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Per Gardeström - Leaf Mitochondria and Their Roles in Photosynthesis and Senescence |
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Plants need a flexible metabolism in order to respond to the variable environmental conditions that they experience. We investigate leaf metabolism with the aim of obtaining a better understanding of the metabolic pathways involved, their regulation and compartmentation. We focus in particular on the interactions between mitochondria and chloroplasts. The project has two foci: (1) the interaction of respiratory and photosynthetic metabolic pathways in photosynthetically active cells and (2) the involvement of mitochondria and respiratory metabolism in the process of leaf senescence.

Respiration/photorespiration Mitochondria fulfil essential functions in the energy metabo- lism of all cells. The conclusion from studies during the last few years is that mitochondrial oxidative phosphorylation is important for the supply of ATP to the cytosol of photosynthetic cells. However, mitochondrial activities in the light are closely related to photosynthetic metabolism, and many of the interactions between chloroplasts and mitochondria are coupled to photorespiration. In the light, a major function for leaf mitochondria is oxidation of glycine in the photores- piratory glycolate pathway. The flux through this pathway is considerable and involves redox reactions in chloroplasts, peroxisomes and mitochondria that strongly affect the redox situation of the cell. From estimations of subcellular redox states of NAD(H) and NADP(H) pools and ATP/ADP ratios, it is clear that the functions of leaf mitochondria are different in the light with from those in the dark. The TCA cycle appears to be reorganized in the light, so that it changes from being the main source of energy in the cell to providing a flexible mechanism that enables the cell to sustain optimal photosynthesis. This highlights the fact that the cell functions as a unit. Current studies aim to further explore the contributions of mitochondria to photosynthetic metabolism.
Senescence
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Rapid senescence is induced by darkening a few leaves while the rest of the plant remain in light (top right). The yellow leaf at 11 o ́clock was darkened for 6 days. Confocal microscopy pictures of leaf cells from whole darkened plants (top left) and individually darkened leaves (bottom left). Chloroplasts are red and mitochondria green. |
Leaf senescence is an active and closely controlled process in which nutrients are reallocated from decaying leaves to other plant organs. Mitochondria and respiratory metabolism can contribute to this process by providing ATP and carbon skeletons. Analyses of ESTs from poplar indicate that respiration is important during the process of autumn leaf senescence. This is further supported by analysis of transcripts during the process, and determination of a detailed cellular timetable of autumn senescence. We use Arabidopsis as a model to study dark-induced leaf senescence by comparing whole darkened plants (DP) and individually darkened leaves (IDL) (figure top right). In DP, chloroplasts are retained after a 6-day dark treatment and photosynthetic capacity is maintained, while the number of mitochondria and respiration decrease (figure top left). In IDL darkened for the same period of time, the photosynthetic capacity severely decreases aused due to chloroplast degra- dation, while mitochondria become bigger and respiration is maintained (figure bottom left). Based on metabolomic and transcriptomic results, we suggest that leaves from DP enter a stand-by metabolic state of low respiratory activity. In contrast, IDL show high respiratory activity with active mitochondrial contribution to the retrieval of nutrients from senescing leaves. In ongoing experiments we aim to elucidate the metabolic adjustments related to the rapid senescence in IDL.
Svensk samanfattning
Key publications
Hurry VM, Keerberg O, Pärnik T, Öquist G, Gardeström P (1996) Effect of cold hardening on the components of respiratory decarboxylation in the light and in the dark in leaves of winter rye. Plant Physiol 111:713-719
Igamberdiev AU, Gardeström P (2003) Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. BBA 1606:117-125
Bykova NV, Keerberg O, Pärnik T, Bauwe H, Gardeström P (2005) Interaction between photorespiration and respiration in transgenic plants with antisense reduction in glycine decarboxylase. Planta, 222: 130-140
Keskitalo J, Bergkvist G, Gardeström P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139: 1635-1648
Keech O, Pesquet, Ahad A, Askne A, Malmberg G, Nordvall D, Vodnala S, Tuominen H, Dizengremel P, Hurry V, Gardeström P (2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves, Plant Cell & Env 30: 1523-1534
Expand Full Publications List
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Sani M-A, Keech O, Gardeström P, Dufourc EJ, Gröbner G
Magic-angle phosphorus NMR of functional mitochondria: in situ monitoring of lipid response under apoptotic-like stress The FASEB Journal: 2009 23:2872-2878
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Szal B, Dabrowska Z, Malmberg G, Gardeström P, Rychter AM
Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement
Planta: 2008 227:697-706
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Keech O, Pesquet E, Ahad A, Askne A, Nordvall D, Vodnala SM, Tuominen H, Hurry V, Dizengremel P, Gardeström P
The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves
Plant, Cell and Environment: 2007 30:1523-1534
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Moller IM, Gardeström P
Plant mitochondria - more active than ever!
Physiologia Plantarum: 2007 129:1-5
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Gama F, Keech O, Eymery F, Finkemeier I, Gelhaye E, Gardeström P, Dietz KJ, Rey P, Jacquot J-P, Rouhier N
The mitochondrial type II peroxiredoxin from poplar
Physiologia Plantarum: 2007 129:196-206
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Covey-Crump EM, Bykova NV, Affourtit C, Hoefnagel MHN, Gardeström P, Atkin OK
Temperature-dependent changes in respiration rates and redox poise of the ubiquinone pool in protoplasts and isolated mitochondria of potato leaves
Physiologia Plantarum: 2007 129:175-184
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Ivanov AG, Krol M, Sveshnikov D, Malmberg G, Gardestrom P, Hurry V, Oquist G, Huner NPA
Characterization of the photosynthetic apparatus in cortical bark chlorenchyma of Scots pine Planta: 2006 223:1165-1177
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Igamberdiev AU, Shen TY, Gardestrom P
Function of mitochondria during the transition of barley protoplasts from low light to high light Planta: 2006 224:196-204
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Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardestrom P, Schroder W, Hurry V
The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature Plant Journal: 2006 47:720-734
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Persson J, Gardestrom P, Nasholm T
Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris Journal of Experimental Botany: 2006 57:2651-2659
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Hurry V, Igamberdiev AU, Keerberg O, Pärnik T, Atkin OK, Zaragoza-Castells J, Gardeström P
Respiration in photosynthetic cells: Gas exchange components, interactions with photorespiration and the operation of mitochondria in the light
In: Plant Respiration: From Cell to Ecosystem, Lambers H and Ribas-Carbo M, eds. Springer, pp. 43-61
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Keskitalo J, Bergquist G, Gardestrom P, Jansson S
A cellular timetable of autumn senescence Plant Physiol: 2005 139:1635-1648
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Bykova NV, Keerberg O, Parnik T, Bauwe H, Gardestrom P
Interaction between photorespiration and respiration in transgenic potato plants with antisense reduction in glycine decarboxylase Planta: 2005 222:130-140
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Gardestrom P, Hurry V
New in Physiologia Plantarum Physiologia Plantarum: 2005 124:1-3
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Keech O, Dizengremel P, Gardestrom P
Preparation of leaf mitochondria from Arabidopsis thaliana Physiologia Plantarum: 2005 124:403-409
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Baba K, Schmidt J, Ruiz AE, Villarejo A, Shiina T, Gardestrom P, Sane AP, Bhalerao RP
Organellar gene transcription and early seedling development are affected in the rpoT,2 mutant of Arabidopsis Plant J: 2004 38:38-48
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Igamberdiev AU, Mikkelsen TN, Ambus P, Bauwe H, Lea PJ, Gardestrom P
Photorespiration contributes to stomatal regulation and carbon isotope fractionation: a study with barley, potato and Arabidopsis plants deficient in glycine decarboxylase Photosynthesis Research: 2004 81:139-152
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Talts P, Parnik T, Gardestrom P, Keerberg O
Respiratory acclimation in Arabidopsis thaliana leaves at low temperature Journal of Plant Physiology: 2004 161:573-579
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Strand A, Foyer CH, Gustafsson P, Gardestrom P, Hurry V
Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance Plant Cell and Environment: 2003 26:523-535
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Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Bjorkbacka H, Birve SJ, Karlsson J, Gardestrom P, Gustafsson P, Lundeberg J, Jansson S
Gene expression in autumn leaves Plant Physiol: 2003 131:430-442
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Igamberdiev AU, Gardestrom P
Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves Biochimica Et Biophysica Acta-Bioenergetics: 2003 1606:117-125
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Gardestrom P
What's new in photosynthesis Physiologia Plantarum: 2003 119:311-311
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Romanowska E, Igamberdiev AU, Parys E, Gardestrom P
Stimulation of respiration by Pb2+ in detached leaves and mitochondria of C-3 and C-4 plants Physiologia Plantarum: 2002 116:148-154
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Savitch LV, Barker-Astrom J, Ivanov AG, Hurry V, Oquist G, Huner NPA, Gardestrom P
Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma Planta: 2001 214:295-303
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Igamberdiev AU, Ivlev AA, Bykova NV, Threlkeld CN, Lea PJ, Gardestrom P
Decarboxylation of glycine contributes to carbon isotope fractionation in photosynthetic organisms Photosynth Res: 2001 67:177-184
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Heineke D, Bykova N, Gardestrom P, Bauwe H
Metabolic response of potato plants to an antisense reduction of the P-protein of glycine decarboxylase Planta: 2001 212:880-887
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Igamberdiev AU, Romanowska E, Gardestrom P
Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions Journal of Plant Physiology: 2001 158:1325-1332
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Ivanov AG, Sane PV, Zeinalov Y, Malmberg G, Gardestrom P, Huner NPA, Oquist G
Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.) Planta: 2001 213:575-585
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Igamberdiev AU, Bykova NV, Lea PJ, Gardestrom P
The role of photorespiration in redox and energy balance of photosynthetic plant cells: A study with a barley mutant deficient in glycine decarboxylase Physiologia Plantarum: 2001 111:427-438
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Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardestrom P
Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana Plant Journal: 2000 23:759-770
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Siedlecka A, Gardestrom P, Samuelsson G, Kleczkowski LA, Krupa Z
A relationship between carbonic anhydrase and rubisco in response to moderate cadmium stress during light activation of photosynthesis Zeitschrift Fur Naturforschung C-a Journal of Biosciences: 1999 54:759-763
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Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardestrom P, Stitt M
Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway Plant Physiology: 1999 119:1387-1397
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Bykova NV, Rasmusson AG, Igamberdiev AU, Gardestrom P, Moller IM
Two separate transhydrogenase activities are present in plant mitochondria Biochem Biophys Res Commun: 1999 265:106-111
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Eriksson M, Villand P, Gardestrom P, Samuelsson G
Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii Plant Physiology: 1998 116:637-641
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Igamberdiev AU, Hurry V, Kromer S, Gardestrom P
The role of mitochondrial electron transport during photosynthetic induction. A study with barley (Hordeum vulgare) protoplasts incubated with rotenone and oligomycin Physiologia Plantarum: 1998 104:431-439
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Strand A, Hurry V, Gustafsson P, Gardestrom P
Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates Plant Journal: 1997 12:605-614
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Igamberdiev AU, Bykova NV, Gardestrom P
Involvement of cyanide-resistant and rotenone-insensitive pathways of mitochondrial electron transport during oxidation of glycine in higher plants Febs Letters: 1997 412:265-269
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Siedlecka A, Krupa Z, Samuelsson G, Oquist G, Gardestrom P
Primary carbon metabolism in Phaseolus vulgaris plants under Cd/Fe interaction Plant Physiology and Biochemistry: 1997 35:951-957
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Igamberdiev AU, Zhou GQ, Malmberg G, Gardestrom P
Respiration of barley protoplasts before and after illumination Physiologia Plantarum: 1997 99:15-22
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Eriksson M, Karlsson J, Ramazanov Z, Gardestrom P, Samuelsson G
Discovery of an algal mitochondrial carbonic anhydrase: Molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii Proceedings of the National Academy of Sciences of the United States of America: 1996 93:12031-12034
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Hurry V, Keerberg O, Parnik T, Oquist G, Gardestrom P
Effect of Cold Hardening on the Components of Respiratory Decarboxylation in the Light and in the Dark in Leaves of Winter Rye Plant Physiol: 1996 111:713-719
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Gardestrom P
Interactions between mitochondria and chloroplasts Biochimica Et Biophysica Acta-Bioenergetics: 1996 1275:38-40
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Kromer S, Gardestrom P, Samuelsson G
Regulation of the supply of cytosolic oxaloacetate for mitochondrial metabolism via phospho enolpyruvate carboxylase in barley leaf protoplasts .1. The effect of covalent modification on PEPC activity, pH response, and kinetic properties Biochimica Et Biophysica Acta-General Subjects: 1996 1289:343-350
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Kromer S, Gardestrom P, Samuelsson G
Regulation of the supply of oxaloacetate for mitochondrial metabolism via phospho enolpyruvate carboxylase in barley leaf protoplasts .2. Effects of metabolites on PEPC activity at different activation states of the protein Biochimica Et Biophysica Acta-General Subjects: 1996 1289:351-361
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Hurry VM, Strand A, Tobiaeson M, Gardestrom P, Oquist G
Cold Hardening of Spring and Winter-Wheat and Rape Results in Differential-Effects on Growth, Carbon Metabolism, and Carbohydrate Content Plant Physiology: 1995 109:697-706
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Hurry VM, Keerberg O, Parnik T, Gardestrom P, Oquist G
Cold-Hardening Results in Increased Activity of Enzymes Involved in Carbon Metabolism in Leaves of Winter Rye (Secale-Cereale L) Planta: 1995 195:554-562
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Eriksson M, Gardestrom P, Samuelsson G
Isolation, Purification, and Characterization of Mitochondria from Chlamydomonas-Reinhardtii Plant Physiology: 1995 107:479-483
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Hurry V, Tobiaeson M, Kromer S, Gardestrom P, Oquist G
Mitochondria Contribute to Increased Photosynthetic Capacity of Leaves of Winter Rye (Secale-Cereale L) Following Cold-Hardening Plant Cell and Environment: 1995 18:69-76
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Gardestrom P, Lernmark U
The Contribution of Mitochondria to Energetic Metabolism in Photosynthetic Cells Journal of Bioenergetics and Biomembranes: 1995 27:415-421
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Gardestrom P
Atp Synthesis During Photosynthetic Induction Studied with a Very High Time Resolution Biologicheskie Membrany: 1994 11:283-288
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Lernmark U, Gardestrom P
Distribution of Pyruvate-Dehydrogenase Complex Activities between Chloroplasts and Mitochondria from Leaves of Different Species Plant Physiology: 1994 106:1633-1638
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Karlsson J, Ramazanov Z, Hiltonen T, Gardestrom P, Samuelsson G
Effect of Vanadate on Photosynthesis and the Atp Adp Ratio in Low-Co2-Adapted Chlamydomonas-Reinhardtii Cells Planta: 1994 192:46-51
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Hurry VM, Malmberg G, Gardestrom P, Oquist G
Effects of a Short-Term Shift to Low-Temperature and of Long-Term Cold Hardening on Photosynthesis and Ribulose-1,5-Bisphosphate Carboxylase Oxygenase and Sucrose-Phosphate Synthase Activity in Leaves of Winter Rye (Secale-Cereale L) Plant Physiology: 1994 106:983-990
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Kromer S, Lernmark U, Gardestrom P
In-Vivo Mitochondrial Pyruvate-Dehydrogenase Activity, Studied by Rapid Fractionation of Barley Leaf Protoplasts Journal of Plant Physiology: 1994 144:485-490
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Gardestrom P, Petit PX, Moller IM
Purification and Characterization of Plant-Mitochondria and Submitochondrial Particles Methods in Enzymology: 1994 228:424-431
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Borodin V, Gardestrom P, Samuelsson G
The Effect of Light Quality on the Induction of Efficient Photosynthesis under Low Co2 Conditions in Chlamydomonas-Reinhardtii and Chlorella-Pyrenoidosa Physiologia Plantarum: 1994 92:254-260
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Sitbon F, Edlund A, Gardestrom P, Olsson O, Sandberg G
Compartmentation of Indole- 3- Acetic- Acid Metabolism in Protoplasts Isolated from Leaves of Wild- Type and Iaa- Overproducing Transgenic Tobacco Plants
Planta: 1993 191:274-279
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Gardestrom P
Metabolite Levels in the Chloroplast and Extrachloroplast Compartments of Barley Leaf Protoplasts During the Initial Phase of Photosynthetic Induction Biochimica Et Biophysica Acta: 1993 1183:327-332
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Kromer S, Malmberg G, Gardestrom P
Mitochondrial Contribution to Photosynthetic Metabolism - a Study with Barley (Hordeum-Vulgare L) Leaf Protoplasts at Different Light Intensities and Co2 Concentrations Plant Physiology: 1993 102:947-955
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Pawlik B, Skowronski T, Ramazanow Z, Gardestrom P, Samuelsson G
Ph-Dependent Cadmium Transport Inhibits Photosynthesis in the Cyanobacterium Synechocystis-Aquatilis Environmental and Experimental Botany: 1993 33:331-337
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Hurry VM, Gardestrom P, Oquist G
Reduced Sensitivity to Photoinhibition Following Frost-Hardening of Winter Rye Is Due to Increased Phosphate Availability Planta: 1993 190:484-490
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Wigge B, Kromer S, Gardestrom P
The Redox Levels and Subcellular-Distribution of Pyridine-Nucleotides in Illuminated Barley Leaf Protoplasts Studied by Rapid Fractionation Physiologia Plantarum: 1993 88:10-18
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Valerio M, Haraux F, Gardestrom P, Diolez P
Tissue-Specificity of the Regulation of Atp Hydrolysis by Isolated Plant-Mitochondria Febs Letters: 1993 318:113-117
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Kromer S, Malmberg G, Gardestrom P
Mitochondrial Contribution to Photosynthetic Metabolism at Different Light Intensities and Co2 Concentrations in Barley Leaf Protoplasts Photosynthesis Research: 1992 34:198-198
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Lernmark U, Henricson D, Wigge B, Gardestrom P
Glycine Oxidation in Mitochondria Isolated from Light Grown and Etiolated Plant-Tissue Physiologia Plantarum: 1991 82:339-344
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Wingsle G, Gardestrom P, Hallgren JE, Karpinski S
Isolation, Purification, and Subcellular-Localization of Isozymes of Superoxide-Dismutase from Scots Pine (Pinus-Sylvestris L) Needles Plant Physiology: 1991 95:21-28
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Petit PX, Gardestrom P, Rasmusson AG, Moller IM
Properties of Submitochondrial Particles from Plant-Mitochondria - Generation, Surface Characteristics and Nad(P)H Oxidation Plant Science: 1991 78:177-183
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Sundblad LG, Samuelsson G, Wigge B, Gardestrom P
Luminescence Decay Kinetics in Relation to Quenching and Stimulation of Dark Fluorescence from High and Low Co2 Adapted Cells of Scenedesmus-Obliquus and Chlamydomonas-Reinhardtii Photosynthesis Research: 1990 23:269-282
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Palmqvist K, Ramazanov ZM, Gardestrom P, Samuelsson G
Mechanisms of Adaptation of Microalgae to Conditions of Carbon-Dioxide Limitation of Photosynthesis - Possible Role of Carbonic-Anhydrase Soviet Plant Physiology: 1990 37:680-686
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Bligny R, Gardestrom P, Roby C, Douce R
P-31 Nmr-Studies of Spinach Leaves and Their Chloroplasts Journal of Biological Chemistry: 1990 265:1319-1326
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Sandberg G, Gardestrom P, Sitbon F, Olsson O
Presence of Indole- 3- Acetic- Acid in Chloroplasts of Nicotiana- Tabacum and Pinus- Sylvestris
Planta: 1990 180:562-568
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Wigge B, Gardestrom P
Extraction and Measurements of Pyridine-Nucleotides in Subcellular Compartments of Barley Protoplasts Physiologia Plantarum: 1988 73:A19-A19
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Nakamoto H, Sundblad LG, Gardestrom P, Sundbom E
Far-Red Stimulated Long-Lived Luminescence from Barley Protoplasts Plant Science: 1988 55:1-7
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Henricson D, Petit P, Gardestrom P
Fractionation of Plant Mitochondrial Proteins by Temperature-Induced Phase-Separation in Triton X-114 Physiologia Plantarum: 1988 73:A13-A13
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Gardestrom P, Wigge B
Influence of Photorespiration on Atp/Adp Ratios in the Chloroplasts, Mitochondria, and Cytosol, Studies by Rapid Fractionation of Barley (Hordeum-Vulgare) Protoplasts Plant Physiology: 1988 88:69-76
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Gardestrom P, Malmberg G, Petit P
The Contribution of Mitochondria to Photosynthetic Metabolism in C-3 and C-4 Plants Physiologia Plantarum: 1988 73:A15-A15
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Gardestrom P
Adenylate Ratios in the Cytosol, Chloroplasts and Mitochondria of Barley Leaf Protoplasts During Photosynthesis at Different Carbon-Dioxide Concentrations Febs Letters: 1987 212:114-118
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Edwards GE, Gardestrom P
Isolation of Mitochondria from Leaves of C-3, C-4, and Crassulacean Acid Metabolism Plants Methods in Enzymology: 1987 148:421-433
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Moller IM, Liden AC, Ericson I, Gardestrom P
Isolation of Submitochondrial Particles with Different Polarities Methods in Enzymology: 1987 148:442-453
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Gardestrom P, Ericson I
Separation of Spinach Leaf Mitochondria According to Surface-Properties - Partition in Aqueous Polymer 2-Phase Systems Methods in Enzymology: 1987 148:434-442
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Petit PX, Edman KA, Gardestrom P, Ericson I
Some Properties of Mitochondria, Mitoplasts and Submitochondrial Particles of Different Polarities from Plant-Tissues Biochimica Et Biophysica Acta: 1987 890:377-386
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