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Per Gardeström - Leaf Mitochondria and Their Roles in Photosynthesis and Senescence Print E-mail

info_16x16Plants 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.
Per_Gardestrm_portrait

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
gardestrom_1 gardestrom_2
gardestrom_3 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.
sweden_greySvensk 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

playExpand Full Publications List

  1. 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
  2. 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
  3. 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
  4. Moller IM, Gardeström P
    Plant mitochondria - more active than ever!
    Physiologia Plantarum: 2007 129:1-5
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. Keskitalo J, Bergquist G, Gardestrom P, Jansson S
    A cellular timetable of autumn senescence
    Plant Physiol: 2005 139:1635-1648
  13. 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
  14. Gardestrom P, Hurry V
    New in Physiologia Plantarum
    Physiologia Plantarum: 2005 124:1-3
  15. Keech O, Dizengremel P, Gardestrom P
    Preparation of leaf mitochondria from Arabidopsis thaliana
    Physiologia Plantarum: 2005 124:403-409
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. Gardestrom P
    What's new in photosynthesis
    Physiologia Plantarum: 2003 119:311-311
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. Igamberdiev AU, Zhou GQ, Malmberg G, Gardestrom P
    Respiration of barley protoplasts before and after illumination
    Physiologia Plantarum: 1997 99:15-22
  40. 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
  41. 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
  42. Gardestrom P
    Interactions between mitochondria and chloroplasts
    Biochimica Et Biophysica Acta-Bioenergetics: 1996 1275:38-40
  43. 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
  44. 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
  45. 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
  46. 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
  47. Eriksson M, Gardestrom P, Samuelsson G
    Isolation, Purification, and Characterization of Mitochondria from Chlamydomonas-Reinhardtii
    Plant Physiology: 1995 107:479-483
  48. 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
  49. Gardestrom P, Lernmark U
    The Contribution of Mitochondria to Energetic Metabolism in Photosynthetic Cells
    Journal of Bioenergetics and Biomembranes: 1995 27:415-421
  50. Gardestrom P
    Atp Synthesis During Photosynthetic Induction Studied with a Very High Time Resolution
    Biologicheskie Membrany: 1994 11:283-288
  51. 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
  52. 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
  53. 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
  54. 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
  55. Gardestrom P, Petit PX, Moller IM
    Purification and Characterization of Plant-Mitochondria and Submitochondrial Particles
    Methods in Enzymology: 1994 228:424-431
  56. 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
  57. 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
  58. 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
  59. 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
  60. 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
  61. 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
  62. 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
  63. 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
  64. 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
  65. 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
  66. 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
  67. 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
  68. 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
  69. 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
  70. 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
  71. 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
  72. Wigge B, Gardestrom P
    Extraction and Measurements of Pyridine-Nucleotides in Subcellular Compartments of Barley Protoplasts
    Physiologia Plantarum: 1988 73:A19-A19
  73. Nakamoto H, Sundblad LG, Gardestrom P, Sundbom E
    Far-Red Stimulated Long-Lived Luminescence from Barley Protoplasts
    Plant Science: 1988 55:1-7
  74. 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
  75. 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
  76. 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
  77. 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
  78. 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
  79. Moller IM, Liden AC, Ericson I, Gardestrom P
    Isolation of Submitochondrial Particles with Different Polarities
    Methods in Enzymology: 1987 148:442-453
  80. 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
  81. 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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