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Cited by 86Photosynthetic Processes and MechanismsPlant nutrient uptake and metabolismATP Synthase and ATPases Research

ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing

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Voon, Chia Pao, Guan, Xiaoqian, Sun, Yuzhe, Sahu, Abira, Chan, May Ngor, Gardeström, Per, Wagner, Stephan, Fuchs, Philippe +4 more·2018·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1711497115PMC PMC6233094
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Abstract

Significance: By studying in vivo changes of ATP levels in the plastids and cytosol of Arabidopsis thaliana using a FRET-based ATP sensor, we show that the plastidic ATP concentrations in cotyledon, hypocotyl, and root of 10-day-old seedlings are significantly lower than the cytosolic concentrations. We show that chloroplasts consume ATP rapidly and the import of ATP into mature chloroplasts is impeded by the low density of NTT transporter. Hence, unlike in diatoms, where ATP is imported into chloroplasts to support the Calvin–Benson–Bassham (CBB) cycle, mature chloroplasts of Arabidopsis do not balance the ATP:NADPH ratio by importing ATP from the cytosol. Rather, chloroplasts can export surplus reducing equivalents, which can be used by the mitochondria to supply ATP to the cytosol.

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  • In vivo cytosolic ATP measurements in Arabidopsis cotyledons using a fluorescent protein sensor are consistent with some export of chloroplast ATP even under a relatively low PPFD of 296 μmol m−2 s−1.

    “Recent analyses of in vivo cytosolic ATP levels in Arabidopsis cotyledons using a fluorescent protein sensor are consistent with some export of chloroplast ATP even under a relatively low PPFD of 296 μmol m−2 s−1 (Voon et al., 2018).”

    From Leaf Energy Balance Requires Mitochondrial Respiration and Export of Chloroplast NADPH in the Light (2019) · cites this paper as Voon et al., 2018

    The Results (Fig. 4B–C; page not provided) report fluorescent-sensor measurements in Arabidopsis cotyledons illuminated at 296 µmol m−2 s−1, including a light-dependent rise in cytosolic ATP. They do not attribute that rise to export of ATP from chloroplasts: the authors say they detected no chloroplast ATP transport at this developmental stage and suggest mitochondrial ATP production or export of carbon compounds followed by cytosolic ATP production instead. (LLM, conf=0.85)

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Research works printed but not linked: 43

  1. [1]Allen JF 2003 Cyclic, pseudocyclic and noncyclic photophosphorylation: New links in the chain Trends Plant Sci 8 15 19 12523995
  2. [2]Kramer DM Evans JR 2011 The importance of energy balance in improving photosynthetic productivity Plant Physiol 155 70 78 21078862 PMC3075755
  3. [3]Shikanai T 2016 Regulatory network of proton motive force: Contribution of cyclic electron transport around photosystem I Photosynth Res 129 253 260 26858094
  4. [5]Bailleul B 2015 Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms Nature 524 366 369 26168400
  5. [6]Heldt HW 1969 Adenine nucleotide translocation in spinach chloroplasts FEBS Lett 5 11 14 11947226
  6. [7]Cheung CY Poolman MG Fell DA Ratcliffe RG Sweetlove LJ 2014 A diel flux balance model captures interactions between light and dark metabolism during day-night cycles in C3 and crassulacean acid metabolism leaves Plant Physiol 165 917 929 24596328 PMC4044858
  7. [10]Gardeström P Wigge B 1988 Influence of photorespiration on ATP/ADP ratios in the chloroplasts, mitochondria, and cytosol, studied by rapid fractionation of barley (Hordeum vulgare) protoplasts Plant Physiol 88 69 76 16666282 PMC1055527
  8. [11]Imamura H 2009 Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators Proc Natl Acad Sci USA 106 15651 15656 19720993 PMC2735558
  9. [12]Hatsugai N Perez Koldenkova V Imamura H Noji H Nagai T 2012 Changes in cytosolic ATP levels and intracellular morphology during bacteria-induced hypersensitive cell death as revealed by real-time fluorescence microscopy imaging Plant Cell Physiol 53 1768 1775 22942251
  10. [13]De Col V 2017 ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology eLife 6 e26770 28716182 PMC5515573
  11. [14]Tsuyama T 2013 In vivo fluorescent adenosine 5′-triphosphate (ATP) imaging of Drosophila melanogaster and Caenorhabditis elegans by using a genetically encoded fluorescent ATP biosensor optimized for low temperatures Anal Chem 85 7889 7896 23875533
  12. [15]Gupta RK Gupta P Yushok WD Rose ZB 1983 Measurement of the dissociation constant of MgATP at physiological nucleotide levels by a combination of 31P NMR and optical absorbance spectroscopy Biochem Biophys Res Commun 117 210 216 6607050
  13. [16]Portis AR 1981 Evidence of a low stromal Mg2+ concentration in intact chloroplasts in the dark: I. Studies with the ionophore A23187 Plant Physiol 67 985 989 16661806 PMC425814
  14. [17]Krause GH 1977 Light-induced movement of magnesium ions in intact chloroplasts. Spectroscopic determination with eriochrome blue SE Biochim Biophys Acta 460 500 510 880298
  15. [18]Banerjee S Garcia LR Versaw WK 2016 Quantitative imaging of FRET-based biosensors for cell- and organelle-specific analyses in plants Microsc Microanal 22 300 310 26879593
  16. [19]Gout E Rébeillé F Douce R Bligny R 2014 Interplay of Mg2+, ADP, and ATP in the cytosol and mitochondria: Unravelling the role of Mg2+ in cell respiration Proc Natl Acad Sci USA 111 E4560 E4567 25313036 PMC4217410
  17. [20]Edhofer I Muhlbauer SK Eichacker LA 1998 Light regulates the rate of translation elongation of chloroplast reaction center protein D1 Eur J Biochem 257 78 84 9799105
  18. [21]Reinhold T 2007 Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage Plant J 50 293 304 17355434
  19. [22]Reiser J Linka N Lemke L Jeblick W Neuhaus HE 2004 Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis Plant Physiol 136 3524 3536 15516503 PMC527152
  20. [23]Møller IM Rasmusson AG Fredlund KM 1993 NAD(P)H-ubiquinone oxidoreductases in plant mitochondria J Bioenerg Biomembr 25 377 384 8226719
  21. [24]Labs M Rühle T Leister D 2016 The antimycin A-sensitive pathway of cyclic electron flow: From 1963 to 2015 Photosynth Res 129 231 238 26781235
  22. [25]Yoshida K Watanabe C Kato Y Sakamoto W Noguchi K 2008 Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: A case study with Arabidopsis yellow variegated 2 Plant Cell Physiol 49 592 603 18296449
  23. [26]Yoshida K Terashima I Noguchi K 2007 Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light Plant Cell Physiol 48 606 614 17339232
  24. [27]Atteia A 2004 Identification of prokaryotic homologues indicates an endosymbiotic origin for the alternative oxidases of mitochondria (AOX) and chloroplasts (PTOX) Gene 330 143 148 15087133
  25. [28]Trentmann O Jung B Neuhaus HE Haferkamp I 2008 Nonmitochondrial ATP/ADP transporters accept phosphate as third substrate J Biol Chem 283 36486 36493 19001371 PMC2606016
  26. [29]Klingenberg M 2008 The ADP and ATP transport in mitochondria and its carrier Biochim Biophys Acta 1778 1978 2021 18510943
  27. [30]Sun Y Zerges W 2015 Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta 1847 809 820 25988717
  28. [31]Shi LX Theg SM 2013 Energetic cost of protein import across the envelope membranes of chloroplasts Proc Natl Acad Sci USA 110 930 935 23277572 PMC3549074
  29. [33]Pospísil P 2009 Production of reactive oxygen species by photosystem II Biochim Biophys Acta 1787 1151 1160 19463778
  30. [34]Heineke D 1991 Redox transfer across the inner chloroplast envelope membrane Plant Physiol 95 1131 1137 16668101 PMC1077662
  31. [35]Scheibe R 2004 Malate valves to balance cellular energy supply Physiol Plant 120 21 26 15032873
  32. [36]Kinoshita H 2011 The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism Plant J 65 15 26 21175886
  33. [38]Vishwakarma A Tetali SD Selinski J Scheibe R Padmasree K 2015 Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana Ann Bot 116 555 569 26292995 PMC4578005
  34. [39]Krömer S Heldt HW 1991 On the role of mitochondrial oxidative-phosphorylation in photosynthesis metabolism as studied by the effect of oligomycin on photosynthesis in protoplasts and leaves of barley (Hordeum vulgare) Plant Physiol 95 1270 1276 16668123 PMC1077684
  35. [40]Broussard JA Rappaz B Webb DJ Brown CM 2013 Fluorescence resonance energy transfer microscopy as demonstrated by measuring the activation of the serine/threonine kinase Akt Nat Protoc 8 265 281 23306460 PMC3756929
  36. [41]Nagai T Sawano A Park ES Miyawaki A 2001 Circularly permuted green fluorescent proteins engineered to sense Ca2+ Proc Natl Acad Sci USA 98 3197 3202 11248055 PMC30630
  37. [42]Schwarzländer M Logan DC Fricker MD Sweetlove LJ 2011 The circularly permuted yellow fluorescent protein cpYFP that has been used as a superoxide probe is highly responsive to pH but not superoxide in mitochondria: Implications for the existence of superoxide “flashes.” Biochem J 437 381 387 21631430
  38. [43]Earley KW 2006 Gateway-compatible vectors for plant functional genomics and proteomics Plant J 45 616 629 16441352
  39. [44]Fricker MD 2016 Quantitative redox imaging software Antioxid Redox Signal 24 752 762 26154420
  40. [45]Banerjee S Versaw WK Garcia LR 2015 Imaging cellular inorganic phosphate in Caenorhabditis elegans using a genetically encoded FRET-based biosensor PLoS One 10 e0141128 26484766 PMC4615621
  41. [46]Truernit E Haseloff J 2008 A simple way to identify non-viable cells within living plant tissue using confocal microscopy Plant Methods 4 15 18573203 PMC2442066
  42. [47]Wu FH 2009 Tape-Arabidopsis sandwich—a simpler Arabidopsis protoplast isolation method Plant Methods 5 16 19930690 PMC2794253
  43. [48]Zhang R 2016 AtPAP2 modulates the import of the small subunit of Rubisco into chloroplasts Plant Signal Behav 11 e1239687 27700374 PMC5117095

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Authors
Voon, C. P., Guan, X., Sun, Y., Sahu, A., Chan, M. N., Gardeström, P., Wagner, S., Fuchs, P., Nietzel, T., Versaw, W. K., Schwarzländer, M., & Lim, B. L.
Affiliations
  • University of Hong Kong (HK)
  • Texas A&M University (US)
  • Umeå Plant Science Centre (SE)
  • University of Bonn (DE)
  • Chinese University of Hong Kong (HK)
Corresponding author
Lim, Boon Leong
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2018-10-23
Volume
115
Issue
45
Pages
E10778-E10787
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1711497115
PMC
PMC6233094
OpenAlex
W2896930560
Cited by
86
References
2
Citations by year
2026: 7 · 2025: 7 · 2024: 14 · 2023: 6 · 2022: 14 · 2021: 20 · 2020: 12 · 2019: 6
FWCI
3.38
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • DiVA at Umeå University (Umeå University) (submittedVersion, other-oa)
Funders
  • Seed Funding Program for Basic Research (201411159108)
  • The Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M403/16)
  • Deutsche Forschungsgemeinschaft (SCHW1719/1-1)
  • Research Training Group GRK 2064 (SCHW1719/5-1)
  • USA Department of Energy (DE-SC01014037)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
Keywords
plastids, chloroplasts, cytosol, ATP/NADPH ratio, reducing equivalents, Calvin cycle, Arabidopsis thaliana, seedlings, mitochondria
MeSH terms
Adenosine Triphosphate, Biological Transport, Chloroplasts, Cytosol, Light, Mitochondria, NADP, Oxidation-Reduction, Photosynthesis, Recombinant Proteins, Biosensing Techniques, Signal Transduction, Arabidopsis, Genes, Reporter, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, Fluorescence Resonance Energy Transfer, Nucleotide Transport Proteins, Seedlings

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