Loss of Cytosolic Phosphoglucose Isomerase Affects Carbohydrate Metabolism in Leaves and Is Essential for Fertility of Arabidopsis

Kunz, Hans‐Henning; Zamani-Nour, Shirin; Häusler, Rainer E.; Ludewig, Katja; Schroeder, Julian I.; Malinova, Irina; Fettke, Joerg; Flügge, Ulf Ingo; Gierth, Markus

doi:10.1104/pp.114.241091

Cited by 37 publications

(41 citation statements)

References 75 publications

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“…Plastid and cytosolic PGI activity are controlled by different genes (Kunz et al, 2014). We detected a cis-QTL for cPGI activity at SIS/AT5G42740.…”

Section: Cis-qtl In Structural Genes Encoding For Enzymesmentioning

confidence: 88%

Genome-Wide Association Mapping Reveals That Specific and Pleiotropic Regulatory Mechanisms Fine-Tune Central Metabolism and Growth in Arabidopsis

et al. 2017

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ORCID IDs: 0000-0001-6809-0266 (C.M.F.); 0000-0001-8593-1741 (M.G.A.); 0000-0002-6113-9570 (R.S.); 0000-0002-4900-1763 (M.S.); 0000-0001-8918-0711 (J.J.B.K.)Central metabolism is a coordinated network that is regulated at multiple levels by resource availability and by environmental and developmental cues. Its genetic architecture has been investigated by mapping metabolite quantitative trait loci (QTL). A more direct approach is to identify enzyme activity QTL, which distinguishes between cis-QTL in structural genes encoding enzymes and regulatory trans-QTL. Using genome-wide association studies, we mapped QTL for 24 enzyme activities, nine metabolites, three structural components, and biomass in Arabidopsis thaliana. We detected strong cis-QTL for five enzyme activities. A cis-QTL for UDP-glucose pyrophosphorylase activity in the UGP1 promoter is maintained through balancing selection. Variation in acid invertase activity reflects multiple evolutionary events in the promoter and coding region of VAC-INV. cis-QTL were also detected for ADP-glucose pyrophosphorylase, fumarase, and phosphoglucose isomerase activity. We detected many trans-QTL, including transcription factors, E3 ligases, protein targeting components, and protein kinases, and validated some by knockout analysis. trans-QTL are more frequent but tend to have smaller individual effects than cis-QTL. We detected many colocalized QTL, including a multitrait QTL on chromosome 4 that affects six enzyme activities, three metabolites, protein, and biomass. These traits are coordinately modified by different ACCELERATED CELL DEATH6 alleles, revealing a trade-off between metabolism and defense against biotic stress.

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“…Plastid and cytosolic PGI activity are controlled by different genes (Kunz et al, 2014). We detected a cis-QTL for cPGI activity at SIS/AT5G42740.…”

Section: Cis-qtl In Structural Genes Encoding For Enzymesmentioning

confidence: 88%

Genome-Wide Association Mapping Reveals That Specific and Pleiotropic Regulatory Mechanisms Fine-Tune Central Metabolism and Growth in Arabidopsis

et al. 2017

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“…Subsequently CTPS genes were cloned into either N-or C-terminal frame with Venus (YFP) via indicated restriction sites. The binary plasmid used for in planta expression were pBARII_UT_mVenusN vector in the case of N-terminal translational YFP fusions (Waadt et al, 2015) or for C-terminal translational YFP fusions pHygII_UT_mVenusC (Kunz et al, 2014). YFP fusion constructs were then transformed into Agrobacterium tumefaciens strain GV3101.…”

Section: Cloning Of Ctpssmentioning

confidence: 99%

Characterization of filament‐forming CTP synthases from Arabidopsis thaliana

et al. 2018

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Cytidine triphosphate (CTP) is essential for DNA, RNA and phospholipid biosynthesis. De novo synthesis is catalyzed by CTP synthases (CTPS). Arabidopsis encodes five CTPS isoforms that unanimously share conserved motifs found across kingdoms, suggesting all five are functional enzymes. Whereas CTPS1-4 are expressed throughout Arabidopsis tissues, CTPS5 reveals exclusive expression in developing embryos. CTPS activity and substrates affinities were determined for a representative plant enzyme on purified recombinant CTPS3 protein. As demonstrated in model organisms such as yeast, fruit fly and mammals, CTPS show the capacity to assemble into large filaments called cytoophidia. Transient expression of N- and C-terminal YFP-CTPS fusion proteins in Nicotiana benthamiana allowed to monitor such filament formation. Interestingly, CTPS1 and 2 always appeared as soluble proteins, whereas filaments were observed for CTPS3, 4 and 5 independent of the YFP-tag location. However, when similar constructs were expressed in Saccharomyces cerevisiae, no filaments were observed, pointing to a requirement for organism-specific factors in vivo. Indications for filament assembly were also obtained in vitro when recombinant CTPS3 protein was incubated in the presence of CTP. T-DNA-insertion mutants in four CTPS loci revealed no apparent phenotypical alteration. In contrast, CTPS2 T-DNA-insertion mutants did not produce homozygous progenies. An initial characterization of the CTPS protein family members from Arabidopsis is presented. We provide evidence for their involvement in nucleotide de novo synthesis and show that only three of the five CTPS isoforms were able to form filamentous structures in the transient tobacco expression system. This represents a striking difference from previous observations in prokaryotes, yeast, Drosophila and mammalian cells. This finding will be highly valuable to further understand the role of filament formation to regulate CTPS activity.

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“…Thus, using knockout mutants and transgenic Arabidopsis plants, clear influences were observed of the cytosolic phosphoglucomutase [47] and the cytosolic phosphoglucoisomerase on growth and fertility as well as carbohydrate partitioning, including that between starch and sucrose [48]. Cytosolic glucose 1-phosphate should thus be regarded as an important metabolite for both the sucrose synthetic and the starch degradative pathway [10].…”

mentioning

confidence: 98%