Mild reductions in cytosolic NADP-dependent isocitrate dehydrogenase activity result in lower amino acid contents and pigmentation without impacting growth

Sulpice, Ronan; Sienkiewicz‐Porzucek, Agata; Osorio, Sonia; Krahnert, Ina; Stitt, Mark; Fernie, Alisdair R.; Nunes‐Nesi, Adriano

doi:10.1007/s00726-010-0617-0

Cited by 33 publications

(24 citation statements)

References 68 publications

(100 reference statements)

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“…An increase in apoplastic malate concentration was recently demonstrated to regulate the closure of stomata via the guard cell-specific R-type anion channel AtALMT12 (Meyer et al, 2010b). Thus, a feedback response of changes in malate levels of photosynthetic gene expression is plausible, and changes in photosynthetic rates are often observed in TCA cycle mutants (Carrari et al, 2003;Nunes-Nesi et al, 2005Sienkiewicz-Porzucek et al, 2010;Sulpice et al, 2010;Araújo et al, 2011). The observation that citrate had a generally repressive effect on the abundance of photosynthetic transcripts while malate feeding resulted in a slight accumulation of these transcripts is interesting in this context (Supplemental Tables S1 and S2).…”

Section: Citrate and Malate Have Unique Roles In Cellular Metabolism mentioning

confidence: 99%

Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves

et al. 2013

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The transcriptional response to metabolites is an important mechanism by which plants integrate information about cellular energy and nutrient status. Although some carboxylic acids have been implicated in the regulation of gene expression for select transcripts, it is unclear whether all carboxylic acids have the same effect, how many transcripts are affected, and how carboxylic acid signaling is integrated with other metabolite signals. In this study, we demonstrate that perturbations in cellular concentrations of citrate, and to a lesser extent malate, have a major impact on nucleus-encoded transcript abundance. Functional categories of transcripts that were targeted by both organic acids included photosynthesis, cell wall, biotic stress, and protein synthesis. Specific functional categories that were only regulated by citrate included tricarboxylic acid cycle, nitrogen metabolism, sulfur metabolism, and DNA synthesis. Further quantitative real-time polymerase chain reaction analysis of specific citrate-responsive transcripts demonstrated that the transcript response to citrate is time and concentration dependent and distinct from other organic acids and sugars. Feeding of isocitrate as well as the nonmetabolizable citrate analog tricarballylate revealed that the abundance of selected marker transcripts is responsive to citrate and not downstream metabolites. Interestingly, the transcriptome response to citrate feeding was most similar to those observed after biotic stress treatments and the gibberellin biosynthesis inhibitor paclobutrazol. Feeding of citrate to mutants with defects in plant hormone signaling pathways did not completely abolish the transcript response but hinted at a link with jasmonic acid and gibberellin signaling pathways. Our results suggest that changes in carboxylic acid abundances can be perceived and signaled in Arabidopsis (Arabidopsis thaliana) by as yet unknown signaling pathways.

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Section: Citrate and Malate Have Unique Roles In Cellular Metabolism mentioning

confidence: 99%

Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves

et al. 2013

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“…In the cells of higher plants, NADP-ICDH activity has been detected and characterized in the different subcellular compartments including the cytosol, mitochondria, chloroplasts and peroxisomes (Attucci et al 1994, Rasmusson and Møller 1998, Corpas et al 1999b, Leterrier et al 2007, Pascual et al 2008, McCarthy-Suárez et al 2011). Significant progress is being achieved in understanding how the NADP-ICDH is involved in nitrogen metabolism, in redox regulation, and in response to oxidative stress (Scheible et al 2000, Hodges et al 2003, Valderrama et al 2006, Mateos et al 2009, Mhamdi et al 2010, Sulpice et al 2010. However, the specific function of this enzyme in each subcellular compartment in physiological and stress conditions remains unclear.…”

Section: Introductionmentioning

confidence: 98%

Cytosolic NADP-isocitrate dehydrogenase in Arabidopsis leaves and roots

Leterrier¹,

Barroso²,

Palma³

et al. 2012

Biol. plant.

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NADP-dependent isocitrate dehydrogenase (NADP-ICDH) catalyses the production of NADPH, which is an essential component in the cellular homeostasis. In Arabidopsis, the kinetic parameters (K m and V max ) of cytosolic NADP-ICDH were different in leaves and roots. In vitro applied H 2 O 2 did not affect the NADP-ICDH activity in either organ, however, the reduced glutathione inhibited the activity in leaves but not in roots. On the other hand, S-nitrosoglutathione (a NO donor) and peroxynitrite depressed NADP-ICDH activity in leaves and roots.Additional key words: hydrogen peroxide, nitric oxide, peroxynitrite, reactive nitrogen species, S-nitrosoglutathione.

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“…With the exception of a handful of studies concerning root metabolism (Koyama et al, 2000;Ló pez-Bucio et al, 2000, 2003van der Merwe et al, 2009), the majority of studies have focused on leaf tissue, despite the fact that the role of the TCA cycle in the illuminated leaf remains somewhat contentious (Tcherkez et al, 2005;Nunes-Nesi et al, 2007a). Intriguingly, quite diverse effects were observed upon downregulation of the various steps of the cycle, with deficiency of expression of aconitase and the mitochondrial malate dehydrogenase resulting in enhanced photosynthetic rates Nunes-Nesi et al, 2005), whereas inhibition of either citrate synthase, succinyl CoA ligase, or isocitrate dehydrogenase had little effect on the rates of photosynthesis itself and relatively minor consequences on photosynthetic metabolism in general (Studart-Guimarã es et al, 2007;Sienkiewicz-Porzucek et al, 2008Sulpice et al, 2010). By contrast, downregulation of the expression of fumarase restricted photosynthesis and plant growth.…”

Section: Introductionmentioning

confidence: 99%

Antisense Inhibition of the Iron-Sulphur Subunit of Succinate Dehydrogenase Enhances Photosynthesis and Growth in Tomato via an Organic Acid–Mediated Effect on Stomatal Aperture

et al. 2011

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Transgenic tomato (Solanum lycopersicum) plants expressing a fragment of the Sl SDH2-2 gene encoding the iron sulfur subunit of the succinate dehydrogenase protein complex in the antisense orientation under the control of the 35S promoter exhibit an enhanced rate of photosynthesis. The rate of the tricarboxylic acid (TCA) cycle was reduced in these transformants, and there were changes in the levels of metabolites associated with the TCA cycle. Furthermore, in comparison to wild-type plants, carbon dioxide assimilation was enhanced by up to 25% in the transgenic plants under ambient conditions, and mature plants were characterized by an increased biomass. Analysis of additional photosynthetic parameters revealed that the rate of transpiration and stomatal conductance were markedly elevated in the transgenic plants. The transformants displayed a strongly enhanced assimilation rate under both ambient and suboptimal environmental conditions, as well as an elevated maximal stomatal aperture. By contrast, when the Sl SDH2-2 gene was repressed by antisense RNA in a guard cell-specific manner, changes in neither stomatal aperture nor photosynthesis were observed. The data obtained are discussed in the context of the role of TCA cycle intermediates both generally with respect to photosynthetic metabolism and specifically with respect to their role in the regulation of stomatal aperture.

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Mild reductions in cytosolic NADP-dependent isocitrate dehydrogenase activity result in lower amino acid contents and pigmentation without impacting growth

Cited by 33 publications

References 68 publications

Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves

Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves

Cytosolic NADP-isocitrate dehydrogenase in Arabidopsis leaves and roots

Antisense Inhibition of the Iron-Sulphur Subunit of Succinate Dehydrogenase Enhances Photosynthesis and Growth in Tomato via an Organic Acid–Mediated Effect on Stomatal Aperture

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