Differential secretion of lactate and activity of plasma membrane H+-ATPase in the roots of soybean seedlings in response to low-oxygen stress
Hong Shen A B D , Weibin Jing A , Tiancheng Ai A , Ying Lu B and Jianxun Cheng CA Engineering and Technology Research Center of Hubei Waterlogging Lowland Department, Changjiang University, Jingzhou 434103, China.
B College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China.
C College of Life Science, South China Agricultural University, Guangzhou 510642, China.
D Corresponding author. Email: hshen@scau.edu.cn
Australian Journal of Botany 54(5) 471-477 https://doi.org/10.1071/BT05141
Submitted: 16 August 2005 Accepted: 21 December 2005 Published: 3 August 2006
Abstract
Plants display a series of tolerance mechanism following exposure to low-oxygen stress. Increased secretion of end production of carbohydrate catabolism and synthesis of stress-related proteins are important mechanisms enabling the plant to develop tolerance to anoxia stress. In this study, the secretion of lactate and the activity of plasma membrane H+-ATPase in a wild-type (WTS) and a cultivated soybean (CTS) were investigated in response to low-oxygen stress. Low oxygen (0.1% O2, anoxia) increased the secretion of lactate and reduced the activity of plasma membrane H+-ATPase and ATP content in a time-dependent manner. WTS showed greater root elongation and higher survivability than CTS. The higher lactate secretion coincided with the lower accumulation of lactate in WTS than in CTS. Anoxia decreased the cellular pH in soybean roots. Hypoxia (5% O2) increased the secretion of lactate and the activity of plasma membrane H+-ATPase. In comparison to anoxia, hypoxia stress induced increases of 57.4 and 29.7% of endogenous abscisic acid (ABA) in the root apices of WTS and CTS, respectively. Exogenous application of ABA showed a stimulatory effect on the activity of plasma membrane H+-ATPase and the secretion of citrate from soybean roots. However, cycloheximide, an inhibitor of protein synthesis, abolished ABA effects. These results suggest that the modulation of the secretion of lactate and activity of plasma membrane H+-ATPase in soybean roots is associated with the mechanisms of tolerance to low-oxygen stress. ABA might be involved in the hypoxia signal transmitted in soybean roots.
Acknowledgments
This research was supported by the Foundation of Engineering and Technology Research Center of Hubei Waterlogging Lowland (HNKFJ2002C04), Changjiang University, National Natural Science Foundation of China (30471040, 30100110), International Foundation for Science (C/3042-1, 2), Guangdong Province Natural Science Foundation (No. 000642) and the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry.
Ahn SJ,
Im YJ,
Chung GC, Cho BH
(1999) Inducible expression of plasma membrane H+-ATPase in the roots of fig leaf gourd plants under chilling root temperature. Physiologia Plantarum 106, 35–40.
| Crossref | GoogleScholarGoogle Scholar |
Bradford MM
(1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
Carystinos GD,
MacDonald HR,
Monroy AF,
Dhindsa RS, Poole RJ
(1995) Vacuolar H+-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiology 108, 641–649.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Dennis ES,
Dolferus R, Ellis M
(2000) Molecular strategies for improving waterlogging tolerance in plants. Journal of Experimental Botany 51, 89–97.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Dolferus R,
Ellis M,
Bruxelles G,
Trevaskis B,
Hoeren F,
Dennis ES, Peacock WJ
(1997) Strategies of gene action in Arabidopsis during hypoxia. Annals of Botany 79, 21–31.
Drew MC
(1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48, 223–250.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Ellis MH,
Dennis ES, Peacock WJ
(1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiology 119, 57–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Felle HH
(1996) Control of cytoplasmic pH under anoxic conditions and its implication for plasma membrane proton transport in Medicago sativa root hairs. Journal of Experimental Botany 47, 967–973.
Fukao T,
Kennedy RA,
Yamasue Y, Rumpho ME
(2003) Genetic and biochemical analysis of anaerobically-induced enzymes during seed germination of Echinochloacrus-galli varieties tolerant and intolerant of anoxia. Journal of Experimental Botany 54, 1421–1429.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Germain V,
Ricard B,
Raymond P, Saglio PH
(1997) The role of sugars, hexokinase, and sucrose synthase in the determination of hypoxically induced tolerance to anoxia in tomato roots. Plant Physiology 114, 167–175.
| PubMed |
| PubMed |
| PubMed |
Gibbs J, Greenway H
(2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Functional Plant Biology 30, 1–47.
| Crossref | GoogleScholarGoogle Scholar |
Gout E,
Boisson AM,
Aubert S,
Douce R, Bligny R
(2001) Origin of the cytoplasmatic pH changes during anaerobic stress in higher plant cells: carbon-13 and phosphorus-31 nuclear magnetic resonance studies. Plant Physiology 125, 912–925.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Greenway H, Gibbs J
(2003) Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential process. Functional Plant Biology 30, 999–1036.
| Crossref | GoogleScholarGoogle Scholar |
Hwang SY, Vantoai TT
(1991) Abscisic acid induces anaerobiosis tolerance in corn. Plant Physiology 97, 593–597.
| PubMed |
| PubMed |
| PubMed |
Johnson JR,
Cobb BG, Drew MC
(1994) Hypoxic induction of anoxia tolerance in roots of Adh1 null Zea mays L. Plant Physiology 105, 61–67.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Kato-Noguchi H
(2000) Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings. Journal of Experimental Botany 51, 1939–1944.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Macnicol PK, Jacobsen JV
(2001) Regulation of alcohol dehydrogenase gene expression in barley aleurone by gibberellin and abscisic acid. Physiologia Plantarum 111, 533–539.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Menegus F,
Cattaruzza L,
Chersi A, Fronza G
(1989) Differences in the anaerobic lactate-succinate production and in the changes of cell sap pH for plants with high and low resistance to anoxia. Plant Physiology 90, 29–32.
| PubMed |
| PubMed |
| PubMed |
Mertens R,
Neumann D, Weiler EW
(1983) Monoclonal antibodies for the detection and quantitation of the endogenous plant growth regulator, abscisic acid. FEBS Letters 160, 269–272.
| Crossref | GoogleScholarGoogle Scholar |
Ohno T,
Nakahira S,
Suzuki Y,
Kani T,
Hara T, Koyama H
(2004) Molecular characterization of plasma membrane H+-ATPase in a carrot mutant cell line with enhanced citrate excretion. Physiologia Plantarum 122, 265–273.
| Crossref | GoogleScholarGoogle Scholar |
Ricard B,
Toai T,
Chourey P, Saglio P
(1998) Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant. Plant Physiology 116, 1323–1331.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Roberts JKM,
Chang K,
Webster C,
Callis J,
Wemmer D, Walbot V
(1989) Dependence of ethanolic fermentation, cytoplasmic pH regulation and viability on the activity of alcohol dehydrogenase in hypoxic maize root tips. Plant Physiology 89, 1275–1278.
| PubMed |
| PubMed |
| PubMed |
Sachs MM,
Subbaiah CC, Saab IN
(1996) Anaerobic gene expression and flooding tolerance in maize. Journal of Experimental Botany 47, 1–15.
Scott AC, Allen NS
(1999) Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiology 121, 1291–1298.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Shen H,
He LF,
Sasaki T,
Yamamoto Y,
Zheng SJ,
Ligaba A,
Yan XL,
Ahn SJ,
Yamaguchi M,
Sasakawa H, Matsumoto H
(2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiology 138, 287–296.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Sousa D, Sodek D
(2002) The metabolic response of plants to oxygen deficiency. Brazilian Journal of Plant Physiology 14, 83–94.
| Crossref |
Crossref |
Crossref |
Umeda M, Uchimiya H
(1994) Differential transcript levels of genes associated with glycolysis and alcohol fermentation in rice plants (Oryza sativa L.) under submergence stress. Plant Physiology 106, 1015–1022.
| PubMed |
| PubMed |
| PubMed |
Vartapetian BB, Jackson MB
(1997) Plant adaptations to anaerobic stress. Annals of Botany 79, 3–20.
| Crossref | GoogleScholarGoogle Scholar |
Vitart V,
Baxter I,
Doerner P, Harper JF
(2001) Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis. Plant Journal 27, 191–201.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Xia JH, Roberts JKM
(1994) 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 Physiology 105, 651–657.
| PubMed |
| PubMed |
| PubMed |
Xia JH, Saglio P
(1992) Lactic acid efflux as a mechanism of hypoxic acclimation of maize root tips to anoxia. Plant Physiology 100, 40–46.
| PubMed |
| PubMed |
| PubMed |
Xia JH,
Saglio P, Roberts JKM
(1995) Nucleotide levels do not critically determine survival of maize root tips acclimated to a low-oxygen environment. Plant Physiology 108, 589–595.
| PubMed |
| PubMed |
| PubMed |
Yan F,
Zhu Y,
Muller C,
Zorb C, Schubert S
(2002) Adaptation of H+-pumping and plasma membrane ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiology 129, 50–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
PubMed |
PubMed |
Zeevaart JAD, Creelman RA
(1988) Metabolism and physiology of abscisic acid. Annual Review of Plant Physiology and Plant Molecular Biology 39, 439–473.
| Crossref | GoogleScholarGoogle Scholar |