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. 1997 May;114(1):167–175. doi: 10.1104/pp.114.1.167

The Role of Sugars, Hexokinase, and Sucrose Synthase in the Determination of Hypoxically Induced Tolerance to Anoxia in Tomato Roots.

V Germain 1, B Ricard 1, P Raymond 1, P H Saglio 1
PMCID: PMC158291  PMID: 12223696

Abstract

Hypoxic pretreatment of tomato (Lycopersicon esculentum M.) roots induced an acclimation to anoxia. Survival in the absence of oxygen was improved from 10 h to more than 36 h if external sucrose was present. The energy charge value of anoxic tissues increased during the course of hypoxic acclimation, indicating an improvement of energy metabolism. In acclimated roots ethanol was produced immediately after transfer to anoxia and little lactic acid accumulated in the tissues. In nonacclimated roots significant ethanol synthesis occurred after a 1-h lag period, during which time large amounts of lactic acid accumulated in the tissues. Several enzyme activities, including that of alcohol dehydrogenase, lactate dehydrogenase, pyruvate decarboxylase, and sucrose synthase, increased during the hypoxic pretreatment. In contrast to maize, hexokinase activities did not increase and phosphorylation of hexoses was strongly inhibited during anoxia in both kinds of tomato roots. Sucrose, but not glucose or fructose, was able to sustain glycolytic flux via the sucrose synthase pathway and allowed anoxic tolerance of acclimated roots. These results are discussed in relation to cytosolic acidosis and the ability of tomato roots to survive anoxia.

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Selected References

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  1. Andrews D. L., Drew M. C., Johnson J. R., Cobb B. G. The Response of Maize Seedlings of Different Ages to Hypoxic and Anoxic Stress (Changes in Induction of Adh1 mRNA, ADH Activity, and Survival of Anoxia). Plant Physiol. 1994 May;105(1):53–60. doi: 10.1104/pp.105.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bouny J. M., Saglio P. H. Glycolytic Flux and Hexokinase Activities in Anoxic Maize Root Tips Acclimated by Hypoxic Pretreatment. Plant Physiol. 1996 May;111(1):187–194. doi: 10.1104/pp.111.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  4. Mocquot B., Prat C., Mouches C., Pradet A. Effect of anoxia on energy charge and protein synthesis in rice embryo. Plant Physiol. 1981 Sep;68(3):636–640. doi: 10.1104/pp.68.3.636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Mujer C. V., Rumpho M. E., Lin J. J., Kennedy R. A. Constitutive and Inducible Aerobic and Anaerobic Stress Proteins in the Echinochloa Complex and Rice. Plant Physiol. 1993 Jan;101(1):217–226. doi: 10.1104/pp.101.1.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Nguyen-Quoc B., Krivitzky M., Huber S. C., Lecharny A. Sucrose Synthase in Developing Maize Leaves: Regulation of Activity by Protein Level during the Import to Export Transition. Plant Physiol. 1990 Oct;94(2):516–523. doi: 10.1104/pp.94.2.516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Rivoal J., Hanson A. D. Evidence for a Large and Sustained Glycolytic Flux to Lactate in Anoxic Roots of Some Members of the Halophytic Genus Limonium. Plant Physiol. 1993 Feb;101(2):553–560. doi: 10.1104/pp.101.2.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Rivoal J., Hanson A. D. Metabolic Control of Anaerobic Glycolysis (Overexpression of Lactate Dehydrogenase in Transgenic Tomato Roots Supports the Davies-Roberts Hypothesis and Points to a Critical Role for Lactate Secretion. Plant Physiol. 1994 Nov;106(3):1179–1185. doi: 10.1104/pp.106.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Rivoal J., Ricard B., Pradet A. Purification and partial characterization of pyruvate decarboxylase from Oryza sativa L. Eur J Biochem. 1990 Dec 27;194(3):791–797. doi: 10.1111/j.1432-1033.1990.tb19471.x. [DOI] [PubMed] [Google Scholar]
  10. Roberts J. K., Andrade F. H., Anderson I. C. Further Evidence that Cytoplasmic Acidosis Is a Determinant of Flooding Intolerance in Plants. Plant Physiol. 1985 Feb;77(2):492–494. doi: 10.1104/pp.77.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Roberts J. K., Callis J., Jardetzky O., Walbot V., Freeling M. Cytoplasmic acidosis as a determinant of flooding intolerance in plants. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6029–6033. doi: 10.1073/pnas.81.19.6029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Roberts J. K., Hooks M. A., Miaullis A. P., Edwards S., Webster C. Contribution of Malate and Amino Acid Metabolism to Cytoplasmic pH Regulation in Hypoxic Maize Root Tips Studied Using Nuclear Magnetic Resonance Spectroscopy. Plant Physiol. 1992 Feb;98(2):480–487. doi: 10.1104/pp.98.2.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Russell D. A., Wong D. M., Sachs M. M. The anaerobic response of soybean. Plant Physiol. 1990 Feb;92(2):401–407. doi: 10.1104/pp.92.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Sachs M. M., Freeling M., Okimoto R. The anaerobic proteins of maize. Cell. 1980 Jul;20(3):761–767. doi: 10.1016/0092-8674(80)90322-0. [DOI] [PubMed] [Google Scholar]
  15. Saglio P. H., Raymond P., Pradet A. Metabolic Activity and Energy Charge of Excised Maize Root Tips under Anoxia: CONTROL BY SOLUBLE SUGARS. Plant Physiol. 1980 Dec;66(6):1053–1057. doi: 10.1104/pp.66.6.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Saint-Ges V., Roby C., Bligny R., Pradet A., Douce R. Kinetic studies of the variations of cytoplasmic pH, nucleotide triphosphates (31P-NMR) and lactate during normoxic and anoxic transitions in maize root tips. Eur J Biochem. 1991 Sep 1;200(2):477–482. doi: 10.1111/j.1432-1033.1991.tb16207.x. [DOI] [PubMed] [Google Scholar]
  17. Wang F., Smith A. G., Brenner M. L. Isolation and sequencing of tomato fruit sucrose synthase cDNA. Plant Physiol. 1993 Dec;103(4):1463–1464. doi: 10.1104/pp.103.4.1463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Xia J. H., Roberts JKM. Regulation of H+ Extrusion and Cytoplasmic pH in Maize Root Tips Acclimated to a Low-Oxygen Environment. Plant Physiol. 1996 May;111(1):227–233. doi: 10.1104/pp.111.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Xia J. H., Saglio P., Roberts JKM. Nucleotide Levels Do Not Critically Determine Survival of Maize Root Tips Acclimated to a Low-Oxygen Environment. Plant Physiol. 1995 Jun;108(2):589–595. doi: 10.1104/pp.108.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]

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