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Cited by 18Plant nutrient uptake and metabolismPhotosynthetic Processes and MechanismsNitrogen and Sulfur Effects on Brassica

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Experimental Evidence of Phospho enol pyruvate Resynthesis from Pyruvate in Illuminated Leaves

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Tcherkez, Guillaume, Mahé, Aline, Boex-Fontvieille, Edouard, Gout, Elisabeth, Guérard, Florence, Bligny, Richard·2011·Plant Physiology
DOI 10.1104/pp.111.180711PMC PMC3165900
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Abstract

Day respiration is the cornerstone of nitrogen assimilation since it provides carbon skeletons to primary metabolism for glutamate (Glu) and glutamine synthesis. However, recent studies have suggested that the tricarboxylic acid pathway is rate limiting and mitochondrial pyruvate dehydrogenation is partly inhibited in the light. Pyruvate may serve as a carbon source for amino acid (e.g. alanine) or fatty acid synthesis, but pyruvate metabolism is not well documented, and neither is the possible resynthesis of phosphoenolpyruvate (PEP). Here, we examined the capacity of pyruvate to convert back to PEP using 13C and 2H labeling in illuminated cocklebur (Xanthium strumarium) leaves. We show that the intramolecular labeling pattern in Glu, 2-oxoglutarate, and malate after 13C-3-pyruvate feeding was consistent with 13C redistribution from PEP via the PEP-carboxylase reaction. Furthermore, the deuterium loss in Glu after 2H3-13C-3-pyruvate feeding suggests that conversion to PEP and back to pyruvate washed out 2H atoms to the solvent. Our results demonstrate that in cocklebur leaves, PEP resynthesis occurred as a flux from pyruvate, approximately 0.5‰ of the net CO2 assimilation rate. This is likely to involve pyruvate inorganic phosphate dikinase and the fundamental importance of this flux for PEP and inorganic phosphate homeostasis is discussed.

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Research works printed but not linked: 55

  1. Aoyagi, 1983, Pyruvate orthophosphate dikinase in wheat leaves, Plant Physiol, 73, 853, 10.1104/pp.73.3.853 · DOI
  2. Baysdorfer, 1984, Spinach pyruvate kinase isoforms: partial purification and regulatory properties, Plant Physiol, 74, 374, 10.1104/pp.74.2.374 · DOI
  3. Beatty, 2009, Transcriptome analysis of nitrogen-efficient rice over-expressing alanine aminotransferase, Plant Biotechnol J, 7, 562, 10.1111/j.1467-7652.2009.00424.x · DOI
  4. Bligny, 1990, 31P NMR studies of spinach leaves and their chloroplasts, J Biol Chem, 265, 1319, 10.1016/S0021-9258(19)40016-1 · DOI
  5. Budde, 1990, Pea leaf mitochondrial PDH complex is inactivated in vivo in a light-dependent manner, Proc Natl Acad Sci USA, 87, 673, 10.1073/pnas.87.2.673 · DOI
  6. Chastain, 2003, Regulation of pyruvate orthophosphate dikinase by ADP/Pi dependent reversible phosphorylation in C3 and C4 plants, Plant Physiol Biochem, 41, 523, 10.1016/S0981-9428(03)00065-2 · DOI
  7. Chastain, 2002, Pyruvate, orthophosphate dikinase in leaves and chloroplasts of C3 plants undergoes light-/dark-induced reversible phosphorylation, Plant Physiol, 128, 1368, 10.1104/pp.010806 · DOI
  8. Dancer, 1990, Independent changes of inorganic phyrophosphate and the ATP/ADP or UTP/UDP ratios in plant cell suspension cultures, Plant Sci, 66, 59, 10.1016/0168-9452(90)90169-O · DOI
  9. Doubnerová, 2011, What can enzymes of C photosynthesis do for C plants under stress?, Plant Sci, 180, 575, 10.1016/j.plantsci.2010.12.005 · DOI
  10. Dyson, 1975, The reversibility of skeletal muscle pyruvate kinase and an assessment of its capacity to support glyconeogenesis, J Biol Chem, 250, 3316, 10.1016/S0021-9258(19)41516-0 · DOI
  11. Edwards, 1978, Photosynthesis by isolated protoplasts, protoplast extracts, and chloroplasts of wheat: influence of orthophosphate, pyrophosphate, and adenylates, Plant Physiol, 62, 313, 10.1104/pp.62.2.313 · DOI
  12. Edwards, 1980, Light and temperature dependence of the rate and degree of activation of pyruvate, Pi dikinase in vivo in maize, Photosynth Res, 1, 199, 10.1007/BF00020599 · DOI
  13. Esposito, 1999, The reversible enolization and hydration of pyruvate: possible roles of keto, enol, and hydrated pyruvate in lactate dehydrogenase catalysis, Can J Chem, 77, 1108, 10.1139/v99-071 · DOI
  14. Farré, 2006, Subcellular pyrophosphate metabolism in developing tubers of potato (Solanum tuberosum), Plant Mol Biol, 62, 165, 10.1007/s11103-006-9011-4 · DOI
  15. Gardeström, 1987, Adenylate ratios in the cytosol, chloroplasts and mitochondria of barley leaf protoplasts during photosynthesis at different carbon dioxide concentrations, FEBS Lett, 212, 114, 10.1016/0014-5793(87)81567-3 · DOI
  16. Gauthier, 2010, In folio isotopic tracing demonstrates that nitrogen assimilation into glutamate is mostly independent from current CO2 assimilation in illuminated leaves of Brassica napus, New Phytol, 185, 988, 10.1111/j.1469-8137.2009.03130.x · DOI
  17. Ghosh, 1966, Adenosine diphosphate glucose pyrophosphorylase: a regulatory enzyme in the biosynthesis of starch in spinach leaf chloroplasts, J Biol Chem, 241, 4491, 10.1016/S0021-9258(18)99747-4 · DOI
  18. Gout, 1993, The C-13 nuclear magnetic resonance studies of malate and citrate synthesis and compartmentation in higher plant cells, J Biol Chem, 286, 3986, 10.1016/S0021-9258(18)53568-7 · DOI
  19. Hanning, 1993, On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves (partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products), Plant Physiol, 103, 1147, 10.1104/pp.103.4.1147 · DOI
  20. Harding, 1970, The pyruvate dehydrogenase complex from the mitochondrial fraction of Neurospora crassa, Arch Biochem Biophys, 138, 653, 10.1016/0003-9861(70)90393-0 · DOI
  21. Hibberd, 2002, Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants, Nature, 415, 451, 10.1038/415451a · DOI
  22. Kang, 2005, White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C-type pyruvate orthophosphate dikinase gene (OsPPDKB), Plant J, 42, 901, 10.1111/j.1365-313X.2005.02423.x · DOI
  23. Kok, 1948, A critical consideration of the quantum yield of Chlorella photosynthesis, Enzymologia, 13, 1
  24. Krimsky, 1959, Phosphorylation of pyruvate by the pyruvate kinase reaction and reversal of glycolysis in a reconstructed system, J Biol Chem, 234, 232, 10.1016/S0021-9258(18)70278-0 · DOI
  25. Lasanthi-Kudahettige, 2007, Transcript profiling of the anoxic rice coleoptile, Plant Physiol, 144, 218, 10.1104/pp.106.093997 · DOI
  26. Lin, 2004, Molecular events in senescing Arabidopsis leaves, Plant J, 39, 612, 10.1111/j.1365-313X.2004.02160.x · DOI
  27. Lin, 1989, Pyruvate kinase isozymes from the green alga, Selenastrum minutum. II. Kinetic and regulatory properties, Arch Biochem Biophys, 269, 228, 10.1016/0003-9861(89)90104-5 · DOI
  28. Linka, 2010, Intracellular metabolite transporters in plants, Mol Plant, 3, 21, 10.1093/mp/ssp108 · DOI
  29. Long, 1960, Spectroscopic study of the pyruvate ion, Trans Faraday Soc, 56, 1570, 10.1039/tf9605601570 · DOI
  30. Marillia, 2003, Biochemical and physiological studies of Arabidopsis thaliana transgenic lines with repressed expression of the mitochondrial pyruvate dehydrogenase kinase, J Exp Bot, 54, 259, 10.1093/jxb/erg020 · DOI
  31. McQuate, 1959, Equilibrium and kinetic studies of the pyruvic kinase reaction, J Biol Chem, 234, 2151, 10.1016/S0021-9258(18)69883-7 · DOI
  32. Nageswara Rao, 1979, 31P NMR studies of enzyme-bound substrates of rabbit muscle pyruvate kinase: equilibrium constants, exchange rates, and NMR parameters, J Biol Chem, 254, 2689, 10.1016/S0021-9258(17)30127-8 · DOI
  33. Nakamoto, 1983, Influence of oxygen and temperature on the dark inactivation of pyruvate orthophosphate dikinase and NADP-malate dehydrogenase in maize, Plant Physiol, 71, 568, 10.1104/pp.71.3.568 · DOI
  34. Nunes-Nesi, 2007, Operation and function of the tricarboxylic acid cycle in the illuminated leaf, Physiol Plant, 129, 45, 10.1111/j.1399-3054.2006.00778.x · DOI
  35. Ohlrogge, 1997, Regulation of fatty acid synthesis, Annu Rev Plant Physiol Plant Mol Biol, 48, 109, 10.1146/annurev.arplant.48.1.109 · DOI
  36. Paul, 2003, Carbon metabolite feedback regulation of leaf photosynthesis and development, J Exp Bot, 54, 539, 10.1093/jxb/erg052 · DOI
  37. Plaxton, 1996, The organization and regulation of plant glycolysis, Annu Rev Plant Physiol Plant Mol Biol, 47, 185, 10.1146/annurev.arplant.47.1.185 · DOI
  38. Pratt, 2009, Phosphate (Pi) starvation effect on the cytosolic Pi concentration and Pi exchanges across the tonoplast in plant cells: an in vivo 31P-nuclear magnetic resonance study using methylphosphonate as a Pi analog, Plant Physiol, 151, 1646, 10.1104/pp.109.144626 · DOI
  39. Rapp, 1987, Pyruvate dehydrogenase complexes from Ricinus communis endosperm, J Plant Physiol, 127, 293, 10.1016/S0176-1617(87)80148-7 · DOI
  40. Rebeillé, 1983, Relationship between the cytoplasm and the vacuole phosphate pool in Acer pseudoplatanus cells, Arch Biochem Biophys, 225, 143, 10.1016/0003-9861(83)90017-6 · DOI
  41. Rivasseau, 2009, Accumulation of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate in illuminated plant leaves at supraoptimal temperatures reveals a bottleneck of the prokaryotic methylerythritol 4-phosphate pathway of isoprenoid biosynthesis, Plant Cell Environ, 32, 82, 10.1111/j.1365-3040.2008.01903.x · DOI
  42. Robinson, 1972, The proton transfer reactions of muscle pyruvate kinase, J Biol Chem, 247, 1096, 10.1016/S0021-9258(19)45620-2 · DOI
  43. Rohmer, 1993, Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate, Biochem J, 295, 517, 10.1042/bj2950517 · DOI
  44. Rohmer, 1996, Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis, J Am Chem Soc, 118, 2564, 10.1021/ja9538344 · DOI · Paper page
  45. Rojas-Beltrán, 1999, Identification of cytosolic Mg2+-dependent soluble inorganic pyrophosphatases in potato and phylogenetic analysis, Plant Mol Biol, 39, 449, 10.1023/A:1006136624210 · DOI
  46. Rose, 1991, A rate-determining proton relay in the pyruvate kinase reaction, Biochemistry, 30, 722, 10.1021/bi00217a021 · DOI
  47. Santarius, 1965, Changes in the intracellular levels of ATP, ADP, AMP and P1 and regulatory function of the adenylate system in leaf cells during photosynthesis, Biochim Biophys Acta, 102, 39, 10.1016/0926-6585(65)90201-3 · DOI
  48. Scheible, 2000, Reciprocal diurnal changes of PEPc expression, cytosolic pyruvate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves, Plant Cell Environ, 23, 1155, 10.1046/j.1365-3040.2000.00634.x · DOI
  49. Stitt, 1982, Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts, Plant Physiol, 70, 971, 10.1104/pp.70.4.971 · DOI
  50. Taylor, 2010, Cytosolic pyruvate,orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content, Plant J, 62, 641, 10.1111/j.1365-313X.2010.04179.x · DOI
  51. Tcherkez, 2008, Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions, Proc Natl Acad Sci USA, 105, 797, 10.1073/pnas.0708947105 · DOI
  52. Tcherkez, 2005, In vivo respiratory metabolism of illuminated leaves, Plant Physiol, 138, 1596, 10.1104/pp.105.062141 · DOI
  53. Tcherkez, 2009, In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid “cycle” in illuminated leaves, Plant Physiol, 151, 620, 10.1104/pp.109.142976 · DOI
  54. Tovar-Méndez, 2003, Regulation of pyruvate dehydrogenase complex activity in plant cells, Eur J Biochem, 270, 1043, 10.1046/j.1432-1033.2003.03469.x · DOI · Paper page
  55. Weiner, 1987, Subcellular compartmentation of pyrophosphate and alkaline pyrophosphatase in leaves, Biochim Biophys Acta, 893, 13, 10.1016/0005-2728(87)90143-5 · DOI

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Authors
Tcherkez, G., Mahé, A., Boex-Fontvieille, E., Gout, E., Guérard, F., & Bligny, R.
Affiliations
  • Université Paris-Sud (FR)
  • Institut de Biologie des Plantes, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8618 (G.T., A.M., E.B.-F.), and Plateforme Métabolisme-Métabolome, Institut Fédératif de Recherche 87 (G.T., F.G.), Université Paris-Sud, 91405 Orsay cedex, France; Institut Universitaire de France, 75005 Paris, France (G.T.); Laboratoire de Physiologie Cellulaire Végétale, Unité Mixte de Reche
ORCID
Venue
Plant Physiology
Publisher
Oxford University Press (OUP)
Published
2011-07-05
Volume
157
Issue
1
Pages
86-95
ISSN
  • 0032-0889 (ISSN-L)
  • 1532-2548
DOI
10.1104/pp.111.180711
PMC
PMC3165900
OpenAlex
W2077728914
Cited by
18
References
0
Citations by year
2023: 1 · 2022: 1 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 1 · 2014: 1 · 2013: 1 · 2012: 3
FWCI
1.93
Type
journal article
Language
en
Open access
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations
  • PLANT PHYSIOLOGY (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Nitrogen and Sulfur Effects on Brassica
Keywords
pyruvate, phosphoenolpyruvate carboxylase, nitrogen assimilation, glutamate synthesis, deuterium labeling, cocklebur, Xanthium strumarium, inorganic phosphate homeostasis, TCA cycle, alpha-ketoglutarate, malate
MeSH terms
Carbon Isotopes, Phosphoenolpyruvate, Plant Leaves, Pyruvic Acid

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