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

Pentatricopeptide repeat (PPR) protein comprises a large family, participating in various aspects of organellar RNA metabolism in land plants. There are approximately 600 PPR proteins in maize, but the functions of many PPR proteins remain unknown. In this study, we defined the function of PPR18 in the cis-splicing of nad4 intron 1 in mitochondria and seed development in maize. Loss function of PPR18 seriously impairs embryo and endosperm development, resulting in the empty pericarp (emp) phenotype in maize. PPR18 encodes a mitochondrion-targeted P-type PPR protein with 18 PPR motifs. Transcripts analysis indicated that the splicing of nad4 intron 1 is impaired in the ppr18 mutant, resulting in the absence of nad4 transcript, leading to severely reduced assembly and activity of mitochondrial complex I and dramatically reduced respiration rate. These results demonstrate that PPR18 is required for the cis-splicing of nad4 intron 1 in mitochondria, and critical to complex I assembly and seed development in maize.

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Maize Empty Pericarp602 Encodes a P-Type PPR Protein That Is Essential for Seed Development

Plant and Cell Physiology ◽

10.1093/pcp/pcz083 ◽

2019 ◽

Vol 60 (8) ◽

pp. 1734-1746 ◽

Cited By ~ 12

Author(s):

Zhenjing Ren ◽

Kaijian Fan ◽

Ting Fang ◽

Jiaojiao Zhang ◽

Li Yang ◽

...

Keyword(s):

Seed Development ◽

Rna Splicing ◽

Complex I ◽

Intron Splicing ◽

Loss Of Function ◽

Pentatricopeptide Repeat ◽

Ppr Protein ◽

Intron 1 ◽

Ppr Proteins ◽

P Type

Abstract Pentatricopeptide repeat (PPR) proteins play crucial roles in intron splicing, which is important for RNA maturation. Identification of novel PPR protein with the function of intron splicing would help to understand the RNA splicing mechanism. In this study, we identified the maize empty pericarp602 (emp602) mutants, the mature kernels of which showed empty pericarp phenotype. We cloned the Emp602 gene from emp602 mutants and revealed that Emp602 encodes a mitochondrial-localized P-type PPR protein. We further revealed that Emp602 is specific for the cis-splicing of mitochondrial Nad4 intron 1 and intron 3, and mutation of Emp602 led to the loss of mature Nad4 transcripts. The loss of function of Emp602 nearly damaged the assembly and accumulation of complex I and arrested mitochondria formation, which arrested the seed development. The failed assembly of complex I triggers significant upregulation of Aox expression in emp602 mutants. Transcriptome analysis showed that the expression of mitochondrial-related genes, e.g. the genes associated with mitochondrial inner membrane presequence translocase complex and electron carrier activity, were extensively upregulated in emp602 mutant. These results demonstrate that EMP602 functions in the splicing of Nad4 intron 1 and intron 3, and the loss of function of Emp602 arrested maize seed development by disrupting the mitochondria complex I assembly.

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Comprehensive Transcriptome Analyses Reveal Candidate Genes for Variation in Seed Size/Weight During Peanut (Arachis hypogaea L.) Domestication

Frontiers in Plant Science ◽

10.3389/fpls.2021.666483 ◽

2021 ◽

Vol 12 ◽

Author(s):

Zhongfeng Li ◽

Xingguo Zhang ◽

Kunkun Zhao ◽

Kai Zhao ◽

Chengxin Qu ◽

...

Keyword(s):

Candidate Genes ◽

Seed Development ◽

Seed Size ◽

Snp Markers ◽

Pentatricopeptide Repeat ◽

Significant Differential Expression ◽

Ppr Protein ◽

Cultivated Peanut ◽

Transcriptome Analyses ◽

Wild Peanut

Seed size/weight, a key domestication trait, is also an important selection target during peanut breeding. However, the mechanisms that regulate peanut seed development are unknown. We re-sequenced 12 RNA samples from developing seeds of two cultivated peanut accessions (Lines 8106 and 8107) and wild Arachis monticola at 15, 30, 45, and 60 days past flowering (DPF). Transcriptome analyses showed that ∼36,000 gene loci were expressed in each of the 12 RNA samples, with nearly half exhibiting moderate (2 ≤ FPKM < 10) expression levels. Of these genes, 12.2% (4,523) were specifically expressed during seed development, mainly at 15 DPF. Also, ∼12,000 genes showed significant differential expression at 30, 45, and/or 60 DPF within each of the three peanut accessions, accounting for 31.8–34.1% of the total expressed genes. Using a method that combined comprehensive transcriptome analysis and previously mapped QTLs, we identified several candidate genes that encode transcription factor TGA7, topless-related protein 2, IAA-amino acid hydrolase ILR1-like 5, and putative pentatricopeptide repeat-containing (PPR) protein. Based on sequence variations identified in these genes, SNP markers were developed and used to genotype both 30 peanut landraces and a genetic segregated population, implying that EVM0025654 encoding a PPR protein may be associated with the increased seed size/weight of the cultivated accessions in comparison with the allotetraploid wild peanut. Our results provide additional knowledge for the identification and functional research into candidate genes responsible for the seed size/weight phenotype in peanut.

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The DYW-subgroup pentatricopeptide repeat protein PPR27 interacts with ZmMORF1 to facilitate mitochondrial RNA editing and seed development in maize

Journal of Experimental Botany ◽

10.1093/jxb/eraa273 ◽

2020 ◽

Vol 71 (18) ◽

pp. 5495-5505 ◽

Cited By ~ 1

Author(s):

Rui Liu ◽

Shi-Kai Cao ◽

Aqib Sayyed ◽

Huan-Huan Yang ◽

Jiao Zhao ◽

...

Keyword(s):

Rna Editing ◽

Seed Development ◽

Plant Mitochondria ◽

Endosperm Development ◽

Complex Iii ◽

Mitochondrial Rna ◽

Mitochondrial Complex ◽

Pentatricopeptide Repeat ◽

Ppr Protein ◽

Ppr Proteins

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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E+ subgroup PPR protein defective kernel 36 is required for multiple mitochondrial transcripts editing and seed development in maize and Arabidopsis

New Phytologist ◽

10.1111/nph.14507 ◽

2017 ◽

Vol 214 (4) ◽

pp. 1563-1578 ◽

Cited By ~ 32

Author(s):

Gang Wang ◽

Mingyu Zhong ◽

Bilian Shuai ◽

Jiandong Song ◽

Jie Zhang ◽

...

Keyword(s):

Seed Development ◽

Ppr Protein ◽

Mitochondrial Transcripts

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Emp10encodes a mitochondrial PPR protein that affects thecis-splicing ofnad2intron 1 and seed development in maize

The Plant Journal ◽

10.1111/tpj.13551 ◽

2017 ◽

Vol 91 (1) ◽

pp. 132-144 ◽

Cited By ~ 45

Author(s):

Manjun Cai ◽

Shuzhen Li ◽

Feng Sun ◽

Qin Sun ◽

Hailiang Zhao ◽

...

Keyword(s):

Seed Development ◽

Ppr Protein

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The PPR protein SLOW GROWTH 4 is involved in editing of nad4 and affects the splicing of nad2 intron 1

Plant Molecular Biology ◽

10.1007/s11103-016-0566-4 ◽

2016 ◽

Vol 93 (4-5) ◽

pp. 355-368 ◽

Cited By ~ 20

Author(s):

Stefan Weißenberger ◽

Jürgen Soll ◽

Chris Carrie

Keyword(s):

Slow Growth ◽

Ppr Protein ◽

Intron 1

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MISF2 Encodes an Essential Mitochondrial Splicing Co-factor Required for nad2 mRNA Processing and Embryo Development in Arabidopsis thaliana

10.20944/preprints202201.0113.v1 ◽

2022 ◽

Author(s):

Tan-Trung Nguyen ◽

Corinne Best ◽

Sofia Shevtsov ◽

Michal Zmudjak ◽

Martine Quadrado ◽

...

Keyword(s):

Gene Expression ◽

Embryo Development ◽

Mitochondrial Gene ◽

Orthologous Gene ◽

Early Embryo ◽

Pentatricopeptide Repeat ◽

Ppr Protein ◽

Intron 1 ◽

Ppr Proteins ◽

Plant Embryo

Mitochondria play key roles in cellular energy metabolism in eukaryotes. Mitochondria of most organisms contain their own genome and specific transcription and translation machineries. The expression of angiosperm mtDNA involves extensive RNA-processing steps, such as RNA trimming, editing, and the splicing of numerous group II-type introns. Pentatricopeptide repeat (PPR) proteins are key players of plant organelle gene expression and RNA metabolism. In the present analysis, we reveal the function of the MITOCHONDRIAL SPLICING FACTOR 2 gene (MISF2, AT3G22670) and show that it encodes a mitochondria-localized PPR protein that is crucial for early embryo-development in Arabidopsis. Molecular characterization of embryo-rescued misf2 plantlets indicates that the splicing of nad2 intron 1 and thus respiratory complex I biogenesis are strongly compromised. Moreover, the molecular function seems conserved between MISF2 protein in Arabidopsis and its orthologous gene (EMP10) in maize, suggesting that the ancestor of MISF2/EMP10 was recruited to function in nad2 processing before the monocot-dicot divergence, ~200 million years ago. These data provide new insights into the function of nuclear-encoded factors in mitochondrial gene expression and respiratory chain biogenesis during plant embryo development.

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