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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

Éric Claeyssen, Sonia Dorion, Audrey Clendenning, Jiang Zhou He, Owen Wally, Jingkui Chen, Evgenia L. Auslender, Marie-Claude Moisan, Mario Jolicoeur, Jean Rivoal

Article (2013)

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Abstract

The metabolism of potato (Solanum tuberosum) roots constitutively over-and underexpressing hexokinase (HK, EC 2.7.1.1) was examined. An 11-fold variation in HK activity resulted in altered root growth, with antisense roots growing better than sense roots. Quantification of sugars, organic acids and amino acids in transgenic roots demonstrated that the manipulation of HK activity had very little effect on the intracellular pools of these metabolites. However, adenylate and free Pi levels were negatively affected by an increase in HK activity. The flux control coefficient of HK over the phosphorylation of glucose was measured for the first time in plants. Its value varied with HK level. It reached 1.71 at or below normal HK activity value and was much lower (0.32) at very high HK levels. Measurements of glycolytic flux and O-2 uptake rates demonstrated that the differences in glucose phosphorylation did not affect significantly glycolytic and respiratory metabolism. We hypothesized that these results could be explained by the existence of a futile cycle between the pools of hexose-Ps and carbohydrates. This view is supported by several lines of evidence. Firstly, activities of enzymes capable of catalyzing these reactions were detected in roots, including a hexose-P phosphatase. Secondly, metabolic tracer experiments using C-14-glucose as precursor showed the formation of C-14-fructose and C-14-sucrose. We conclude that futile cycling of hexose-P could be partially responsible for the differences in energetic status in roots with high and low HK activity and possibly cause the observed alterations in growth in transgenic roots. The involvement of HK and futile cycles in the control of glucose-6P metabolism is discussed.

Uncontrolled Keywords

Energy Metabolism; Glucose; Hexokinase; Hexosephosphates; Phosphorylation; Plant Roots; Plants, Genetically Modified; Solanum tuberosum; Substrate Cycling; Hexosephosphates; Hexokinase; Glucose

Subjects: 1800 Chemical engineering > 1800 Chemical engineering
5400 Biochemistry > 5400 Biochemistry
5400 Biochemistry > 5408 Metabolism
Department: Department of Chemical Engineering
Funders: CRSNG / NSERC, China Scholarship Council - State Scholarship Fund, Undergraduate Student Research Canada - Award from the Natural Science and Engineering Research Council, Université de Montréal - Fonds de Bourses en Sciences Biologiques, Canada Research Chair in Applied Metabolic Engineering
PolyPublie URL: https://publications.polymtl.ca/3444/
Journal Title: PLOS One (vol. 8, no. 1)
Publisher: PLOS
DOI: 10.1371/journal.pone.0053898
Official URL: https://doi.org/10.1371/journal.pone.0053898
Date Deposited: 15 Jan 2019 13:34
Last Modified: 10 Nov 2022 20:25
Cite in APA 7: Claeyssen, É., Dorion, S., Clendenning, A., He, J. Z., Wally, O., Chen, J., Auslender, E. L., 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). https://doi.org/10.1371/journal.pone.0053898

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