Abstract
Main conclusion
Futile cycling between free sugars and hexose phosphates occurring under phosphate deficiency could be involved in the maintenance of a threshold level of free cellular phosphate to preserve respiratory metabolism.
We studied the metabolic response of potato cell cultures growing in Pi sufficient (2.5 mM, +Pi) or deficient (125 µM, −Pi) conditions. Under Pi deficiency, cellular growth was severely affected, however −Pi cells were able to maintain a low but steady level of free Pi. We surveyed the activities of 33 primary metabolic enzymes during the course of a 12 days Pi deficiency period. Our results show that many of these enzymes had higher specific activity in –Pi cells. Among these, we found typical markers of Pi deficiency such as phosphoenolpyruvate phosphatase and phosphoenolpyruvate carboxylase as well as enzymes involved in the biosynthesis of organic acids. Intriguingly, several ATP-consuming enzymes such as hexokinase (HK) and phosphofructokinase also displayed increased activity in –Pi condition. For HK, this was associated with an increase in the steady state of a specific HK polypeptide. Quantification of glycolytic intermediates showed a pronounced decrease in phosphate esters under Pi deficiency. Adenylate levels also decreased in –Pi cells, but the Adenylate Energy Charge was not affected by the treatment. To investigate the significance of HK induction under low Pi, [U-14C]-glucose tracer studies were conducted. We found in vivo evidence of futile cycling between pools of hexose phosphates and free sugars under Pi deficiency. Our study suggests that the futile cycling between hexose phosphates and free sugars which is active under +Pi conditions is sustained under Pi deficiency. The possibility that this process represents a metabolic adaptation to Pi deficiency is discussed with respect to Pi homeostasis in Pi-deficient conditions.
Similar content being viewed by others
References
Abel S (2017) Phosphate scouting by root tips. Curr Opin Plant Biol 39:168–177. https://doi.org/10.1016/j.pbi.2017.04.016
Alonso AP, Vigeolas H, Raymond P, Rolin D, Dieuaide-Noubhani M (2005) A new substrate cycle in plants. Evidence for a high glucose-phosphate-to-glucose turnover from in vivo steady-state and pulse-labeling experiments with [13C]glucose and [14C]glucose. Plant Physiol 138:2220–2232
Alonso AP, Raymond P, Rolin D, Dieuaide-Noubhani M (2007) Substrate cycles in the central metabolism of maize root tips under hypoxia. Phytochem 68:2222–2231. https://doi.org/10.1016/j.phytochem.2007.04.022
Alonso AP, Val DL, Shachar-Hill Y (2011) Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering. Metab Eng 13:96–107. https://doi.org/10.1016/j.ymben.2010.10.002
Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant PhysioL 132:2205–2217. https://doi.org/10.1104/pp.103.023903
Attucci S, Rivoal J, Brouquisse R, Carde JP, Pradet A, Raymond P (1994) Characterization of a mitochondrial NADP-dependent isocitrate dehydrogenase in axes of germinating sunflower seeds. Plant Sci 102:49–59
Bozzo GG, Raghothama KG, Plaxton WC (2004) Structural and kinetic properties of a novel purple acid phosphatase from phosphate-starved tomato (Lycopersicon esculentum) cell cultures. Biochem J 377:419–428
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Caparros-Martin JA, McCarthy-Suarez I, Culianez-Macia FA (2013) HAD hydrolase function unveiled by substrate screening: enzymatic characterization of Arabidopsis thaliana subclass I phosphosugar phosphatase AtSgpp. Planta 237:943–954. https://doi.org/10.1007/s00425-012-1809-5
Caparros-Martin JA, McCarthy-Suarez I, Culianez-Macia FA (2014) The kinetic analysis of the substrate specificity of motif 5 in a HAD hydrolase-type phosphosugar phosphatase of Arabidopsis thaliana. Planta 240:479–487. https://doi.org/10.1007/s00425-014-2102-6
Carswell MC, Grant BR, Plaxton WC (1997) Disruption of the phosphate-starvation response of oilseed rape suspension cells by the fungicide phosphonate. Planta 203:67–74. https://doi.org/10.1007/s004250050166
Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: Occurrence, properties and functions. Phytochem 68(6):709–731
Claeyssen E, Wally O, Matton DP, Morse D, Rivoal J (2006) Cloning, expression, purification, and properties of a putative plasma membrane hexokinase from Solanum chacoense. Prot Exp Purif 47:329–339
Claeyssen E, Dorion S, Clendenning A, He JZ, Wally O, Chen J, Auslender EL, Moisan M-C, Jolicoeur M, Rivoal J (2013) The futile cycling of hexose phosphates could account for the fact that hexokinase exerts a high control on glucose phosphorylation but not on glycolytic rate in transgenic potato (Solanum tuberosum) roots. PLoS One 8(1):e53898. https://doi.org/10.1371/journal.pone.0053898
Clark DG, Rognstad R, Katz J (1973) Isotopic evidence for futile cycles in liver-cells. Biochem Biophys Res Commun 54:1141–1148. https://doi.org/10.1016/0006-291x(73)90811-5
Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Chang 19:292–305. https://doi.org/10.1016/j.gloenvcha.2008.10.009
Curi R, Newsholme P, Marzuca-Nassr GN, Takahashi HK, Hirabara SM, Cruzat V, Krause M, de Bittencourt PIH (2016) Regulatory principles in metabolism—then and now. Biochem J 473:1845–1857. https://doi.org/10.1042/bcj20160103
Dorion S, Rivoal J (2003) Quantification of uridine 5'-diphosphate (UDP)-glucose by high-performance liquid chromatography and its application to nonradioactive assay for nucleoside diphosphate kinase using UDP-glucose pyrophosphorylase as a coupling enzyme. Anal Biochem 323:188–196
Dorion S, Rivoal J (2009) A rapid ion exchange procedure that facilitates spectrophotometric assays of phosphorylated metabolites in potato extracts. Acta Physiol Plant 31:855–859
Dorion S, Parveen, Jeukens J, Matton DP, Rivoal J (2005) Cloning and characterization of a cytosolic isoform of triosephosphate isomerase developmentally regulated in potato leaves. Plant Sci 168:183–194
Dorion S, Clendenning A, Jeukens J, Salas JJ, Parveen N, Haner AA, Law RD, Martinez-Force E, Rivoal J (2012) A large decrease of cytosolic triosephosphate isomerase in transgenic potato roots affects the distribution of carbon in primary metabolism. Planta 236:1177–1190
Dorion S, Clendenning A, Rivoal J (2017) Engineering the expression level of cytosolic nucleoside diphosphate kinase in transgenic Solanum tuberosum roots alters growth, respiration and carbon metabolism. Plant J 89:914–926
Duff SMG, Lefebvre DD, Plaxton WC (1989a) Purification and characterization of a phosphoenolpyruvate phosphatase from Brassica nigra suspension cell cultures. Plant Physiol 90:734–741
Duff SMG, Moorhead GB, Lefebvre DD, Plaxton WC (1989b) Phosphate starvation inducible 'bypasses' of adenylate and phosphate dependent glycolytic enzymes in Brassica nigra suspension cells. Plant Physiol 90:1275–1278
Ehara M, Noguchi T, Ueda K (1996) Uptake of neutral red by the vacuoles of a green alga, Micrasterias pinnatifida. Plant Cell Physiol 37:734–741
Ferreira CV, Taga EM, Aoyama H (1999) Glycolytic intermediates as substrates of soybean acid phosphatase isoforms. Plant Sci 147:49–54. https://doi.org/10.1016/S0168-9452(99)00096-5
Ganie AH, Ahmad A, Pandey R, Aref IM, Yousuf PY, Ahmad S, Iqbal M (2015) Metabolite profiling of low-P tolerant and low-P sensitive maize genotypes under phosphorus starvation and restoration conditions. PloS ONE. https://doi.org/10.1371/journal.pone.0129520
Geigenberger P, Stitt M (1991) A “futile” cycle of sucrose synthesis and degradation is involved in regulating partitioning between sucrose, starch and respiration in cotyledons of germinating Ricinus communis L. seedlings when phloem transport is inhibited. Planta 185:81–90. https://doi.org/10.1007/bf00194518
Giehl RFH, von Wirén N (2014) Root Nutrient Foraging. Plant Physiol 166:509–517. https://doi.org/10.1104/pp.114.245225
Good AG, Crosby WL (1989) Anaerobic induction of alanine aminotransferase in barley root tissue. Plant Physiol 90:1305–1309
Gregory AL, Hurley BA, Tran HT, Valentine AJ, She Y-M, Knowles VL, Plaxton WC (2009) In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana. Biochem J 420:57–65. https://doi.org/10.1042/bj20082397
Hauschild R, von Schaewen A (2003) Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato. Plant Physiol 133:47–62
Hendry JI, Prasannan C, Ma FF, Mollers KB, Jaiswal D, Digmurti M, Allen DK, Frigaard NU, Dasgupta S, Wangikar PP (2017) Rerouting of carbon flux in a glycogen mutant of cyanobacteria assessed via isotopically non-stationary C-13 metabolic flux analysis. Biotechnol Bioeng 114:2298–2308. https://doi.org/10.1002/bit.26350
Hernández-Domíguez EE, Valencia-Turcotte LG, Rodríguez-Sotres R (2012) Changes in expression of soluble inorganic pyrophosphatases of Phaseolus vulgaris under phosphate starvation. Plant Sci 187:39–48. https://doi.org/10.1016/j.plantsci.2012.01.009
Hodgson RJ, Plaxton WC (1998) Purification and characterization of cytosolic fructose-1, 6- bisphosphate aldolase from endosperm of germinated castor oil seeds. Arch of Biochem Biophys 355:189–196
Hottiger T, Schmutz P, Wiemken A (1987) Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol 169:5518–5522
Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB, Sheen J, Moore BD (2008) Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228:411–425. https://doi.org/10.1007/s00425-008-0746-9
Kavanová M, Lattanzi FA, Grimoldi AA, Schnyder H (2006) Phosphorus deficiency decreases cell division and elongation in grass leaves. Plant Physiol 141:766–775. https://doi.org/10.1104/pp.106.079699
Kelly GJ, Gibbs M (1973) Nonreversible D-Glyceraldehyde 3-Phosphate Dehydrogenase of plant tissues. Plant Physiol 52:111–118. https://doi.org/10.1104/pp.52.2.111
Kruger NJ, Le Lay P, Ratcliffe RG (2007) Vacuolar compartmentation complicates the steady-state analysis of glucose metabolism and forces reappraisal of sucrose cycling in plants. Phytochem 68:2189–2196. https://doi.org/10.1016/j.phytochem.2007.04.004
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lattanzi FA, Ostler U, Wild M, Morvan-Bertrand A, Decau ML, Lehmeier CA, Meuriot F, Prud'homme MP, Schaufele R, Schnyder H (2012) Fluxes in central carbohydrate metabolism of source leaves in a fructan-storing C-3 grass: rapid turnover and futile cycling of sucrose in continuous light under contrasted nitrogen nutrition status. J Exp Bot 63:2363–2375. https://doi.org/10.1093/jxb/ers020
Law RD, Plaxton WC (1997) Regulatory phosphorylation of banana fruit phosphoenolpyruvate carboxylase by a copurifying phosphoenolpyruvate carboxylase-kinase. Eur J Biochem 247:642–651
López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: Improving low phosphate tolerance in crops. Ann Rev Plant Biol 65:95–123
Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12:250–258. https://doi.org/10.1016/j.pbi.2009.04.003
Magadlela A, Vardien W, Kleinert A, Steenkamp ET, Valentine AJ (2016) Variable P supply affects N metabolism in a legume tree, Virgilia divaricata, from nutrient-poor Mediterranean-type ecosystems. Func Plant Biol 43:287–297. https://doi.org/10.1071/fp15262
Masakapalli SK, Bryant FM, Kruger NJ, Ratcliffe RG (2014) The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a flexible balance between the cytosolic and plastidic contributions to carbohydrate oxidation in response to phosphate limitation. Plant J 78:964–977. https://doi.org/10.1111/tpj.12522
Miller SS, Driscoll BT, Gregerson RG, Gantt JS, Vance CP (1998) Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J 15:173–184
Moorhead GBG, Plaxton WC (1988) Binding of glycolytic enzymes to a particulate fraction in carrot and sugar beet storage roots. Dependence on metabolic state. Plant Physiol 86:348–351. https://doi.org/10.1104/pp.86.2.348
Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523. https://doi.org/10.1073/pnas.93.19.10519
Murley VR, Theodorou ME, Plaxton WC (1998) Phosphate starvation-inducible pyrophosphate-dependent phosphofructokinase occurs in plants whose roots do not form symbiotic associations with mycorrhizal fungi. Physiol Plant 103:405–414. https://doi.org/10.1034/j.1399-3054.1998.1030314.x
Neset T-SS, Cordell D (2012) Global phosphorus scarcity: identifying synergies for a sustainable future. J Sci Food Agric 92:2–6. https://doi.org/10.1002/jsfa.4650
Newsholme EA, Arch JRS, Brooks B, Surholt B (1983) The role of substrate cycles in metabolic regulation. Biochem Soc Trans 11:52–56. https://doi.org/10.1042/bst0110052
Nguyen-Quoc B, Foyer CH (2001) A role for 'futile cycles' involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. J Exp Bot 52(358):881–889
O'Leary B, Park J, Plaxton WC (2011) The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. Biochem J 436:15–34. https://doi.org/10.1042/BJ20110078
Palma DA, Blumwald E, Plaxton WC (2000) Upregulation of vacuolar H(+)-translocating pyrophosphatase by phosphate starvation of Brassica napus (rapeseed) suspension cell cultures. FEBS Lett 486:155–158
Pandey BK, Mehra P, Verma L, Bhadouria J, Giri J (2017) OsHAD1, a haloacid dehalogenase-like APase, enhances phosphate accumulation. Plant Physiol 174:2316–2332. https://doi.org/10.1104/pp.17.00571
Parsons HL, Yip JY, Vanlerberghe GC (1999) Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol 121:1309–1320
Péret B, Clément M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16:442–450. https://doi.org/10.1016/j.tplants.2011.05.006
Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015
Portais J-C, Delort A-M (2002) Carbohydrate cycling in micro-organisms: what can 13C-NMR tell us? FEMS Microbiol Rev 26:375–402. https://doi.org/10.1111/j.1574-6976.2002.tb00621.x
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49. https://doi.org/10.1007/s11104-004-2005-6
Rivoal J, Hanson AD (1993) Evidence for a large and sustained glycolytic flux to lactate in anoxic roots of some members of the halophytic genus Limonium. Plant Physiol 101:553–560
Rivoal J, Ricard B, Pradet A (1989) Glycolytic and fermentative enzyme induction during anaerobiosis in rice seedlings. Plant Physiol Biochem 27:43–52
Rivoal J, Ricard B, Pradet A (1990) Purification and partial characterization of pyruvate decarboxylase from Oryza sativa L. Eur J Biochem 194:791–797
Rivoal J, Ricard B, Pradet A (1991) Lactate dehydrogenase in Oryza sativa L. seedlings and roots: Identification and partial characterization. Plant Physiol 95:682–686
Rivoal J, Dunford R, Plaxton WC, Turpin DH (1996) Purification and properties of four phosphoenolpyruvate carboxylase isoforms from the green alga Selenastrum minutum: evidence that association of the 102-kDa catalytic subunit with unrelated polypeptides may modify the physical and kinetic properties of the enzyme. Arch Biochem Biophys 332:47–57
Rivoal J, Trzos S, Gage DA, Plaxton WC, Turpin DH (2001) Two unrelated phosphoenolpyruvate carboxylase polypeptides physically interact in the high molecular mass isoforms of this enzyme in the unicellular green alga Selenastrum minutum. J Biol Chem 276:12588–12597
Rontein D, Dieuaide-Noubhani M, Dufourc EJ, Raymond P, Rolin D (2002) The metabolic architecture of plant cells. Stability of central metabolism and flexibility of anabolic pathways during the growth cycle of tomato cells. J Biol Chem 277:43948–43960
Le Roux MR, Ward CL, Botha FC, Valentine AJ (2006) Routes of pyruvate synthesis in phosphorus-deficient lupin roots and nodules. New Phytol 169:399–408. https://doi.org/10.1111/j.1469-8137.2005.01594.x
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/. Accessed 2 Aug 2018
Russell JB (2007) The energy spilling reactions of bacteria and other organisms. J Mol Microbiol Biotechnol 13:1–11. https://doi.org/10.1159/000103591
Rychter AM, Chauveau M, Bomsel JL, Lance C (1992) The effect of phosphate deficiency on mitochondrial activity and adenylate levels in bean roots. Physiol Plant 84:80–86
Sangwan RS, Singh N, Plaxton WC (1992) Phosphoenolpyruvate carboxylase activity and concentration in the endosperm of developing and germinating castor oil seeds. Plant Physiol 99:445–449. https://doi.org/10.1104/pp.99.2.445
Sano T, Kuraya Y, Amino S, Nagata T (1999) Phosphate as a limiting factor for the cell division of tobacco BY-2 cells. Plant Cell Physiol 40:1–8
Scholz RW, Wellmer F-W (2013) Approaching a dynamic view on the availability of mineral resources: What we may learn from the case of phosphorus? Global Environ Chang 23:11–27
Shinano T, Yonetani R, Ushihara N, Adachi H, Wasaki J, Matsui H, Osaki M (2001) Characteristics of phosphoenolpyruvate phosphatase purified from Allium cepa. Plant Sci 161:861–869. https://doi.org/10.1016/s0168-9452(01)00480-0
Shulman RG, Rothman DL (2015) Homeostasis and the glycogen shunt explains aerobic ethanol production in yeast. Proc Natl Acad Sci USA 112:10902–10907. https://doi.org/10.1073/pnas.1510730112
Sieger SM, Kristensen BK, Robson CA, Amirsadeghi S, Eng EWY, Abdel-Mesih A, Moller IM, Vanlerberghe GC (2005) The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J Exp Bot 56:1499–1515. https://doi.org/10.1093/jxb/eri146
Simcox PD, Dennis DT (1978) 6-Phosphogluconate dehydrogenase isoenzymes from developing endosperm of ricinus communis L. Plant Physiol 62:287–290. https://doi.org/10.1104/pp.62.2.287
Sun L, Song L, Zhang Y, Zheng Z, Liu D (2016) Arabidopsis PHL2 and PHR1 act redundantly as the key components of the central regulatory system controlling transcriptional responses to phosphate starvation. Plant Physiol 170:499–514. https://doi.org/10.1104/pp.15.01336
Sweetlove LJ, Burrell MM, ap Rees T (1996) Characterization of transgenic potato (Solanum tuberosum) tubers with increased ADPglucose pyrophosphorylase. Biochem J 320:487–492
Theodorou ME, Plaxton WC (1994) Induction of PPi-dependent phosphofructokinase by phosphate starvation in seedlings of Brassica nigra. Plant Cell Environ 17:287–294. https://doi.org/10.1111/j.1365-3040.1994.tb00294.x
Theodorou ME, Cornel FA, Duff SM, Plaxton WC (1992) Phosphate starvation-inducible synthesis of the alpha-subunit of the pyrophosphate-dependent phosphofructokinase in black mustard suspension cells. J Biol Chem 267:21901–21905
Tran HT, Hurley BA, Plaxton WC (2010) Feeding hungry plants: The role of purple acid phosphatases in phosphate nutrition. Plant Sci 179:14–27. https://doi.org/10.1016/j.plantsci.2010.04.005
Troncoso-Ponce MA, Rivoal J, Cejudo FJ, Dorion S, Garcés R, Martinez-Force E (2010) Cloning, biochemical characterisation, tissue localisation and possible post-translational regulatory mechanism of the cytosolic phosphoglucose isomerase from developing sunflower seeds. Planta 232:845–859
Turner WL, Plaxton WC (2001) Purification and characterization of banana fruit acid phosphatase. Planta 214(2):243–249. https://doi.org/10.1007/s004250100607
Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126. https://doi.org/10.1093/pcp/pcq084
van Heerden JH, Wortel MT, Bruggeman FJ, Heijnen JJ, Bollen YJM, Planque R, Hulshof J, O'Toole TG, Wahl SA, Teusink B (2014) Lost in transition: Start-up of glycolysis yields subpopulations of nongrowing cells. Science. https://doi.org/10.1126/science.1245114
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447
Veljanovski V, Vanderbeld B, Knowles VL, Snedden WA, Plaxton WC (2006) Biochemical and molecular characterization of AtPAP26, a vacuolar purple acid phosphatase up-regulated in phosphate-deprived Arabidopsis suspension cells and seedlings. Plant Physiol 142:1282–1293. https://doi.org/10.1104/pp.106.087171
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15
Wood SM, King SP, Kuzma MM, Blakeley SD, Newcomb W, Dennis DT (2002) Pyrophosphate-dependent fructose-6-phosphate 1-phosphotransferase overexpression in transgenic tobacco: physiological and biochemical analysis of source and sink tissues. Can J Bot 80:983–992
Zhao Z, ten Pierick A, de Jonge L, Heijnen JJ, Wahl SA (2012) Substrate cycles in Penicillium chrysogenum quantified by isotopic non-stationary flux analysis. Microb Cell Fact 11:14. https://doi.org/10.1186/1475-2859-11-140
Acknowledgements
This work was supported by a Natural Science and Engineering Research Council of Canada Discovery grant to Jean Rivoal. Jiang Zhou He was partly funded by scholarships from the Chinese Scholarship Council and FRQNT. The authors wish to thank Dr. WC Plaxton (Queen’s University) for the gift of anti-PEPC antibody.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
He, J.Z., Dorion, S., Lacroix, M. et al. Sustained substrate cycles between hexose phosphates and free sugars in phosphate-deficient potato (Solanum tuberosum) cell cultures. Planta 249, 1319–1336 (2019). https://doi.org/10.1007/s00425-019-03088-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-019-03088-4