qKW9encodes a pentatricopeptide repeat protein affecting photosynthesis and grain filling in maize

Rice Floury Shrunken Endosperm5 encodes a putative plant organelle RNA recognition protein that is required for cis-splicing of mitochondrial nad4 intron 1

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