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Lindén, P., Keech, O., Stenlund, H., Gardeström, P. & Moritz, T. (2016). Reduced mitochondrial malate dehydrogenase activity has a strong effect on photorespiratory metabolism as revealed by 13C labelling. Journal of Experimental Botany, 67(10), 3123-3135.
Open this publication in new window or tab >>Reduced mitochondrial malate dehydrogenase activity has a strong effect on photorespiratory metabolism as revealed by 13C labelling
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2016 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 67, no 10, 3123-3135 p.Article in journal (Refereed) Published
Abstract [en]

Mitochondrial malate dehydrogenase (mMDH) catalyses the interconversion of malate and oxaloacetate (OAA) in the tricarboxylic acid (TCA) cycle. Its activity is important for redox control of the mitochondrial matrix, through which it may participate in regulation of TCA cycle turnover. In Arabidopsis, there are two isoforms of mMDH. Here, we investigated to which extent the lack of the major isoform, mMDH1 accounting for about 60% of the activity, affected leaf metabolism. In air, rosettes of mmdh1 plants were only slightly smaller than wild type plants although the fresh weight was decreased by about 50%. In low CO2 the difference was much bigger, with mutant plants accumulating only 14% of fresh weight as compared to wild type. To investigate the metabolic background to the differences in growth, we developed a 13CO2 labelling method, using a custom-built chamber that enabled simultaneous treatment of sets of plants under controlled conditions. The metabolic profiles were analysed by gas- and liquid- chromatography coupled to mass spectrometry to investigate the metabolic adjustments between wild type and mmdh1. The genotypes responded similarly to high CO2 treatment both with respect to metabolite pools and 13C incorporation during a 2-h treatment. However, under low CO2 several metabolites differed between the two genotypes and, interestingly most of these were closely associated with photorespiration. We found that while the glycine/serine ratio increased, a concomitant altered glutamine/glutamate/α-ketoglutarate relation occurred. Taken together, our results indicate that adequate mMDH activity is essential to shuttle reductants out from the mitochondria to support the photorespiratory flux, and strengthen the idea that photorespiration is tightly intertwined with peripheral metabolic reactions.

Keyword
Heavy isotope labelling, mass spectrometry, mitochondrial malate dehydrogenase, photorespiration, primary carbon metabolism, redox balance
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-118760 (URN)10.1093/jxb/erw030 (DOI)000376658300019 ()26889011 (PubMedID)
Note

Special issue: Photorespiration: Origins and Metabolic Integration in Interacting Compartments

Available from: 2016-04-04 Created: 2016-04-04 Last updated: 2017-11-30Bibliographically approved
Gardeström, P. & Igamberdiev, A. U. (2016). The origin of cytosolic ATP in photosynthetic cells. Physiologia Plantarum: An International Journal for Plant Biology, 157(3), 367-379.
Open this publication in new window or tab >>The origin of cytosolic ATP in photosynthetic cells
2016 (English)In: Physiologia Plantarum: An International Journal for Plant Biology, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 157, no 3, 367-379 p.Article, review/survey (Refereed) Published
Abstract [en]

In photosynthetically active cells, both chloroplasts and mitochondria have the capacity to produce ATP via photophosphorylation and oxidative phosphorylation, respectively. Thus, theoretically, both organelles could provide ATP for the cytosol, but the extent, to which they actually do this, and how the process is regulated, both remain unclear. Most of the evidence discussed comes from experiments with rapid fractionation of isolated protoplasts subjected to different treatments in combination with application of specific inhibitors. The results obtained indicate that, under conditions where ATP demand for photosynthetic CO2 fixation is sufficiently high, the mitochondria supply the bulk of ATP for the cytosol. In contrast, under stress conditions where CO2 fixation is severely limited, ATP will build up in chloroplasts and it can then be exported to the cytosol, by metabolite shuttle mechanisms. Thus, depending on the conditions, either mitochondria or chloroplasts can supply the bulk of ATP for the cytosol. This supply of ATP is discussed in relation to the idea that mitochondrial functions may be tuned to provide an optimal environment for the chloroplast. By balancing cellular redox states, mitochondria can contribute to an optimal photosynthetic capacity.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2016
National Category
Cell Biology Botany
Identifiers
urn:nbn:se:umu:diva-124251 (URN)10.1111/ppl.12455 (DOI)000379260400010 ()27087668 (PubMedID)
Available from: 2016-07-29 Created: 2016-07-29 Last updated: 2017-11-28Bibliographically approved
Kunz, S., Gardeström, P., Pesquet, E. & Kleczkowski, L. (2015). Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis. Frontiers in Plant Science, 6, Article ID 525.
Open this publication in new window or tab >>Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis
2015 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 6, 525Article in journal (Refereed) Published
Abstract [en]

Simple sugars, like glucose (Glc) and sucrose (Suc), act as signals to modulate the expression of hundreds of genes in plants. Frequently, however, it remains unclear whether this regulation is induced by the sugars themselves or by their derivatives generated in the course of carbohydrate (CH) metabolism. In the present study, we tested the relevance of different CH metabolism and allocation pathways affecting expression patterns of five selected sugar-responsive genes (bZIP63, At5g22920, BT2, MGD2, and TPS9) in Arabidopsis thaliana. In general, the expression followed diurnal changes in the overall sugar availability. However, under steady growth conditions, this response was hardly impaired in the mutants for CH metabolizing/transporting proteins (adg1, sex1, sus1-4, sus5/6, and tpt2), including also hexokinase1 (HXK1) loss- and gain-of-function plants—gin2.1 and oe3.2, respectively. In addition, transgenic plants carrying pbZIP63::GUS showed no changes in reporter-gene-expression when grown on sugar under steady-state conditions. In contrast, short-term treatments of agar-grown seedlings with 1% Glc or Suc induced pbZIP63::GUS repression, which became even more apparent in seedlings grown in liquid media. Subsequent analyses of liquid-grown gin2.1 and oe3.2 seedlings revealed that Glc -dependent regulation of the five selected genes was not affected in gin2.1, whereas it was enhanced in oe3.2 plants for bZIP63, At5g22920, and BT2. The sugar treatments had no effect on ATP/ADP ratio, suggesting that changes in gene expression were not linked to cellular energy status. Overall, the data suggest that HXK1 does not act as Glc sensor controlling bZIP63, At5g22920, and BT2 expression, but it is nevertheless required for the production of a downstream metabolic signal regulating their expression.

Keyword
glucose sensing, hexokinase, BT2 expression, bZIP63 expression, At5g22920 expression, diurnal regulation of expression, sugar regulation of gene expression
National Category
Biochemistry and Molecular Biology Botany
Research subject
Physiological Botany
Identifiers
urn:nbn:se:umu:diva-96578 (URN)10.3389/fpls.2015.00525 (DOI)000358589400001 ()26236323 (PubMedID)
Note

Originally published in thesis in manuscript form with the title: The metabolic activity of HEXOKINASE 1 is required for glucose-induced repression of bZIP63, At5g22920 and BT2 in Arabidopsis

Available from: 2014-11-24 Created: 2014-11-24 Last updated: 2017-12-05Bibliographically approved
Podgorska, A., Ostaszewska, M., Gardeström, P., Rasmusson, A. G. & Szal, B. (2015). In comparison with nitrate nutrition, ammonium nutrition increases growth of the frostbite1 Arabidopsis mutant. Plant, Cell and Environment, 38(1), 224-237.
Open this publication in new window or tab >>In comparison with nitrate nutrition, ammonium nutrition increases growth of the frostbite1 Arabidopsis mutant
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2015 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 38, no 1, 224-237 p.Article in journal (Refereed) Published
Abstract [en]

Ammonium nutrition inhibits the growth of many plant species, including Arabidopsis thaliana. The toxicity of ammonium is associated with changes in the cellular redox state. The cellular oxidant/antioxidant balance is controlled by mitochondrial electron transport chain. In this study, we analysed the redox metabolism of frostbite1 (fro1) plants, which lack mitochondrial respiratory chain complex I. Surprisingly, the growth of fro1 plants increased under ammonium nutrition. Ammonium nutrition increased the reduction level of pyridine nucleotides in the leaves of wild-type plants, but not in the leaves of fro1 mutant plants. The observed higher activities of type II NADH dehydrogenases and cytochrome c oxidase in the mitochondrial electron transport chain may improve the energy metabolism of fro1 plants grown on ammonium. Additionally, the observed changes in reactive oxygen species (ROS) metabolism in the apoplast may be important for determining the growth of fro1 under ammonium nutrition. Moreover, bioinformatic analyses showed that the gene expression changes in fro1 plants significantly overlap with the changes previously observed in plants with a modified apoplastic pH. Overall, the results suggest a pronounced connection between the mitochondrial redox system and the apoplastic pH and ROS levels, which may modify cell wall plasticity and influence growth. In this paper, we analysed the redox metabolism of frostbite1 (fro1) plants lacking Complex I under ammonium nutrition. We showed that, although ammonium leads to stress in wild type plants, ammonium does not cause reductive stress in fro1 plants. Our experimental and bioinformatic analyses indicated that mtETC dysfunction strongly influences apoplastic reactive oxygen species content and pH, and suggested that the faster growth of fro1 plants under ammonium nutrition probably results from modification of the cell wall.

Keyword
ammonium syndrome, apoplast, apoplastic pH, complex I, dysfunction of mtETC, mitochondria, redox meostasis, respiration
National Category
Botany Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-99219 (URN)10.1111/pce.12404 (DOI)000346429800019 ()
Available from: 2015-04-22 Created: 2015-02-04 Last updated: 2017-12-04Bibliographically approved
Igamberdiev, A. U., Lernmark, U. & Gardeström, P. (2014). Activity of the mitochondrial pyruvate dehydrogenase complex in plants is stimulated in the presence of malate. Mitochondrion (Amsterdam. Print), 19(Part B), 184-190.
Open this publication in new window or tab >>Activity of the mitochondrial pyruvate dehydrogenase complex in plants is stimulated in the presence of malate
2014 (English)In: Mitochondrion (Amsterdam. Print), ISSN 1567-7249, E-ISSN 1872-8278, Vol. 19, no Part B, 184-190 p.Article in journal (Refereed) Published
Abstract [en]

The effect of malate on the steady-state activity of the pea (Pisum sativum L.) and barley (Hordeum vulgare L) leaf pyruvate dehydrogenase complex (PDC) has been studied in isolated mitochondria. The addition of malate was found to be stimulatory for the mitochondrial PDC, however there was no stimulation of chloroplast PDC. The stimulation was saturated below 1 mM malate and was apparently related to a partially activated complex, which activity increased in the presence of malate by about twofold. Malate also reversed the reduction of PDC activity in the presence of glycine. Based on the obtained kinetic data, we suggest that the effect of malate is rather not a direct activation of PDC but involves the establishment of NAD-malate dehydrogenase equilibrium, decreasing concentration of NADH and relieving its inhibitory effect of PDC. 

Keyword
Glycine, Malate dehydrogenase, Photorespiration, Plant mitochondria, Pyruvate dehydrogenase complex
National Category
Cell Biology Genetics
Identifiers
urn:nbn:se:umu:diva-99233 (URN)10.1016/j.mito.2014.04.006 (DOI)000346624800008 ()
Available from: 2015-04-17 Created: 2015-02-04 Last updated: 2017-12-04Bibliographically approved
Brouwer, B., Gardeström, P. & Keech, O. (2014). In response to partial plant shading, the lack of phytochrome A does not directly induce leaf senescence but alters the fine-tuning of chlorophyll biosynthesis. Journal of Experimental Botany, 65(14), 4037-4049.
Open this publication in new window or tab >>In response to partial plant shading, the lack of phytochrome A does not directly induce leaf senescence but alters the fine-tuning of chlorophyll biosynthesis
2014 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 65, no 14, 4037-4049 p.Article in journal (Refereed) Published
Abstract [en]

Phytochrome is thought to control the induction of leaf senescence directly, however, the signalling and molecular mechanisms remain unclear. In the present study, an ecophysiological approach was used to establish a functional connection between phytochrome signalling and the physiological processes underlying the induction of leaf senescence in response to shade. With shade it is important to distinguish between complete and partial shading, during which either the whole or only a part of the plant is shaded, respectively. It is first shown here that, while PHYB is required to maintain chlorophyll content in a completely shaded plant, only PHYA is involved in maintaining the leaf chlorophyll content in response to partial plant shading. Second, it is shown that leaf yellowing associated with strong partial shading in phyA-mutant plants actually correlates to a decreased biosynthesis of chlorophyll rather than to an increase of its degradation. Third, it is shown that the physiological impact of this decreased biosynthesis of chlorophyll in strongly shaded phyA-mutant leaves is accompanied by a decreased capacity to adjust the Light Compensation Point. However, the increased leaf yellowing in phyA-mutant plants is not accompanied by an increase of senescence-specific molecular markers, which argues against a direct role of PHYA in inducing leaf senescence in response to partial shade. In conclusion, it is proposed that PHYA, but not PHYB, is essential for fine-tuning the chlorophyll biosynthetic pathway in response to partial shading. In turn, this mechanism allows the shaded leaf to adjust its photosynthetic machinery to very low irradiances, thus maintaining a positive carbon balance and repressing the induction of leaf senescence, which can occur under prolonged periods of shade.

Place, publisher, year, edition, pages
Oxford University Press, 2014
Keyword
Arabidopsis, chlorophyll, far-red light, phytochrome, senescence, shade
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-92956 (URN)10.1093/jxb/eru060 (DOI)000339954000020 ()
Available from: 2014-09-12 Created: 2014-09-09 Last updated: 2017-12-05Bibliographically approved
Bykova, N. V., Møller, I. M., Gardeström, P. & Igamberdiev, A. U. (2014). The function of glycine decarboxylase complex is optimized to maintain high photorespiratory flux via buffering of its reaction products. Mitochondrion (Amsterdam. Print), 19, 357-364.
Open this publication in new window or tab >>The function of glycine decarboxylase complex is optimized to maintain high photorespiratory flux via buffering of its reaction products
2014 (English)In: Mitochondrion (Amsterdam. Print), ISSN 1567-7249, E-ISSN 1872-8278, Vol. 19, 357-364 p.Article in journal (Refereed) Published
Abstract [en]

Oxidation of glycine in photorespiratory pathway is the major flux through mitochondria of C3 plants in the light. It sustains increased intramitochondrial concentrations of NADH and NADPH, which are required to engage the internal rotenone-insensitive NAD(P)H dehydrogenases and the alternative oxidase. We discuss here possible mechanisms of high photorespiratory flux maintenance in mitochondria and suggest that it is fulfilled under conditions where the concentrations of glycine decarboxylase reaction products NADH and CO2 achieve an equilibrium provided by malate dehydrogenase and carbonic anhydrase, respectively. This results in the removal of these products from the glycine decarboxylase multienzyme active sites and in the maintenance of their concentrations at levels sufficiently low to prevent substrate inhibition of the reaction. 

Keyword
Glycine decarboxylase, Non-coupled electron transport, Ma late dehydrogenase, Carbonic anhydrase, otorespiration
National Category
Cell Biology Genetics
Identifiers
urn:nbn:se:umu:diva-99235 (URN)10.1016/j.mito.2014.01.001 (DOI)000346624800030 ()
Available from: 2015-04-17 Created: 2015-02-04 Last updated: 2017-12-04Bibliographically approved
Podgorska, A., Gieczewska, K., Lukawska-Kuzma, K., Rasmusson, A. G., Gardeström, P. & Szal, B. (2013). Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)(+) ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity. Plant, Cell and Environment, 36(11), 2034-2045.
Open this publication in new window or tab >>Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)(+) ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity
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2013 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 36, no 11, 2034-2045 p.Article in journal (Refereed) Published
Abstract [en]

Ammonium nutrition has been suggested to be associated with alterations in the oxidation-reduction state of leaf cells. Herein, we show that ammonium nutrition in Arabidopsis thaliana increases leaf NAD(P)H/NAD(P)(+) ratio, reactive oxygen species content and accumulation of biomolecules oxidized by free radicals. We used the method of rapid fractionation of protoplasts to analyse which cellular compartments were over-reduced under ammonium supply and revealed that observed changes in NAD(P)H/NAD(P)(+) ratio involved only the extrachloroplastic fraction. We also showed that ammonium nutrition changes mitochondrial electron transport chain activity, increasing mitochondrial reactive oxygen species production. Our results indicate that the functional impairment associated with ammonium nutrition is mainly associated with redox reactions outside the chloroplast.

National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-82610 (URN)10.1111/pce.12113 (DOI)000325227400012 ()
Available from: 2013-11-11 Created: 2013-11-05 Last updated: 2017-12-06Bibliographically approved
Brouwer, B., Ziolkowska, A., Bagard, M., Keech, O. & Gardeström, P. (2012). The impact of light intensity on shade-induced leaf senescence. Plant, Cell and Environment, 35(6), 1084-1098.
Open this publication in new window or tab >>The impact of light intensity on shade-induced leaf senescence
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2012 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 35, no 6, 1084-1098 p.Article in journal (Refereed) Published
Abstract [en]

Plants often have to cope with altered light conditions, which in leaves induce various physiological responses ranging from photosynthetic acclimation to leaf senescence. However, our knowledge of the regulatory pathways by which shade and darkness induce leaf senescence remains incomplete. To determine to what extent reduced light intensities regulate the induction of leaf senescence, we performed a functional comparison between Arabidopsis leaves subjected to a range of shading treatments. Individually covered leaves, which remained attached to the plant, were compared with respect to chlorophyll, protein, histology, expression of senescence-associated genes, capacity for photosynthesis and respiration, and light compensation point (LCP). Mild shading induced photosynthetic acclimation and resource partitioning, which, together with a decreased respiration, lowered the LCP. Leaf senescence was induced only under strong shade, coinciding with a negative carbon balance and independent of the red/far-red ratio. Interestingly, while senescence was significantly delayed at very low light compared with darkness, phytochrome A mutant plants showed enhanced chlorophyll degradation under all shading treatments except complete darkness. Taken together, our results suggest that the induction of leaf senescence during shading depends on the efficiency of carbon fixation, which in turn appears to be modulated via light receptors such as phytochrome A.

Place, publisher, year, edition, pages
Malden, MA: Wiley-Blackwell, 2012
Keyword
Arabidopsis thaliana, light compensation point (LCP), photosynthetic acclimation, photosynthetic resource partitioning, phytochromeA (PHYA), R/FR ratio
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-54633 (URN)10.1111/j.1365-3040.2011.02474.x (DOI)000303052500007 ()
Available from: 2012-05-03 Created: 2012-05-03 Last updated: 2017-12-07Bibliographically approved
Keerberg, O., Ivanova, H., Keerberg, H., Pärnik, T., Talts, P. & Gardeström, P. (2011). Quantitative analysis of photosynthetic carbon metabolism in protoplasts and intact leaves of barley. Determination of carbon fluxes and pool sizes of metabolites in different cellular compartments. Biosystems (Amsterdam. Print), 103(2), 291-301.
Open this publication in new window or tab >>Quantitative analysis of photosynthetic carbon metabolism in protoplasts and intact leaves of barley. Determination of carbon fluxes and pool sizes of metabolites in different cellular compartments
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2011 (English)In: Biosystems (Amsterdam. Print), ISSN 0303-2647, E-ISSN 1872-8324, Vol. 103, no 2, 291-301 p.Article in journal (Refereed) Published
Abstract [en]

Rates of carbon fluxes and pool sizes of photosynthetic metabolites in different cellular compartments of barley protoplasts were calculated from the time curves of their labeling in the medium of (CO2)-C-14. Using membrane filtration procedure, kinetics of C-14 incorporation into the products of steady-state photosynthesis was determined separately in chloroplasts, mitochondria and cytosol of barley protoplasts illuminated for different periods in the air containing (CO2)-C-14. To extract the quantitative information, analytical labeling functions P(t) describing the dependence of C-14 content in the primary, intermediate and end products of a linear reaction chain upon the duration of tracer feeding have been derived. The parameters of these functions represent pool sizes of metabolites and rates of carbon fluxes. The values of these parameters were determined by fitting the experimental labeling curves to the functions PM by means of non-linear regression procedure. To elucidate the possible effects of fractionation on the photosynthetic carbon metabolism, the parameters of protoplasts were compared with corresponding values in intact leaves of barley. (C) 2010 Elsevier Ireland Ltd. All rights reserved.

Keyword
Carbon fluxes, Cellular compartments, Labeling functions, Photosynthetic carbon metabolism, Pool sizes of metabolites, Protoplasts of barley
Identifiers
urn:nbn:se:umu:diva-41018 (URN)10.1016/j.biosystems.2010.10.012 (DOI)000287278000020 ()
Available from: 2011-03-16 Created: 2011-03-16 Last updated: 2017-12-11Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0001-5900-7395

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