Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism

Taniguchi, Masaru; Miyake, Hiroshi

doi:10.1016/j.pbi.2012.01.014

Cited by 107 publications

(90 citation statements)

References 50 publications

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“…In general, these studies reported small perturbations of photosynthesis in standard-grown aox1a plants, including slightly lower rates of CO 2 uptake or O 2 release (Gandin et al, 2012;Vishwakarma et al, 2014), slightly higher rates of cyclic electron transport (CET; Yoshida et al, 2011b), and slightly increased susceptibility to photoinhibition after a high light treatment (FlorezSarasa et al, 2011). Generally, these studies concluded that aox1a plants exhibit a biochemical limitation of photosynthesis, in line with the hypothesis that AOX serves as a sink for excess photogenerated reducing power, with the reductant likely reaching the mitochondrion via the malate valve (Noguchi and Yoshida, 2008;Taniguchi and Miyake, 2012). Similar to these Arabidopsis studies, we recently reported that well-watered N. tabacum AOX knockdowns grown at moderate irradiance display a slight reduced rate of photosynthesis (approximately 10%-15%) when measured at high irradiance.…”

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confidence: 82%

Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum

et al. 2014

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The mitochondrial electron transport chain includes an alternative oxidase (AOX) that is hypothesized to aid photosynthetic metabolism, perhaps by acting as an additional electron sink for photogenerated reductant or by dampening the generation of reactive oxygen species. Gas exchange, chlorophyll fluorescence, photosystem I (PSI) absorbance, and biochemical and protein analyses were used to compare respiration and photosynthesis of Nicotiana tabacum 'Petit Havana SR1' wild-type plants with that of transgenic AOX knockdown (RNA interference) and overexpression lines, under both well-watered and moderate droughtstressed conditions. During drought, AOX knockdown lines displayed a lower rate of respiration in the light than the wild type, as confirmed by two independent methods. Furthermore, CO 2 and light response curves indicated a nonstomatal limitation of photosynthesis in the knockdowns during drought, relative to the wild type. Also relative to the wild type, the knockdowns under drought maintained PSI and PSII in a more reduced redox state, showed greater regulated nonphotochemical energy quenching by PSII, and displayed a higher relative rate of cyclic electron transport around PSI. The origin of these differences may lie in the chloroplast ATP synthase amount, which declined dramatically in the knockdowns in response to drought. None of these effects were seen in plants overexpressing AOX. The results show that AOX is necessary to maintain mitochondrial respiration during moderate drought. In its absence, respiration rate slows and the lack of this electron sink feeds back on the photosynthetic apparatus, resulting in a loss of chloroplast ATP synthase that then limits photosynthetic capacity.

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confidence: 82%

Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum

et al. 2014

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“…By analyzing the flux distributions obtained at different light intensities, it was demonstrated that the roles of alternative pathways varied with light. The importance of mitochondria for energy rebalancing (Taniguchi and Miyake, 2012) was confirmed, with the alternative respiratory pathway becoming more important as light intensity increased. The analysis also highlighted the importance of chloroplastic energy-rebalancing mechanisms at high light in addition to the well-recognized cyclic electron flux and water-water cycle.…”

Section: Energy Metabolism In Photosynthetic Tissuesmentioning

confidence: 91%

“…One mechanism of rebalancing this ratio occurs within the photosynthetic electron transport chain itself: the flow of electrons can be reconfigured from a linear pathway between PSII and PSI to cyclic electron flow around PSI (Allen, 2003;Kramer and Evans, 2011). But there are multiple other mechanisms for NADPH-ATP rebalancing, including the water-water cycle (Miyake, 2010), the conversion of NAD(P)H to ATP by the mitochondrial respiratory chain (Taniguchi and Miyake, 2012), and a variety of other metabolic sinks for ATP/ NADPH (Fig. 2).…”

Section: Energy Metabolism In Photosynthetic Tissuesmentioning

confidence: 99%

Inference and prediction of metabolic network fluxes

Nikoloski

Perez-Storey

2015

Plant Physiol.

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In this Update, we cover the basic principles of the estimation and prediction of the rates of the many interconnected biochemical reactions that constitute plant metabolic networks. This includes metabolic flux analysis approaches that utilize the rates or patterns of redistribution of stable isotopes of carbon and other atoms to estimate fluxes, as well as constraints-based optimization approaches such as flux balance analysis. Some of the major insights that have been gained from analysis of fluxes in plants are discussed, including the functioning of metabolic pathways in a network context, the robustness of the metabolic phenotype, the importance of cell maintenance costs, and the mechanisms that enable energy and redox balancing at steady state. We also discuss methodologies to exploit 'omic data sets for the construction of tissue-specific metabolic network models and to constrain the range of permissible fluxes in such models. Finally, we consider the future directions and challenges faced by the field of metabolic network flux phenotyping.The metabolic systems of plants utilize a continual energy stream (i.e. light in the case of photosynthetic tissues and chemical energy in the case of heterotrophic tissues) to drive a complex network of hundreds of chemical reactions away from equilibrium. Ultimately, this leads to the catalyzed biosynthesis of the ordered polymeric biomolecules that make up the biomass of the cells in each tissue and underpins the growth and development of the plant (Smith and Stitt, 2007). To operate on a time scale relevant for life, the system is dependent upon the acceleration of its chemistry by enzymes. Additionally, because of the highly compartmented nature of plant cells, transporter proteins are required to permit the movement of metabolites (i.e. the substrates and products of biochemical reactions) between subcellular compartments. Transporter proteins are also required to bring substrates into cells and to allow the excretion of waste products and other metabolites such as defense compounds. The sum total of expressed genes encoding enzymes and metabolite transporters determines the metabolic capabilities of a cell. In a growing tissue, the net output of this metabolism is anabolic (i.e. leading to the biosynthesis of biomass constituents such as starch, fructans, cell wall, lipid, and protein), but catabolic metabolism is also required. Most importantly, catabolism generates universal energy currencies such as ATP and NAD(P)H, whose turnover is used to provide the energetic driving force for anabolism. Catabolism is also important to allow the turnover of cellular components for regulatory and repair purposes (Linster et al., 2013;Ishihara et al., 2015). The turnover and resynthesis of cellular components, along with the maintenance of electrochemical potentials across membranes, are important facets of metabolism that need to be considered alongside the biosynthesis of macromolecules for growth (Stitt, 2013;Sweetlove et al., 2013).Metabolism, then, is the entirety of c...

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“…Leaf metabolism in the light is known to involve multiple routes for balancing the supply and demand for ATP and NADPH (Noctor and Foyer, 1998;Allen, 2003;Kramer and Evans, 2011;Taniguchi and Miyake, 2012). One immediate problem is that the ratio of ATP to NADPH arising from light-driven LEF does not match the requirements for the fixation of carbon dioxide in the Calvin-Benson cycle (Noctor and Foyer, 1998;Allen, 2003); another problem is the need to dispose of excess energy or reducing equivalents under conditions in which an imbalance arises between supply and demand.…”

Section: Alternative Routes Of Electron Flow and Energy Rebalancing Imentioning

confidence: 99%

“…For example, mitochondria and chloroplasts have several potential mechanisms for maintaining energetic homeostasis, including alternative electron flow pathways, metabolite shuttles for the transfer of reducing power or ATP, and uncoupling mechanisms (Millar et al, 2011;Taniguchi and Miyake, 2012). More generally, the distributed robustness of metabolic networks means that they have the inherent property of being able to achieve cellular objectives in different ways (Wagner, 2005).…”

mentioning

confidence: 99%

A Method of Accounting for Enzyme Costs in Flux Balance Analysis Reveals Alternative Pathways and Metabolite Stores in an Illuminated Arabidopsis Leaf

2015

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Flux balance analysis of plant metabolism is an established method for predicting metabolic flux phenotypes and for exploring the way in which the plant metabolic network delivers specific outcomes in different cell types, tissues, and temporal phases. A recurring theme is the need to explore the flexibility of the network in meeting its objectives and, in particular, to establish the extent to which alternative pathways can contribute to achieving specific outcomes. Unfortunately, predictions from conventional flux balance analysis minimize the simultaneous operation of alternative pathways, but by introducing fluxweighting factors to allow for the variable intrinsic cost of supporting each flux, it is possible to activate different pathways in individual simulations and, thus, to explore alternative pathways by averaging thousands of simulations. This new method has been applied to a diel genome-scale model of Arabidopsis (Arabidopsis thaliana) leaf metabolism to explore the flexibility of the network in meeting the metabolic requirements of the leaf in the light. This identified alternative flux modes in the CalvinBenson cycle revealed the potential for alternative transitory carbon stores in leaves and led to predictions about the lightdependent contribution of alternative electron flow pathways and futile cycles in energy rebalancing. Notable features of the analysis include the light-dependent tradeoff between the use of carbohydrates and four-carbon organic acids as transitory storage forms and the way in which multiple pathways for the consumption of ATP and NADPH can contribute to the balancing of the requirements of photosynthetic metabolism with the energy available from photon capture.

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Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism

Cited by 107 publications

References 50 publications

Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum

Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum

Inference and prediction of metabolic network fluxes

A Method of Accounting for Enzyme Costs in Flux Balance Analysis Reveals Alternative Pathways and Metabolite Stores in an Illuminated Arabidopsis Leaf

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