Combined Transcript and Metabolite Profiling of Arabidopsis Leaves Reveals Fundamental Effects of the Thiol-Disulfide Status on Plant Metabolism

Kolbe, Anna; Oliver, Sandra N.; Fernie, Alisdair R.; Stitt, Mark; Dongen, Joost T. van; Geigenberger, Peter

doi:10.1104/pp.106.081208

Cited by 96 publications

(90 citation statements)

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“…These changes might be indicative of an increased mitochondrial metabolic rate in old5 mutants . Previously, it was shown that redox manipulation by DTT treatment of Arabidopsis leaves increases the level of succinate, malate, and oxaloacetate (Kolbe et al, 2006), suggesting that the changes in NAD/NADH levels may be the direct cause of the increase found in TCA cycle intermediates for the old5 mutant.…”

Section: Old5 Is Characterized By Increased Tricarboxylic Acid Cycle mentioning

confidence: 99%

TheArabidopsis onset of leaf death5Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing

et al. 2008

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Leaf senescence in Arabidopsis thaliana is a strict, genetically controlled nutrient recovery program, which typically progresses in an age-dependent manner. Leaves of the Arabidopsis onset of leaf death5 (old5) mutant exhibit early developmental senescence. Here, we show that OLD5 encodes quinolinate synthase (QS), a key enzyme in the de novo synthesis of NAD. The Arabidopsis QS was previously shown to carry a Cys desulfurase domain that stimulates reconstitution of the oxygen-sensitive Fe-S cluster that is required for QS activity. The old5 lesion in this enzyme does not affect QS activity but it decreases its Cys desulfurase activity and thereby the long-term catalytic competence of the enzyme. The old5 mutation causes increased NAD steady state levels that coincide with increased activity of enzymes in the NAD salvage pathway. NAD plays a key role in cellular redox reactions, including those of the tricarboxylic acid cycle. Broad-range metabolite profiling of the old5 mutant revealed that it contains higher levels of tricarboxylic acid cycle intermediates and nitrogen-containing amino acids. The mutant displays a higher respiration rate concomitant with increased expression of oxidative stress markers. We postulate that the alteration in the oxidative state is integrated into the plant developmental program, causing early ageing of the mutant.

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Section: Old5 Is Characterized By Increased Tricarboxylic Acid Cycle mentioning

confidence: 99%

TheArabidopsis onset of leaf death5Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing

et al. 2008

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“…Recent data suggest that upstream levels of regulation have moderate control over metabolic changes. For example, genes involved in redox regulation in Arabidopsis thaliana have quite stable expression whereas the corresponding fluxes and metabolite contents display marked genetic variations (27). Similarly, various studies on bacteria have shown that transcription is not sufficient to explain the variation of metabolic fluxes or phenotypes in Escherichia coli (28), Bacillus subtilis (29), CoFrom the ‡CNRS, UMR 0320/UMR 8120 Gé né tique Vé gé tale,…”

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Linking Post-Translational Modifications and Variation of Phenotypic Traits

Albertin

Marullo

Bely

et al. 2013

Molecular & Cellular Proteomics

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Enzymes can be post-translationally modified, leading to isoforms with different properties. The phenotypic consequences of the quantitative variability of isoforms have never been studied. We used quantitative proteomics to dissect the relationships between the abundances of the enzymes and isoforms of alcoholic fermentation, metabolic traits, and growth-related traits in Saccharomyces cerevisiae. Although the enzymatic pool allocated to the fermentation proteome was constant over the culture media and the strains considered, there was variation in abundance of individual enzymes and sometimes much more of their isoforms, which suggests the existence of selective constraints on total protein abundance and trade-offs between isoforms. Variations in abundance of some isoforms were significantly associated to metabolic traits and growth-related traits. In particular, cell size and maximum population size were highly correlated to the degree of N-terminal acetylation of the alcohol dehydrogenase. The fermentation proteome was found to be shaped by human selection, through the differential targeting of a few isoforms for each food-processing origin of strains. These results highlight the importance of posttranslational modifications in the diversity of metabolic and life-history traits. Molecular & Cellular Proteomics 12: 10.1074/mcp.M112.024349, 720 -735, 2013.The key problem in understanding genotype-phenotype relationships is the complexity arising from multiple levels of cellular functioning. Among them, metabolic networks involve series of interconnected chemical reactions catalyzed by enzymes, allowing the transformation of input substrates into intermediate or final metabolites. These networks play an essential role in an organism's growth, reproduction, and ability to maintain cell integrity and to respond to environmental changes (1, 2). The metabolic fluxes, as well as the metabolite concentrations, are governed by the activity of the enzymes, which depends on three types of factors: kinetic parameters, enzyme abundance, and activation state of the enzyme. The kinetic parameters are determined by the sequence and the three-dimensional structure of the protein (3). The abundance of the enzymes is the result of numerous molecular processes taking place from the transcriptional to the translational level, including epigenetic modifications of the DNA and chromatin (4), transcriptional regulation by transcription factors (5), mRNA capping and splicing and small RNA regulation (6), protein turnover (7), etc. The enzyme activation state is primarily because of post-translational modifications of the native protein, themselves highly regulated (8, 9). Other mechanisms involved in enzyme activity are proteinprotein interactions and allosteric regulation, such mechanisms being sometimes mediated through post-translational modifications (10, 11). The resulting isoforms can display differences in activity, affinity for partners (protein or effectors), and stability (12). The most studied modification is the reversibl...

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“…The change in the cytosolic redox and pH status by photosynthesis could override the effect of sugar on the expression of sugar-repressive nuclear genes (49). It is possible that enzymes in addition to nitrate reductase, which is regulated by post-translational modifications (3,50,51), are regulated not only by the metabolite levels but also by the conditions of the cell. Fritz et al recently showed that amino acids did not affect each other's level (48).…”

Section: Discussionmentioning

confidence: 99%

“…Hirai et al (1) described the linkage between the levels of some secondary metabolites, such as glucosinolates and the transcripts for genes encoding corresponding metabolic enzymes. However, such approaches for the primary metabolic pathway did not give us clear information on the regulatory systems, presumably due to higher complexity (1)(2)(3).…”

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“…The effects of the loss of chloroplast function on the metabolic pathways, however, have not been previously investigated. Analysis of extracts from albino plants by one-dimensional 1 H NMR revealed a unique metabolite profile, and detailed analysis by two-dimensional 13 C heteronuclear single quantum coherence (HSQC) 3 spectroscopy allowed the detection of dozens of metabolites, including amino acids. Our results indicate that the albino mutations substantially altered the metabolite profile.…”

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Top-down Phenomics of Arabidopsis thaliana

Tian

Chikayama

Tsuboi

et al. 2007

Journal of Biological Chemistry

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Elucidating the function of each gene in a genome is important for understanding the whole organism. We previously constructed 4000 disruptant mutants of Arabidopsis by insertion of Ds transposons. Here, we describe a top-down phenomics approach based on metabolic profiling that uses one-dimensional Plants produce energy sources, foods, and industrial or medical materials that are necessary and useful for us. It has been expected to handle the metabolic flows so as to increase the amount of interested chemical resources in plants. For that purpose, comprehensive understanding of the metabolite network is required. Presumably, the metabolite network is regulated by both genetic information and cellular conditions. In recent years, to address the key factors regulating the metabolite network, metabolomics, the nontargeting comprehensive metabolite analysis of plants, has been introduced in plant research as well as other organisms. To elucidate the linkage between genetic information and metabolites, attempts to integrate transcriptome and metabolomics data have been made. Hirai et al.(1) described the linkage between the levels of some secondary metabolites, such as glucosinolates and the transcripts for genes encoding corresponding metabolic enzymes. However, such approaches for the primary metabolic pathway did not give us clear information on the regulatory systems, presumably due to higher complexity (1-3).To understand such complex biological phenomena, a systems biological approach should be one of the promising ways. To establish systems biology, a vast amount of information on cellular entities, such as transcript, proteins, and metabolites is required and combined functionally. Computational models have been developed for Escherichia coli and Saccharomyces cerevisiae based on data from gene disruption mutants (4 -8) and have proven to be useful for predicting the phenotypes of mutants, cellular behavior, and evolution (9 -13).Completion of the Arabidopsis and rice genome sequences (14 -17) has allowed the application of systems biology to plants (18,19). Furthermore, a large number of gene disruption mutants have been constructed in various plant species, especially Arabidopsis and rice. By taking advantage of these resources, functional genomic approaches can be used to elucidate the function of plant genes (20). In a previous report, we described a phenomic approach analyzing the effects of 4000 gene disruptions in Arabidopsis (21). We found that fewer than 5% of the gene disruptions caused a visible phenotype in the aerial parts, suggesting that a more detailed and practical methodology is needed to determine the effects of losses in gene function.For the purpose of establishing systems biology in plants, we propose the comprehensive analysis of gene disruptant lines by

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Combined Transcript and Metabolite Profiling of Arabidopsis Leaves Reveals Fundamental Effects of the Thiol-Disulfide Status on Plant Metabolism

Cited by 96 publications

References 62 publications

TheArabidopsis onset of leaf death5Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing

TheArabidopsis onset of leaf death5Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing

Linking Post-Translational Modifications and Variation of Phenotypic Traits

Top-down Phenomics of Arabidopsis thaliana

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