Mitochondria-Associated Pyruvate Kinase Complexes Regulate Grain Filling in Rice

Li, Hu; Tu, Bin; Yang, Wen; Yuan, Hua; Li, Jialian; Guo, Lianan; Zheng, Ling; Chen, Weilan; Zhu, Xiaobo; Wang, Yuping; Qin, Peng; Ma, Bo; Li, Shigui

doi:10.1104/pp.20.00279

Cited by 35 publications

(20 citation statements)

References 45 publications

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“…OsPK2/PKpα1 affects starch compound granule formation, starch synthesis, grain filling, and the germination rates of seeds after 1 year of storage ( Cai et al ., 2018 a , b ). The OsPK3-OsPK1/OsPK4 complexes, which are two mitochondria-associated PK complexes, are involved in the regulation of grain filling via the stage-specific fine-tuning of sucrose translocation ( Hu et al , 2020 ). In this study, the disruption of OsPK5 resulted in slow germination and seedling growth during seed germination ( Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies showed that ospkpa1 grains were characterized by a marked decrease in the sugar content during seed development in rice ( Cai et al , 2018 b ). Soluble sugar accumulation is also greatly decreased in developing ospk3 seeds in rice ( Hu et al , 2020 ). Conversely, the accumulation of sugar is observed in developing and germinating seeds of Arabidopsis pkp1 ( Andre et al , 2007 ; Andre and Benning, 2007 ).…”

Section: Discussionmentioning

confidence: 99%

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Identification of OsPK5 involved in rice glycolytic metabolism and GA/ABA balance for improving seed germination via genome-wide association study

Yang

Chen

Zhan

et al. 2022

Journal of Experimental Botany

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Seed germination plays a pivotal role in the plant life cycle, and its precise regulatory mechanisms are not clear. In this study, 19 QTLs associated with seed germination were identified through genome-wide association studies (GWASs) of the following traits in 2016 and 2017: germination rate (GR) at 3, 5, and 7 days after imbibition (DAI) and germination index (GI). Two major stable QTLs, qSG4 and qSG11.1, were found to be associated with GR and GI over two continuous years. Furthermore, the OsPK5 gene, encoding a pyruvate kinase, was shown to be a crucial regulator of seed germination in rice and might be a causal gene of the key QTL qSG11.1, on chromosome 11. Natural variation in OsPK5 function altered the activity of pyruvate kinase. The disruption of OsPK5 function resulted in slow germination and seedling growth during seed germination. The disruption of OsPK5 blocked glycolytic metabolism, caused glucose accumulation, decreased energy levels, and affected the GA/ABA balance. Taken together, our results provide novel insights into the roles of OsPK5 in seed germination and facilitate its application in rice breeding to improve seed vigor.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Identification of OsPK5 involved in rice glycolytic metabolism and GA/ABA balance for improving seed germination via genome-wide association study

Yang

Chen

Zhan

et al. 2022

Journal of Experimental Botany

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“…And this could alter the endosperm metabolism, causing chalkiness formation due to the poor accumulation of storage compounds. In the previous study, the source-limitation was considered a key reason for chalkiness formation, reflected by the insufficiency of nutrients from photosynthetic organs, such as leaves that begins to decrease in the biosynthesis ability of storage compounds (starch and proteins) in the endosperm ( Wang et al, 2008 ; Hu et al, 2020 ). In the present study, we uncovered the mechanism of chalky endosperm formation from the perspective of the embryo–endosperm interaction, showing that the chalky endosperm formation is not only caused by source limitation, but also by nutrient competition between the embryo and the endosperm.…”

Section: Discussionmentioning

confidence: 99%

Metabolic Disturbance Induced by the Embryo Contributes to the Formation of Chalky Endosperm of a Notched-Belly Rice Mutant

Tao

Din

et al. 2022

Front. Plant Sci.

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Grain chalkiness is a key quality trait of the rice grain, whereas its underlying mechanism is still not thoroughly understood because of the complex genetic and environmental interactions. We identified a notched-belly (NB) mutant that has a notched-line on the belly of grains. The line dissects the endosperm into two distinct parts, the upper translucent part, and the bottom chalky part in the vicinity of the embryo. Using this mutant, our previous studies clued the negative influence of embryo on the biochemical makeup of the endosperm, suggesting the need for the in-depth study of the embryo effect on the metabolome of developing endosperm. This study continued to use the NB mutant to evolve a novel comparison method to clarify the role of embryo in the formation of a chalky endosperm. Grain samples of the wild-type (WT) and NB were harvested at 10, 20, and 30 days after fertilization (DAF), and then divided into subsamples of the embryo, the upper endosperm, and the bottom endosperm. Using non-targeted metabolomics and whole-genome RNA sequencing (RNA-seq), a nearly complete catalog of expressed metabolites and genes was generated. Results showed that the embryo impaired the storage of sucrose, amino acid, starch, and storage proteins in the bottom endosperm of NB by enhancing the expression of sugar, amino acids, and peptide transporters, and declining the expression of starch, prolamin, and glutelin synthesis-related genes. Importantly, the competitive advantage of the developing embryo in extracting the nutrients from the endosperm, transformed the bottom endosperm into an “exhaustive source” by diverting the carbon (C) and nitrogen (N) metabolism from synthetic storage to secondary pathways, resulting in impaired filling of the bottom endosperm and subsequently the formation of chalky tissue. In summary, this study reveals that embryo-induced metabolic shift in the endosperm is associated with the occurrence of grain chalkiness, which is of relevance to the development of high-quality rice by balancing the embryo–endosperm interaction.

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“…Through reversible acetylation, succinylation and phosphorylation, the activities of metabolic enzymes are strictly regulated to maintain the equilibrium of substrates and products, including the intermediate acetyl-CoA, succinyl-CoA and ATP molecules. As a link between glycolysis and the citrate cycle, PK catalyzes the transformation of phosphoenolpyruvate to pyruvate, which enters the mitochondrion to generate acetyl-CoA [ 54 ]. By contrast, AGPase catalyzes the formation of ADP-glucose by consuming ATP molecules [ 55 ].…”

Section: Discussionmentioning

confidence: 99%

Proteome-wide analyses reveal diverse functions of protein acetylation and succinylation modifications in fast growing stolons of bermudagrass (Cynodon dactylon L.)

et al. 2022

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Background Bermudagrass (Cynodon dactylon L.) is an important warm-season turfgrass species with well-developed stolons, which lay the foundation for the fast propagation of bermudagrass plants through asexual clonal growth. However, the growth and development of bermudagrass stolons are still poorly understood at the molecular level. Results In this study, we comprehensively analyzed the acetylation and succinylation modifications of proteins in fast-growing stolons of the bermudagrass cultivar Yangjiang. A total of 4657 lysine acetylation sites on 1914 proteins and 226 lysine succinylation sites on 128 proteins were successfully identified using liquid chromatography coupled to tandem mass spectrometry, respectively. Furthermore, 78 proteins and 81 lysine sites were found to be both acetylated and succinylated. Functional enrichment analysis revealed that acetylated proteins regulate diverse reactions of carbohydrate metabolism and protein turnover, whereas succinylated proteins mainly regulate the citrate cycle. These results partly explained the different growth disturbances of bermudagrass stolons under treatment with sodium butyrate and sodium malonate, which interfere with protein acetylation and succinylation, respectively. Moreover, 140 acetylated proteins and 42 succinylated proteins were further characterized having similarly modified orthologs in other grass species. Site-specific mutations combined with enzymatic activity assays indicated that the conserved acetylation of catalase and succinylation of malate dehydrogenase both inhibited their activities, further implying important regulatory roles of the two modifications. Conclusion In summary, our study implied that lysine acetylation and succinylation of proteins possibly play important regulatory roles in the fast growth of bermudagrass stolons. The results not only provide new insights into clonal growth of bermudagrass but also offer a rich resource for functional analyses of protein lysine acetylation and succinylation in plants.

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Mitochondria-Associated Pyruvate Kinase Complexes Regulate Grain Filling in Rice

Cited by 35 publications

References 45 publications

Identification of OsPK5 involved in rice glycolytic metabolism and GA/ABA balance for improving seed germination via genome-wide association study

Identification of OsPK5 involved in rice glycolytic metabolism and GA/ABA balance for improving seed germination via genome-wide association study

Metabolic Disturbance Induced by the Embryo Contributes to the Formation of Chalky Endosperm of a Notched-Belly Rice Mutant

Proteome-wide analyses reveal diverse functions of protein acetylation and succinylation modifications in fast growing stolons of bermudagrass (Cynodon dactylon L.)

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