Abstract
We tested the hypothesis that H+ extrusion contributes to cytoplasmic pH regulation and tolerance of anoxia in maize (Zea mays) root tips. We studied root tips of whole seedlings that were acclimated to a low-oxygen environment by pretreatment in 3% (v/v) O2. Acclimated root tips characteristically regulate cytoplasmic pH near neutrality and survive prolonged anoxia, whereas nonacclimated tips undergo severe cytoplasmic acidosis and die much more quickly. We show that the plasma membrane H+-ATPase can operate under anoxia and that net H+ extrusion increases when cytoplasmic pH falls. However, at an external pH near 6.0, H+ extrusion contributes little to cytoplasmic pH regulation. At more acidic external pH values, net H+ flux into root tips increases dramatically, leading to a decrease in cytoplasmic pH and reduced tolerance of anoxia. We present evidence that, under these conditions, H+ pumps are activated to partly offset acidosis due to H+ influx and, thereby, contribute to cytoplasmic pH regulation and tolerance of anoxia. The regulation of H+ extrusion under anoxia is discussed with respect to the acclimation response and mechanisms of intracellular pH regulation in aerobic plant cells.
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- Gout E., Bligny R., Douce R. Regulation of intracellular pH values in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. J Biol Chem. 1992 Jul 15;267(20):13903–13909. [PubMed] [Google Scholar]
- Hochachka P. W., Mommsen T. P. Protons and anaerobiosis. Science. 1983 Mar 25;219(4591):1391–1397. doi: 10.1126/science.6298937. [DOI] [PubMed] [Google Scholar]
- Hole D. J., Cobb B. G., Hole P. S., Drew M. C. Enhancement of Anaerobic Respiration in Root Tips of Zea mays following Low-Oxygen (Hypoxic) Acclimation. Plant Physiol. 1992 May;99(1):213–218. doi: 10.1104/pp.99.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johansson F., Sommarin M., Larsson C. Fusicoccin Activates the Plasma Membrane H+-ATPase by a Mechanism Involving the C-Terminal Inhibitory Domain. Plant Cell. 1993 Mar;5(3):321–327. doi: 10.1105/tpc.5.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kennedy R. A., Rumpho M. E., Fox T. C. Anaerobic metabolism in plants. Plant Physiol. 1992 Sep;100(1):1–6. doi: 10.1104/pp.100.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lanfermeijer F. C., Prins HBA. Modulation of H+-ATPase Activity by Fusicoccin in Plasma Membrane Vesicles from Oat (Avena sativa L.) Roots (A Comparison of Modulation by Fusicoccin, Trypsin, and Lysophosphatidylcholine). Plant Physiol. 1994 Apr;104(4):1277–1285. doi: 10.1104/pp.104.4.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Roberts J. K., Testa M. P. P-NMR Spectroscopy of Roots of Intact Corn Seedlings. Plant Physiol. 1988 Apr;86(4):1127–1130. doi: 10.1104/pp.86.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roberts J. K., Xia J. H. High-resolution NMR methods for study of higher plants. Methods Cell Biol. 1995;49:245–258. doi: 10.1016/s0091-679x(08)61458-2. [DOI] [PubMed] [Google Scholar]
- Saglio P. H., Raymond P., Pradet A. Oxygen Transport and Root Respiration of Maize Seedlings: A Quantitative Approach Using the Correlation between ATP/ADP and the Respiration Rate Controlled by Oxygen Tension. Plant Physiol. 1983 Aug;72(4):1035–1039. doi: 10.1104/pp.72.4.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Sentenac H., Grignon C. Effect of H Excretion on the Surface pH of Corn Root Cells Evaluated by Using Weak Acid Influx as a pH Probe. Plant Physiol. 1987 Aug;84(4):1367–1372. doi: 10.1104/pp.84.4.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Talbott L. D., Ray P. M., Roberts J. K. Effect of Indoleacetic Acid- and Fusicoccin-Stimulated Proton Extrusion on Internal pH of Pea Internode Cells. Plant Physiol. 1988 May;87(1):211–216. doi: 10.1104/pp.87.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xia J. H., Roberts JKM. Improved Cytoplasmic pH Regulation, Increased Lactate Efflux, and Reduced Cytoplasmic Lactate Levels Are Biochemical Traits Expressed in Root Tips of Whole Maize Seedlings Acclimated to a Low-Oxygen Environment. Plant Physiol. 1994 Jun;105(2):651–657. doi: 10.1104/pp.105.2.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xia J. H., Saglio P. H Efflux and Hexose Transport under Imposed Energy Status in Maize Root Tips. Plant Physiol. 1990 Jun;93(2):453–459. doi: 10.1104/pp.93.2.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Yan F., Schubert S., Mengel K. Effect of Low Root Medium pH on Net Proton Release, Root Respiration, and Root Growth of Corn (Zea mays L.) and Broad Bean (Vicia faba L.). Plant Physiol. 1992 Jun;99(2):415–421. doi: 10.1104/pp.99.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]