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Borysiuk, K., Ostaszewska-Bugajska, M., Kryzheuskaya, K., Gardeström, P. & Szal, B. (2022). Glyoxalase I activity affects Arabidopsis sensitivity to ammonium nutrition. Plant Cell Reports, 41, 2393-2413
Open this publication in new window or tab >>Glyoxalase I activity affects Arabidopsis sensitivity to ammonium nutrition
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2022 (English)In: Plant Cell Reports, ISSN 0721-7714, E-ISSN 1432-203X, Vol. 41, p. 2393-2413Article in journal (Refereed) Published
Abstract [en]

Key message: Elevated methylglyoxal levels contribute to ammonium-induced growth disorders in Arabidopsis thaliana. Methylglyoxal detoxification pathway limitation, mainly the glyoxalase I activity, leads to enhanced sensitivity of plants to ammonium nutrition.

Abstract: Ammonium applied to plants as the exclusive source of nitrogen often triggers multiple phenotypic effects, with severe growth inhibition being the most prominent symptom. Glycolytic flux increase, leading to overproduction of its toxic by-product methylglyoxal (MG), is one of the major metabolic consequences of long-term ammonium nutrition. This study aimed to evaluate the influence of MG metabolism on ammonium-dependent growth restriction in Arabidopsis thaliana plants. As the level of MG in plant cells is maintained by the glyoxalase (GLX) system, we analyzed MG-related metabolism in plants with a dysfunctional glyoxalase pathway. We report that MG detoxification, based on glutathione-dependent glyoxalases, is crucial for plants exposed to ammonium nutrition, and its essential role in ammonium sensitivity relays on glyoxalase I (GLXI) activity. Our results indicated that the accumulation of MG-derived advanced glycation end products significantly contributes to the incidence of ammonium toxicity symptoms. Using A. thaliana frostbite1 as a model plant that overcomes growth repression on ammonium, we have shown that its resistance to enhanced MG levels is based on increased GLXI activity and tolerance to elevated MG-derived advanced glycation end-product (MAGE) levels. Furthermore, our results show that glyoxalase pathway activity strongly affects cellular antioxidative systems. Under stress conditions, the disruption of the MG detoxification pathway limits the functioning of antioxidant defense. However, under optimal growth conditions, a defect in the MG detoxification route results in the activation of antioxidative systems.

Place, publisher, year, edition, pages
Springer, 2022
Keywords
Ammonium nutrition, d-Lactate dehydrogenase, Dicarbonyl stress, Glyoxalase, Methylglyoxal, Mitochondrial Complex I mutant
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-200516 (URN)10.1007/s00299-022-02931-5 (DOI)000869198900001 ()36242617 (PubMedID)2-s2.0-85139934614 (Scopus ID)
Available from: 2023-01-12 Created: 2023-01-12 Last updated: 2023-01-18Bibliographically approved
Liebsch, D., Juvany, M., Li, Z., Wang, H.-L., Ziolkowska, A., Chrobok, D., . . . Keech, O. (2022). Metabolic control of arginine and ornithine levels paces the progression of leaf senescence. Plant Physiology, 189(4), 1943-1960
Open this publication in new window or tab >>Metabolic control of arginine and ornithine levels paces the progression of leaf senescence
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2022 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 189, no 4, p. 1943-1960Article in journal (Refereed) Published
Abstract [en]

Leaf senescence can be induced by stress or aging, sometimes in a synergistic manner. It is generally acknowledged that the ability to withstand senescence-inducing conditions can provide plants with stress resilience. Although the signaling and transcriptional networks responsible for a delayed senescence phenotype, often referred to as a functional stay-green trait, have been actively investigated, very little is known about the subsequent metabolic adjustments conferring this aptitude to survival. First, using the individually darkened leaf (IDL) experimental setup, we compared IDLs of wild-type (WT) Arabidopsis (Arabidopsis thaliana) to several stay-green contexts, that is IDLs of two functional stay-green mutant lines, oresara1-2 (ore1-2) and an allele of phytochrome-interacting factor 5 (pif5), as well as to leaves from a WT plant entirely darkened (DP). We provide compelling evidence that arginine and ornithine, which accumulate in all stay-green contexts—likely due to the lack of induction of amino acids (AAs) transport—can delay the progression of senescence by fueling the Krebs cycle or the production of polyamines (PAs). Secondly, we show that the conversion of putrescine to spermidine (SPD) is controlled in an age-dependent manner. Thirdly, we demonstrate that SPD represses senescence via interference with ethylene signaling by stabilizing the ETHYLENE BINDING FACTOR1 and 2 (EBF1/2) complex. Taken together, our results identify arginine and ornithine as central metabolites influencing the stress- and age-dependent progression of leaf senescence. We propose that the regulatory loop between the pace of the AA export and the progression of leaf senescence provides the plant with a mechanism to fine-tune the induction of cell death in leaves, which, if triggered unnecessarily, can impede nutrient remobilization and thus plant growth and survival.

Place, publisher, year, edition, pages
Oxford University Press, 2022
National Category
Botany Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-198906 (URN)10.1093/plphys/kiac244 (DOI)000803838800001 ()35604104 (PubMedID)2-s2.0-85135924586 (Scopus ID)
Funder
Swedish Research Council, 621-2014-4688The Kempe FoundationsCarl Tryggers foundation , CTS14-247Carl Tryggers foundation , CTS15-262Knut and Alice Wallenberg Foundation, 2016.0341Knut and Alice Wallenberg Foundation, 2016.0352Vinnova, 2016-00504
Available from: 2022-09-05 Created: 2022-09-05 Last updated: 2024-04-09Bibliographically approved
Voon, C. P., Law, Y.-S., Guan, X., Lim, S.-L., Xu, Z., Chu, W.-T., . . . Lim, B. L. (2021). Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth. Quantitative Plant Biology, 2, Article ID e7.
Open this publication in new window or tab >>Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
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2021 (English)In: Quantitative Plant Biology, E-ISSN 2632-8828, Vol. 2, article id e7Article in journal (Refereed) Published
Abstract [en]

Efficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts, and the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here, we showed that the overexpression of purple acid phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP+, the electron acceptors of the linear electron flow (LEF). A higher rate of ATP and NADPH production from the LEF, a higher capacity of carbon fixation by the Calvin-Benson-Bassham (CBB) cycle and a greater consumption of NADH in mitochondria enhance photosynthesis in the chloroplasts, ATP production in the mitochondria and sucrose synthesis in the cytosol and eventually boost plant growth and seed yields in the overexpression lines.

Place, publisher, year, edition, pages
Cambridge University Press, 2021
Keywords
ATP, AtPAP2, chloroplasts, mitochondria, NADPH, photosynthesis
National Category
Biochemistry and Molecular Biology Botany
Identifiers
urn:nbn:se:umu:diva-211845 (URN)10.1017/qpb.2021.7 (DOI)2-s2.0-85107394449 (Scopus ID)
Available from: 2023-07-11 Created: 2023-07-11 Last updated: 2023-07-11Bibliographically approved
Lim, S.-L., Voon, C. P., Guan, X., Yang, Y., Gardeström, P. & Lim, B. L. (2020). In planta study of photosynthesis and photorespiration using NADPH and NADH/NAD+ fluorescent protein sensors. Nature Communications, 11(1)
Open this publication in new window or tab >>In planta study of photosynthesis and photorespiration using NADPH and NADH/NAD+ fluorescent protein sensors
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2020 (English)In: Nature Communications, E-ISSN 2041-1723, Vol. 11, no 1Article in journal (Refereed) Published
Abstract [en]

The challenge of monitoring in planta dynamic changes of NADP(H) and NAD(H) redox states at the subcellular level is considered a major obstacle in plant bioenergetics studies. Here, we introduced two circularly permuted yellow fluorescent protein sensors, iNAP and SoNar, into Arabidopsis thaliana to monitor the dynamic changes in NADPH and the NADH/NAD+ ratio. In the light, photosynthesis and photorespiration are linked to the redox states of NAD(P)H and NAD(P) pools in several subcellular compartments connected by the malate-OAA shuttles. We show that the photosynthetic increases in stromal NADPH and NADH/NAD+ ratio, but not ATP, disappear when glycine decarboxylation is inhibited. These observations highlight the complex interplay between chloroplasts and mitochondria during photosynthesis and support the suggestions that, under normal conditions, photorespiration supplies a large amount of NADH to mitochondria, exceeding its NADH-dissipating capacity, and the surplus NADH is exported from the mitochondria to the cytosol through the malate-OAA shuttle.

Place, publisher, year, edition, pages
Springer Nature, 2020
National Category
Biochemistry and Molecular Biology Botany
Identifiers
urn:nbn:se:umu:diva-173594 (URN)10.1038/s41467-020-17056-0 (DOI)000544946500003 ()32591540 (PubMedID)2-s2.0-85086844355 (Scopus ID)
Available from: 2020-07-23 Created: 2020-07-23 Last updated: 2023-03-28Bibliographically approved
Voon, C. P., Guan, X., Sun, Y., Sahu, A., Chan, M. N., Gardeström, P., . . . Lim, B. L. (2018). ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing. Proceedings of the National Academy of Sciences of the United States of America, 115(45), E10778-E10787
Open this publication in new window or tab >>ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing
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2018 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 115, no 45, p. E10778-E10787Article in journal (Refereed) Published
Abstract [en]

Matching ATP: NADPH provision and consumption in the chloroplast is a prerequisite for efficient photosynthesis. In terms of ATP: NADPH ratio, the amount of ATP generated from the linear electron flow does not meet the demand of the Calvin-Benson-Bassham (CBB) cycle. Several different mechanisms to increase ATP availability have evolved, including cyclic electron flow in higher plants and the direct import of mitochondrial-derived ATP in diatoms. By imaging a fluorescent ATP sensor protein expressed in living Arabidopsis thaliana seedlings, we found that MgATP(2-) concentrations were lower in the stroma of mature chloroplasts than in the cytosol, and exogenous ATP was able to enter chloroplasts isolated from 4- and 5-day-old seedlings, but not chloroplasts isolated from 10- or 20-day-old photosynthetic tissues. This observation is in line with the previous finding that the expression of chloroplast nucleotide transporters (NTTs) in Arabidopsis mesophyll is limited to very young seedlings. Employing a combination of photosynthetic and respiratory inhibitors with compartment-specific imaging of ATP, we corroborate the dependency of stromal ATP production on mitochondrial dissipation of photosynthetic reductant. Our data suggest that, during illumination, the provision and consumption of ATP: NADPH in chloroplasts can be balanced by exporting excess reductants rather than importing ATP from the cytosol.

Place, publisher, year, edition, pages
National Academy of Sciences, 2018
Keywords
ATP, chloroplasts, cytosol, mitochondria, photosynthesis
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-153646 (URN)10.1073/pnas.1711497115 (DOI)000449459000031 ()30352850 (PubMedID)2-s2.0-85056138743 (Scopus ID)
Available from: 2018-11-27 Created: 2018-11-27 Last updated: 2023-03-24Bibliographically approved
Law, S. R., Chrobok, D., Juvany, M., Delhomme, N., Lindén, P., Brouwer, B., . . . Keech, O. (2018). Darkened leaves use different metabolic strategies for senescence and survival. Plant Physiology, 177(1), 132-150
Open this publication in new window or tab >>Darkened leaves use different metabolic strategies for senescence and survival
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2018 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 177, no 1, p. 132-150Article in journal (Refereed) Published
Abstract [en]

In plants, an individually darkened leaf initiates senescence much more rapidly than a leaf from a whole darkened plant. Combining transcriptomic and metabolomic approaches in Arabidopsis (Arabidopsis thaliana), we present an overview of the metabolic strategies that are employed in response to different darkening treatments. Under darkened plant conditions, the perception of carbon starvation drove a profound metabolic readjustment in which branched-chain amino acids and potentially monosaccharides released from cell wall loosening became important substrates for maintaining minimal ATP production. Concomitantly, the increased accumulation of amino acids with a high nitrogen-carbon ratio may provide a safety mechanism for the storage of metabolically derived cytotoxic ammonium and a pool of nitrogen for use upon returning to typical growth conditions. Conversely, in individually darkened leaf, the metabolic profiling that followed our 13C-enrichment assays revealed a temporal and differential exchange of metabolites, including sugars and amino acids, between the darkened leaf and the rest of the plant. This active transport could be the basis for a progressive metabolic shift in the substrates fueling mitochondrial activities, which are central to the catabolic reactions facilitating the retrieval of nutrients from the senescing leaf. We propose a model illustrating the specific metabolic strategies employed by leaves in response to these two darkening treatments, which support either rapid senescence or a strong capacity for survival.

Keywords
Arabidopsis thaliana, senescence, metabolism, dark induced senescence, survival
National Category
Botany
Research subject
biology
Identifiers
urn:nbn:se:umu:diva-147675 (URN)10.1104/pp.18.00062 (DOI)000431347500015 ()29523713 (PubMedID)2-s2.0-85050218739 (Scopus ID)
Available from: 2018-05-14 Created: 2018-05-14 Last updated: 2024-04-09Bibliographically approved
Podgorska, A., Ostaszewska-Bugajska, M., Tarnowska, A., Burian, M., Borysiuk, K., Gardeström, P. & Szal, B. (2018). Nitrogen Source Dependent Changes in Central Sugar Metabolism Maintain Cell Wall Assembly in Mitochondrial Complex I-Defective frostbite1 and Secondarily Affect Programmed Cell Death. International Journal of Molecular Sciences, 19(8), Article ID 2206.
Open this publication in new window or tab >>Nitrogen Source Dependent Changes in Central Sugar Metabolism Maintain Cell Wall Assembly in Mitochondrial Complex I-Defective frostbite1 and Secondarily Affect Programmed Cell Death
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2018 (English)In: International Journal of Molecular Sciences, ISSN 1661-6596, E-ISSN 1422-0067, Vol. 19, no 8, article id 2206Article in journal (Refereed) Published
Abstract [en]

For optimal plant growth, carbon and nitrogen availability needs to be tightly coordinated. Mitochondrial perturbations related to a defect in complex I in the Arabidopsis thalianafrostbite1 (fro1) mutant, carrying a point mutation in the 8-kD Fe-S subunit of NDUFS4 protein, alter aspects of fundamental carbon metabolism, which is manifested as stunted growth. During nitrate nutrition, fro1 plants showed a dominant sugar flux toward nitrogen assimilation and energy production, whereas cellulose integration in the cell wall was restricted. However, when cultured on NH4+ as the sole nitrogen source, which typically induces developmental disorders in plants (i.e., the ammonium toxicity syndrome), fro1 showed improved growth as compared to NO3- nourishing. Higher energy availability in fro1 plants was correlated with restored cell wall assembly during NH4+ growth. To determine the relationship between mitochondrial complex I disassembly and cell wall-related processes, aspects of cell wall integrity and sugar and reactive oxygen species signaling were analyzed in fro1 plants. The responses of fro1 plants to NH4+ treatment were consistent with the inhibition of a form of programmed cell death. Resistance of fro1 plants to NH4+ toxicity coincided with an absence of necrotic lesion in plant leaves.

Place, publisher, year, edition, pages
MDPI, 2018
Keywords
cell wall synthesis, complex I defect, frostbite1, mitochondrial mutant, NDUFS4, necrosis, sugar tabolism, sugar signaling, programmed cell death, reactive oxygen species
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-152417 (URN)10.3390/ijms19082206 (DOI)000442869800058 ()30060552 (PubMedID)2-s2.0-85052065695 (Scopus ID)
Available from: 2018-10-05 Created: 2018-10-05 Last updated: 2023-03-23Bibliographically approved
Keech, O., Gardeström, P., Kleczkowski, L. A. & Rouhier, N. (2017). The redox control of photorespiration: from biochemical and physiological aspects to biotechnological considerations. Plant, Cell and Environment, 40(4), 553-569
Open this publication in new window or tab >>The redox control of photorespiration: from biochemical and physiological aspects to biotechnological considerations
2017 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 40, no 4, p. 553-569Article, review/survey (Refereed) Published
Abstract [en]

Photorespiration is a complex and tightly regulated process occurring in photosynthetic organisms. This process can alter the cellular redox balance, notably via the production and consumption of both reducing and oxidizing equivalents. Under certain circumstances, these equivalents, as well as reactive oxygen or nitrogen species, can become prominent in subcellular compartments involved in the photorespiratory process, eventually promoting oxidative post-translational modifications of proteins. Keeping these changes under tight control should therefore be of primary importance. In order to review the current state of knowledge about the redox control of photorespiration, we primarily performed a careful description of the known and potential redox-regulated or oxidation sensitive photorespiratory proteins, and examined in more details two interesting cases: the glycerate kinase and the glycine cleavage system. When possible, the potential impact and subsequent physiological regulations associated with these changes have been discussed. In a second part, we reviewed the extent to which photorespiration contributes to cellular redox homeostasis considering, in particular, the set of peripheral enzymes associated with the canonical photorespiratory pathway. Finally, some recent biotechnological strategies to circumvent photorespiration for future growth improvements are discussed in the light of these redox regulations.

Keywords
cysteine, photorespiration, post-translational regulation, redox proteomics, reducing equivalent
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-118759 (URN)10.1111/pce.12713 (DOI)000397504400009 ()26791824 (PubMedID)2-s2.0-84963979947 (Scopus ID)
Available from: 2016-04-04 Created: 2016-04-04 Last updated: 2024-07-02Bibliographically approved
Chrobok, D., Law, S. R., Brouwer, B., Linden, P., Ziolkowska, A., Liebsch, D., . . . Keech, O. (2016). Dissecting the Metabolic Role of Mitochondria during Developmental Leaf Senescence. Plant Physiology, 172(4), 2132-2153
Open this publication in new window or tab >>Dissecting the Metabolic Role of Mitochondria during Developmental Leaf Senescence
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2016 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 172, no 4, p. 2132-2153Article in journal (Refereed) Published
Abstract [en]

The functions of mitochondria during leaf senescence, a type of programmed cell death aimed at the massive retrieval of nutrients from the senescing organ to the rest of the plant, remain elusive. Here, combining experimental and analytical approaches, we showed that mitochondrial integrity in Arabidopsis (Arabidopsis thaliana) is conserved until the latest stages of leaf senescence, while their number drops by 30%. Adenylate phosphorylation state assays and mitochondrial respiratory measurements indicated that the leaf energy status also is maintained during this time period. Furthermore, after establishing a curated list of genes coding for products targeted to mitochondria, we analyzed in isolation their transcript profiles, focusing on several key mitochondrial functions, such as the tricarboxylic acid cycle, mitochondrial electron transfer chain, iron-sulfur cluster biosynthesis, transporters, as well as catabolic pathways. In tandem with a metabolomic approach, our data indicated that mitochondrial metabolism was reorganized to support the selective catabolism of both amino acids and fatty acids. Such adjustments would ensure the replenishment of alpha-ketoglutarate and glutamate, which provide the carbon backbones for nitrogen remobilization. Glutamate, being the substrate of the strongly up-regulated cytosolic glutamine synthase, is likely to become a metabolically limiting factor in the latest stages of developmental leaf senescence. Finally, an evolutionary age analysis revealed that, while branched-chain amino acid and proline catabolism are very old mitochondrial functions particularly enriched at the latest stages of leaf senescence, auxin metabolism appears to be rather newly acquired. In summation, our work shows that, during developmental leaf senescence, mitochondria orchestrate catabolic processes by becoming increasingly central energy and metabolic hubs.

National Category
Botany
Identifiers
urn:nbn:se:umu:diva-131100 (URN)10.1104/pp.16.01463 (DOI)000391173400006 ()27744300 (PubMedID)2-s2.0-84998775118 (Scopus ID)
Available from: 2017-02-13 Created: 2017-02-13 Last updated: 2023-03-24Bibliographically approved
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, p. 3123-3135Article 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.

Keywords
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)2-s2.0-84969855885 (Scopus ID)
Note

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

Available from: 2016-04-04 Created: 2016-04-04 Last updated: 2024-07-02Bibliographically approved
Projects
Leaf mitochondria and their roles in photosynthesis and senescence [2008-03580_VR]; Umeå UniversityMitochondria and leaf senescence [2008-694_Formas]; Umeå UniversityLeaf mitochondria and their roles in photosynthesis and senescence [2011-04718_VR]; Umeå University
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0001-5900-7395

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