The nuclear-localized PPR protein OsNPPR1 is important for mitochondrial function and endosperm development in rice

Hao, Yuanyuan; Wang, Yunlong; Wu, Meiqing; Zhu, Xiangzhen; Teng, Xuan; Sun, Yinglun; Zhu, Jianqing; Zhang, Yuanyan; Jing, Ruonan; Lei, Jie; Li, Jingfang; Bao, Xiuhao; Wang, Chunming; Wang, Yihua

doi:10.1093/jxb/erz226

Cited by 47 publications

(38 citation statements)

References 88 publications

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“…Although the large PPR family is widely distributed among plants, only a small number of PPR proteins have been characterized. The majority of PPR proteins contain chloroplast-or mitochondrion-targeting peptides (Lurin et al 2004), and some contain nucleus-targeting peptides (Ding et al 2006;Hao et al 2019). PPR proteins commonly participate in RNA metabolism in organelles or the nucleus, and are essential for normal plant growth and development.…”

Section: Transcript Levels Of Chloroplast Ribosomal Rnas and Chloropmentioning

confidence: 99%

“…The chloroplast-localized OsPGL12 is mainly involved in the intron splicing of ndhA in chloroplasts (Chen et al 2019). The mitochondrion-localized OsFLO10 is mainly involved in the trans-splicing of the nad1 intron 1 in mitochondria (Wu et al 2019), and the nucleus-localized OsNPPR1 was reported to be involved in the intron splicing of a small number of nuclearlocalized genes, many of which are mitochondrionlocalized (Hao et al 2019). The chloroplast-localized and/or mitochondrion-localized PPR proteins, such as OsPPR1 (Gothandam et al 2005), OsOTP51, OsPPR4, OsWSL, OsALS3 (Lin et al 2015a), OspTAC2 (Wang et al 2016a), OsPPR6 (Tang et al 2017), OsSLA4, OsWSL5 and OsPGL12, are essential for early chloroplast development in rice at the seedling stage.…”

Section: Introductionmentioning

confidence: 99%

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OsSLC1 Encodes a Pentatricopeptide Repeat Protein Essential for Early Chloroplast Development and Seedling Survival

Shang

Chen

et al. 2020

Rice

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Background: The large family of pentatricopeptide repeat (PPR) proteins is widely distributed among land plants. Such proteins play vital roles in intron splicing, RNA editing, RNA processing, RNA stability and RNA translation. However, only a small number of PPR genes have been identified in rice. Results: In this study, we raised a mutant from tissue-culture-derived plants of Oryza sativa subsp. japonica 'Zhonghua 11', which exhibited a lethal chlorosis phenotype from germination to the third-leaf stage. The mutant was designated seedling-lethal chlorosis 1 (slc1). The slc1 mutant leaves showed extremely low contents of photosynthetic pigments and abnormal chloroplast development, and were severely defective in photosynthesis. Map-based cloning of OsSLC1 revealed that a single base (G) deletion was detected in the first exon of Os06g0710800 in the slc1 mutant, which caused a premature stop codon. Knockout and complementation experiments further confirmed that OsSLC1 is responsible for the seedling-lethal chlorosis phenotype in the slc1 mutant. OsSLC1 was preferentially expressed in green leaves, and encoded a chloroplast-localized PPR protein harboring 12 PPR motifs. Loss-of-function of OsSLC1 affected the intron splicing of multiple group II introns, and especially precluded the intron splicing of rps16, and resulted in significant increase in the transcript levels of 3 chloroplast ribosomal RNAs and 16 chloroplast development-related and photosynthesis-related genes, and in significant reduction in the transcript levels of 1 chloroplast ribosomal RNAs and 2 chloroplast development-related and photosynthesis-related genes. Conclusion: We characterized a novel chloroplast-localized PPR protein, OsSLC1, which plays a vital role in the intron splicing of multiple group II introns, especially the rps16 intron, and is essential for early chloroplast development and seedling survival in rice.

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Section: Transcript Levels Of Chloroplast Ribosomal Rnas and Chloropmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

OsSLC1 Encodes a Pentatricopeptide Repeat Protein Essential for Early Chloroplast Development and Seedling Survival

Shang

Chen

et al. 2020

Rice

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“…We found that most PPR genes showed preferential accumulation in leaves compared to other tissues, which were likely to be responsible for their subcellular localization, and most reported PPR proteins were located in mitochondria or chloroplast. A relatively high expression level was revealed in seeds, suggesting that they have potential function in seed development, which has been reported to be involved in endosperm development [14]. As shown in Figure 9, Glyma.11G008800, Glyma.13G220400 and Glyma.15G192000 showed extremely high expression in roots and root hairs, indicating that the DYW subgroup PPR genes may play specific roles in responding to drought stress.…”

Section: Resultsmentioning

confidence: 86%

“…It was reported that the nuclear OsNPPR1 encoded a PPR protein, which was involved in the Regulation of mitochondrial development and endosperm development. The mutant named fgr1 exhibited a lower content of starch and delayed seedling growth [14]. Rice PPS1 encodes a DYW motif-containing PPR protein, which is important for C-to-U RNA editing of nad3 transcripts.…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Analysis of the DYW Subgroup PPR Gene Family and Identification of GmPPR4 Responses to Drought Stress

Song

et al. 2019

IJMS

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Pentatricopeptide-repeat (PPR) proteins were identified as a type of nucleus coding protein that is composed of multiple tandem repeats. It has been reported that PPR genes play an important role in RNA editing, plant growth and development, and abiotic stresses in plants. However, the functions of PPR proteins remain largely unknown in soybean. In this study, 179 DYW subgroup PPR genes were identified in soybean genome (Glycine max Wm82.a2.v1). Chromosomal location analysis indicated that DYW subgroup PPR genes were mapped to all 20 chromosomes. Phylogenetic relationship analysis revealed that DYW subgroup PPR genes were categorized into three distinct Clusters (I to III). Gene structure analysis showed that most PPR genes were featured by a lack of intron. Gene duplication analysis demonstrated 30 PPR genes (15 pairs; ~35.7%) were segmentally duplicated among Cluster I PPR genes. Furthermore, we validated the mRNA expression of three genes that were highly up-regulated in soybean drought- and salt-induced transcriptome database and found that the expression levels of GmPPR4 were induced under salt and drought stresses. Under drought stress condition, GmPPR4-overexpressing (GmPPR4-OE) plants showed delayed leaf rolling; higher content of proline (Pro); and lower contents of H2O2, O2− and malondialdehyde (MDA) compared with the empty vector (EV)-control plants. GmPPR4-OE plants exhibited increased transcripts of several drought-inducible genes compared with EV-control plants. Our results provided a comprehensive analysis of the DYW subgroup PPR genes and an insight for improving the drought tolerance in soybean.

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“…PPR proteins have been found to exhibit RNA-binding properties, which facilitate in mediating gene expression through posttranscriptional processes associated with transcripts in the mitochondria, chloroplast, and nucleus. Thus, PPR genes are thought to have a major impact on organelle stability, including biogenesis, and function through their involvement in various posttranscriptional processes such as RNA-editing [ 1 , 8 ], RNA-splicing [ 9 ], and RNA-processing [ 10 ].…”

Section: Introductionmentioning

confidence: 99%

A Genome-Wide Analysis of the Pentatricopeptide Repeat (PPR) Gene Family and PPR-Derived Markers for Flesh Color in Watermelon (Citrullus lanatus)

Subburaj

Lee

et al. 2020

Genes

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Watermelon (Citrullus lanatus) is an economically important fruit crop grown for consumption of its large edible fruit flesh. Pentatricopeptide-repeat (PPR) encoding genes, one of the large gene families in plants, are important RNA-binding proteins involved in the regulation of plant growth and development by influencing the expression of organellar mRNA transcripts. However, systematic information regarding the PPR gene family in watermelon remains largely unknown. In this comprehensive study, we identified and characterized a total of 422 C. lanatus PPR (ClaPPR) genes in the watermelon genome. Most ClaPPRs were intronless and were mapped across 12 chromosomes. Phylogenetic analysis showed that ClaPPR proteins could be divided into P and PLS subfamilies. Gene duplication analysis suggested that 11 pairs of segmentally duplicated genes existed. In-silico expression pattern analysis demonstrated that ClaPPRs may participate in the regulation of fruit development and ripening processes. Genotyping of 70 lines using 4 single nucleotide polymorphisms (SNPs) from 4 ClaPPRs resulted in match rates of over 0.87 for each validated SNPs in correlation with the unique phenotypes of flesh color, and could be used in differentiating red, yellow, or orange watermelons in breeding programs. Our results provide significant insights for a comprehensive understanding of PPR genes and recommend further studies on their roles in watermelon fruit growth and ripening, which could be utilized for cultivar development of watermelon.

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The nuclear-localized PPR protein OsNPPR1 is important for mitochondrial function and endosperm development in rice

Cited by 47 publications

References 88 publications

OsSLC1 Encodes a Pentatricopeptide Repeat Protein Essential for Early Chloroplast Development and Seedling Survival

OsSLC1 Encodes a Pentatricopeptide Repeat Protein Essential for Early Chloroplast Development and Seedling Survival

Genome-Wide Analysis of the DYW Subgroup PPR Gene Family and Identification of GmPPR4 Responses to Drought Stress

A Genome-Wide Analysis of the Pentatricopeptide Repeat (PPR) Gene Family and PPR-Derived Markers for Flesh Color in Watermelon (Citrullus lanatus)

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