Combined Transcript and Metabolite Profiling of Arabidopsis Leaves Reveals Fundamental Effects of the Thiol-Disulfide Status on Plant Metabolism1(W)(OA) (original) (raw)
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Frontiers in plant science, 2013
Glutathione is a small redox-active molecule existing in two main stable forms: the thiol (GSH) and the disulphide (GSSG). In plants growing in optimal conditions, the GSH:GSSG ratio is high in most cell compartments. Challenging environmental conditions are known to alter this ratio, notably by inducing the accumulation of GSSG, an effect that may be influential in the perception or transduction of stress signals. Despite the potential importance of glutathione status in redox signaling, the reactions responsible for the oxidation of GSH to GSSG have not been clearly identified. Most attention has focused on the ascorbate-glutathione pathway, but several other candidate pathways may couple the availability of oxidants such as H2O2 to changes in glutathione and thus impact on signaling pathways through regulation of protein thiol-disulfide status. We provide an overview of the main candidate pathways and discuss the available biochemical, transcriptomic, and genetic evidence relating to each. Our analysis emphasizes how much is still to be elucidated on this question, which is likely important for a full understanding of how stress-related redox regulation might impinge on phytohormone-related and other signaling pathways in plants.
PLANT PHYSIOLOGY, 2005
Sulfur is an essential macroelement in plant and animal nutrition. Plants assimilate inorganic sulfate into two sulfur-containing amino acids, cysteine and methionine. Low supply of sulfate leads to decreased sulfur pools within plant tissues. As sulfurrelated metabolites represent an integral part of plant metabolism with multiple interactions, sulfur deficiency stress induces a number of adaptive responses, which must be coordinated. To reveal the coordinating network of adaptations to sulfur deficiency, metabolite profiling of Arabidopsis has been undertaken. Gas chromatography-mass spectrometry and liquid chromatography-mass spectrometry techniques revealed the response patterns of 6,023 peaks of nonredundant ion traces and relative concentration levels of 134 nonredundant compounds of known chemical structure. Here, we provide a catalogue of the detected metabolic changes and reconstruct the coordinating network of their mutual influences. The observed decrease in biomass, as well as in levels of proteins, chlorophylls, and total RNA, gives evidence for a general reduction of metabolic activity under conditions of depleted sulfur supply. This is achieved by a systemic adjustment of metabolism involving the major metabolic pathways. Sulfur/carbon/nitrogen are partitioned by accumulation of metabolites along the pathway O-acetylserine to serine to glycine, and are further channeled together with the nitrogen-rich compound glutamine into allantoin. Mutual influences between sulfur assimilation, nitrogen imbalance, lipid breakdown, purine metabolism, and enhanced photorespiration associated with sulfur-deficiency stress are revealed in this study. These responses may be assembled into a global scheme of metabolic regulation induced by sulfur nutritional stress, which optimizes resources for seed production.
Plants
Sulfur plays a vital role in the primary and secondary metabolism of plants, and carries an important function in a large number of different compounds. Despite this importance, compared to other mineral nutrients, relatively little is known about sulfur sensing and signalling, as well as about the mechanisms controlling sulfur metabolism and homeostasis. Sulfur contents in plants vary largely not only among different species, but also among accessions of the same species. We previously used associative transcriptomics to identify several genes potentially controlling variation in sulfate content in the leaves of Brassica napus, including an OASC gene for mitochondrial O-acetylserine thiollyase (OAS-TL), an enzyme involved in cysteine synthesis. Here, we show that loss of OASC in Arabidopsis thaliana lowers not only sulfate, but also glutathione levels in the leaves. The reduced accumulation is caused by lower sulfate uptake and translocation to the shoots; however, the flux through...
2004
Plant metabolism is a complex set of processes that produce a wide diversity of foods, woods, and medicines. With the genome sequences of Arabidopsis and rice in hands, postgenomics studies integrating all ''omics'' sciences can depict precise pictures of a whole-cellular process. Here, we present, to our knowledge, the first report of investigation for gene-to-metabolite networks regulating sulfur and nitrogen nutrition and secondary metabolism in Arabidopsis, with integration of metabolomics and transcriptomics. Transcriptome and metabolome analyses were carried out, respectively, with DNA macroarray and several chemical analytical methods, including ultra high-resolution Fourier transform-ion cyclotron MS. Mathematical analyses, including principal component analysis and batch-learning self-organizing map analysis of transcriptome and metabolome data suggested the presence of general responses to sulfur and nitrogen deficiencies. In addition, specific responses to either sulfur or nitrogen deficiency were observed in several metabolic pathways: in particular, the genes and metabolites involved in glucosinolate metabolism were shown to be coordinately modulated. Understanding such geneto-metabolite networks in primary and secondary metabolism through integration of transcriptomics and metabolomics can lead to identification of gene function and subsequent improvement of production of useful compounds in plants.
Proceedings of The National Academy of Sciences - PNAS, 2004
Plant metabolism is a complex set of processes that produce a wide diversity of foods, woods, and medicines. With the genome sequences of Arabidopsis and rice in hands, postgenomics studies integrating all "omics" sciences can depict precise pictures of a whole-cellular process. Here, we present, to our knowledge, the first report of investigation for gene-to-metabolite networks regulating sulfur and nitrogen nutrition and secondary metabolism in Arabidopsis, with integration of metabolomics and transcriptomics. Transcriptome and metabolome analyses were carried out, respectively, with DNA macroarray and several chemical analytical methods, including ultra high-resolution Fourier transform-ion cyclotron MS. Mathematical analyses, including principal component analysis and batch-learning self-organizing map analysis of transcriptome and metabolome data suggested the presence of general responses to sulfur and nitrogen deficiencies. In addition, specific responses to either ...
From sulfur to homoglutathione: thiol metabolism in soybean
Amino Acids, 2010
Sulfur is an essential plant nutrient and is metabolized into the sulfur-containing amino acids (cysteine and methionine) and into molecules that protect plants against oxidative and environmental stresses. Although studies of thiol metabolism in the model plant Arabidopsis thaliana (thale cress) have expanded our understanding of these dynamic processes, our knowledge of how sulfur is assimilated and metabolized in crop plants, such as soybean (Glycine max), remains limited in comparison. Soybean is a major crop used worldwide for food and animal feed. Although soybeans are protein-rich, they do not contain high levels of the sulfur-containing amino acids, cysteine and methionine. Ultimately, unraveling the fundamental steps and regulation of thiol metabolism in soybean is important for optimizing crop yield and quality. Here we review the pathways from sulfur uptake to glutathione and homoglutathione synthesis in soybean, the potential biotechnology benefits of understanding and modifying these pathways, and how information from the soybean genome may guide the next steps in exploring this biochemical system.
The role of thiols in plant adaptation to environmental stress
Thiols (-SH groups) are the main form of reduced sulphur in plants present as protein thiols (Cys residues) or low molecular weight thiols, the most prominent is the tripeptide glutathione (GSH). Due to the redox properties of the thiol groups these compounds play important roles in stress responses of plants, since stress is nearly always associated with an enhanced formation of reactive oxygen species (ROS). Because of its antioxidative properties, GSH is directly involved in protection of cells from ROS damage and in regeneration of oxidized substrates. GSH is kept in the active reduced state by glutathione reductase (GR). In the following chapter, responses of GSH and GR system to natural abiotic stresses (drought, low and high temperatures, high light, UV, salinity, anoxia), biotic stresses (pathogen infection), and air pollution impact are discussed. The reviewed results show that plant resistance to stress is commonly correlated with increased GSH contents and GR activities. Damage to plant tissues is often marked by a breakdown of the GSH system. Besides its role as protectant, GSH is thought to play a role in cellular signalling and stress sensing. Apart from GSH, small protein thiols (thioredoxins) are essential for the adjustment of metabolism to environmental conditions. Most recent results suggest that thioredoxins can be directly induced by ROS stress. The role of thiols in regulation of plant stress responses, e.g. by inducing defense enzymes and compounds, is discussed.
Journal of experimental botany, 2014
Understanding the dynamics of physiological process in the systems biology era requires approaches at the genome, transcriptome, proteome, and metabolome levels. In this context, metabolite flux experiments have been used in mapping metabolite pathways and analysing metabolic control. In the present review, sulphur metabolism was taken to illustrate current challenges of metabolic flux analyses. At the cellular level, restrictions in metabolite flux analyses originate from incomplete knowledge of the compartmentation network of metabolic pathways. Transport of metabolites through membranes is usually not considered in flux experiments but may be involved in controlling the whole pathway. Hence, steady-state and snapshot readings need to be expanded to time-course studies in combination with compartment-specific metabolite analyses. Because of species-specific differences, differences between tissues, and stress-related responses, the quantitative significance of different sulphur si...
Journal of Biotechnology, 2007
Redox regulation is a central control element in cell metabolism. It is employed to adjust photosynthesis and the antioxidant defence system of leaves to the prevailing environment. During recent years progress has been made in describing the redoxdependent alterations in metabolism, the thiol/disulfide proteome, the redox-dependent and cross-talking signalling pathways and the target genes of redox regulation. Some transcription factors have been identified as proteins that perform thiol/disulfide transitions linked to the redox-regulation of specific plant promoters. In addition first mathematical models have been designed to simulate antioxidant defence and predict its response. Taken together, a profound experimental data set has been generated which allows to approach a systems biology type of understanding of antioxidant defence in photosynthesising cells in the near future. Since oxidative stress is likely to limit plant growth under stress, such a systematic understanding of antioxidant defence will help to define novel targets for breeding stress-tolerant plants.
Theoretical and Experimental Plant Physiology, 2018
Plant secondary metabolism consists of highly complex pathways by the fact that its structures and levels are largely divergent between different tissues, growth stages, species and environmental conditions. The metabolomics of plant secondary metabolism has been developed for both functional genomics and analysis of physiological processes via multi-platform metabolite profiling as well as integration analysis with other omics data. Whilst recent efforts and significant technological advances of mass spectrometry have solved common analytical problems of metabolite detection at higher sensitivity, the challenge of improving (i) the coverage of detected compounds and (ii) peak annotation to enable functional genomics approach still persists. Here, we review progress made following this approach with research examples and strategies of gene functional analyses in plant species. Taken together, these examples prove that the current strategy of metabolomics focusing on plant secondary metabolism via integration with genetics and transcriptomics is a highly effective tool to understand the function and regulation of metabolic complexity in plants.