Organic acids in the rhizosphere - A critical review

Plant and Soil

Volumn 205, Issue 1, 1998, Pages 25-44

  Jones, David L ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

Author keywords

Bacteria; Fungi; Nutrients; Organic acids; Rhizosphere; Root exudation

Indexed keywords

EID: 0032419655     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1004356007312     Document Type: Review

References (163)

1. Albuzio A and Ferrari G 1989 Modulation of the molecular-size of humic substances by organic acids of the root exudates. Plant Soil 113, 237-241.
2. Anderson H A, Berrow M L, Farmer V C, Hepburn A, Russell J D and Walker A D 1982 A reassessment of podzol formation processes. J. Soil Sci. 33, 125-136.
3. Baziramakenga R, Simard R R and Leroux G D 1995 Determination of organic acids in soil extracts by ion chromatography. Soil Biol. Biochem. 27, 349-356.
4. Barbour W M, Hattermann D R and Stacey G 1991 Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl. Environ. Microbiol. 57, 2635-2639.
5. Bergsma J and Konings W N 1983 The properties of citrate transport in membrane-vesicles from Bacillus subtilis. Eur. J. Biochem. 134, 151-156.
6. Bolan N S, Naidu R, Mahimairaja S and Baskaran S 1994 Influence of low-molecular-weight organic-acids on the solubilization of phosphates. Biol. Fert. Soils 18, 311-319.
7. Boudot J P 1992 Relative efficiency of complexed aluminum, non-crystalline Al hydroxide, allophane and imogolite in retarding the biodegradation of citric acid. Geoderma 52, 29-39.
8. Boudot J P, Belhadj B A and Chone T 1986 Carbon mineralization in andosols and aluminum-rich highland soils. Soil Biol. Biochem. 18, 457-461.
9. Boudot J P, Brahim A B H, Steiman R and Seiglemurandi F 1989 Biodegradation of synthetic organo-metallic complexes of iron and aluminum with selected metal to carbon ratios. Soil Biol. Biochem. 21, 961-966.
10. Bowers J H, Nameth S T, Riedel R M and Rowe R C 1996 Infection and colonization of potato roots by Verticillium dahliae as affected by Pratylenchus penetrans and P. crenatus. Phytopathol. 86, 614-621.
11. Brynhildsen L and Rosswall T 1997 Effects of metals on the microbial mineralization of organic acids. Water Air Soil Pollut. 94, 45-57.
12. Brynhildsen L and Allard B 1994 Influence of metal complexation on the metabolism of citrate by Klebsiella-oxytoca. Biometals 7, 163-169.
13. Brynhildsen L and Rosswall T 1989 Effects of cadmium, copper, magnesium, and zinc on the decomposition of citrate by a Klebsiella sp. Appl. Environ. Microbiol. 55, 1375-1379.
14. Cakmak I and Marschner H 1988 Increase in membrane-permeability and exudation in roots of zinc deficient plants. J. Plant Physiol. 132, 356-361.
15. Cambraia J, Galvani F R, Estevao MM, Santanna R 1983 Effects of aluminum on organic-acid, sugar and amino-acid-composition of the root-system of sorghum (Sorghum bicolor L moench). J. Plant Nutr. 6, 313-322.
16. Cassio F and Leao C 1991 Low-affinity and high-affinity transport-systems for citric acid in the yeast Candida utilis. Appl. Environ. Microbiol. 57, 3623-3628.
17. Chairidchai P and Ritchie G S P 1993a The effect of citrate and pH on zinc uptake by wheat. Agron. J. 85, 322-328.
18. Chairidchai P and Ritchie G S P 1993b Zinc adsorption by sterilized and nonsterilized soil in the presence of citrate and catechol. Comm. Soil Sci. Plant Anal. 24, 261-275.
19. 13C-NMR spectroscopy. Plant Physiol. 89, 97-203.
20. 13C-NMR spectroscopy. Biochim. Biophys. Acta 1092, 29-34.
21. Cline G R, Powell P E, Szaniszlo P J and Reid C P P 1982 Comparison of the abilities of hydroxamic, synthetic, and other natural organic acids to chelate iron and other ions in nutrient solution. Soil Sci. Soc. Am. J. 46, 1158-1164.
22. Côrte-Real M and Leao C 1990 Transport of malic-acid and other dicarboxylic-acids in the yeast Hansenula anomala. Appl. Environ. Microbiol. 56, 1109-1113.
23. Côrte-Real M, Leao C and VanUden N 1989 Transport of L-malic acid and other dicarboxylic-acids in the yeast Candida sphaerica. Appl. Microbiol. Biotechnol. 31, 551-555.
24. Crowley D E, Römheld V, Marschner and Szaniszlo P J 1992 Root-microbial effects on plant iron uptake from siderophores and phytosiderophores. Plant Soil 142, 1-7.
25. Curl E A and Trueglove B 1986 The Rhizosphere. Springer-Verlag, Berlin.
26. Darrah P R 1991a Measuring the diffusion-coefficient of rhizosphere exudates in 2. The diffusion of sorbing compounds. J. Soil Sci. 42, 421-434.
27. Darrah P R 1991b Measuring the diffusion-coefficient of rhizosphere exudates in soil. 1. The diffusion of non-sorbing compounds. J. Soil. Sci. 42, 413-420.
28. Delhaize E, Ryan P R and Randall P J 1993 Aluminum tolerance in wheat (Triticum aestivum L.) 2. Aluminum stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695-702.
29. Dennis D T, Turpin D H, Lefebvre D D and Layzell D B 1997 Plant Metabolism. Longman Group, Essex.
30. De Vos CR, Lubberding HJ and Bienfait HF 1986 Rhizosphere acidification as a response to iron-deficiency in bean plants. Plant Physiol. 81, 842-846.
31. Dinkelaker B, Hengeler C and Marschner H 1995 Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 183-200.
32. Dinkelaker B, Römheld V and Marschner H 1989 Citric-acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ. 12, 285-292.
33. Drever J I and Stillings L L 1997 The role of organic acids in mineral weathering. Colloids Surfaces A: Physicochem. Eng. Aspects 120, 167-181.
34. Dutton M V and Evans C S 1996 Oxalate production by fungi - its role in pathogenicity and ecology in the soil environment. Can. J. Microbiol. 42, 881-895.
35. Earl K D, Syers J K and McLaughlin J R 1979 Origin of citrate, tartrate, and acetate on phosphate sorption by soils and synthetic gels. Soil Sci. Soc. Am. J. 43, 674-678.
36. Ecker D J and Emery T 1983 Iron uptake from ferrichrome A and iron citrate in Ustilago sphaerogena. J. Bacteriol. 155, 616-622.
37. Elkhatib E A 1990 Simultaneous determination of low molecular-weight organic-acids in soil solution by ion chromatography. Z. Pflanzenernähr. Bodenk. 153, 201-205.
38. Evans A 1991 Influence of low-molecular-weight organic-acids on zinc distribution within micronutrient pools and zinc uptake by wheat. J. Plant Nutr. 14, 1307-1318.
39. Fan T W M, Lane A N, Pedler J, Crowley D and Higashi R M 1997 Comprehensive analysis of organic ligands in whole root exudates using nuclear magnetic resonance and gas chromatography mass spectrometry. Anal. Biochem. 251, 57-68.
40. Fedorovich D V, Shavlovskii G M, Dedyshin E E 1989 System of iron transport with participation of citrate in Pichia guilliermondii. Microbiology 58, 289-294.
41. Finan T M, Wood J M and Jordan D C 1981 Succinate transport in Rhizobium leguminosarum. J. Bacteriol. 148, 193-202.
42. Fox T R and Comerford N B 1990 Low-molecular-weight organic-acids in selected forest soils of the Southeastern USA. Soil Sci Soc. Am. J. 54, 1139-1144.
43. Fox T R and Comerford N B 1992 Influence of oxalate loading on phosphorus and aluminum solubility in spodosols. Soil Sci. Soc. Am. J. 56, 290-294.
44. Fox T R, Comerford N B and McFee W W 1990a Phosphorus and aluminum release from a spodic horizon mediated by organic acids. Soil Sci. Soc. Am. J. 54, 1763-1767.
45. Fox T R, Comerford NB and McFee W W 1990b Kinetics of phosphorus release from spodosols - effects of oxalate and formate. Soil Sci. Soc. Am. J. 54, 1441-1447.
46. 2+ in solution. Plant Physiol. 111, 93-100.
47. Foy C D, Lee E H and Wilding S B 1897 Differential aluminum tolerances of two barley cultivars related to organic acids in their roots. J. Plant Nutr. 10, 1089-1101.
48. Francis A J and Dodge C J 1993 Influence of complex structure on the biodegradation of iron-citrate complexes. Appl. Environ. Microbiol. 59, 109-113.
49. Francis A J, Dodge C J and Gillow J B 1992 Biodegradation of metal citrate complexes and implications for toxic-metal mobility. Nature 356, 140-142.
50. 3 and BeO. Geochim. Cosmochim. Acta 50, 1847-1860.
51. Gardner W K, Barber D A and Parberry D G 1983 The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70, 107-114.
52. Gerke J 1992 Phosphate, aluminum and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Z. Pflanzenernähr. Bodenk. 155, 339-343.
53. Gerke J 1993 Solubilization of Fe(III) from humic-Fe complexes, humic Fe oxide mixtures and from poorly ordered Fe-oxide by organic acids: consequences for P-adsorption. Z. Pflanzenernähr. Bodenk. 156, 253-257.
54. Gerke J 1994 Kinetics of soil phosphate desorption as affected by citric acid. Z. Pflanzenernähr. Bodenk. 157, 17-22.
55. Godo G H and Reisenauer H M 1980 Plant effects on soil manganese availability. Soil Sci. Soc. Am. J. 44, 993-995.
56. 13C nuclear-magnetic-resonance studies of malate and citrate synthesis and compartmentation in higher-plant cells. J. Biol. Chem. 268, 3986-3992.
57. Green F and Highley T L 1997 Mechanism of brown-rot decay: Paradigm or paradox. Int. Biodeterioration Biodeg. 39, 113-124.
58. Grierson P F 1992 Organic-acids in the rhizosphere of Banksia integrifolia L. Plant Soil 144, 259-265.
59. Guerinot M L and Yi Y 1994 Iron: nutritious, noxious, and not readily available. Plant Physiol. 104, 815-820.
60. Hoffland E 1992 Quantitative evaluation of the role of organic-acid exudation in the mobilization of rock phosphate by rape. Plant Soil 140, 279-289.
61. Hoffland E, Findenegg G R and Nelemans J A 1989 Solubilization of rock phosphate by rape. 2. Local root exudation of organic acids as a response to P starvation. Plant Soil 113, 161-165.
62. Hoffland E, Van den Boogaard R, Nelemans J and Findenegg G 1992 Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol. 122, 675-680.
63. Huang W H and Keller W D 1972 Organic acids as agents of chemical weathering of silicate minerals. Nature 239, 149-151.
64. Hue N V, Craddock G R and Adams F 1986 Effect of organic-acids on aluminum toxicity in subsoils. Soil Sci. Soc. Am. J. 50, 28-34.
65. Imas P, BarYosef B, Kafkafi U and Ganmore-Neumann R 1997a Phosphate induced carboxylate and proton release by tomato roots. Plant Soil 191, 35-39.
66. Imas P, BarYosef B, Kafkafi U and Ganmore-Neumann R 1997b Release of carboxylic anions and protons by tomato roots in response to ammonium nitrate ratio and pH in nutrient solution. Plant Soil 191, 27-34.
67. Ismail I, DeBellis L, Alpi A and Smith S M 1997 Expression of glyoxylate cycle genes in cucumber roots responds to sugar supply and can be activated by shading or defoliation of the shoot. Plant Mol. Biol. 35, 633-640.
68. Jauregui M A and Reisenauer H M 1982 Dissolution of oxides of manganese and iron by root exudate components. Soil Sci. Soc. Am. J. 46, 314-317.
69. Johnson J F, Allan D L and Vance C P 1994 Phosphorus stress induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol. 104, 657-665.
70. Johnson J F, Allan D L, Vance C P and Weiblen G 1996a Root carbon dioxide fixation by phosphorus-deficient Lupinus albus: Contribution to organic-acid exudation by proteoid roots. Plant Physiol. 112, 19-30.
71. Johnson J F, Vance C P and Allan D L 1996b Phosphorus deficiency in Lupinus albus: altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol. 112, 31-41.
72. Jones D L and Brassington D S 1998 Sorption of organic acids in acid soils and its implications in the rhizosphere. Eur. J. Soil Sci. 49, 447-455.
73. Jones D L and Darrah P R 1994a Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant Soil 163, 1-12.
74. Jones D L and Darrah P R 1994b Role of root derived organic-acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166, 247-257.
75. Jones D L and Darrah P R 1995 Influx and efflux of organic-acids across the soil-root interface of Zea mays L. and its implications in rhizosphere C flow. Plant Soil 173, 103-109.
76. Jones D L and Darrah P R 1996 Re-sorption of organic-compounds by roots of Zea mays L. and its consequences in the rhizosphere. 3. Characteristics of sugar influx and efflux. Plant Soil 178, 153-160.
77. Jones D L and Edwards A C 1998 Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol. Biochem. (In press).
78. Jones D L and Kochian L V 1996 Aluminum-organic acid interactions in acid soils. 1. Effect of root-derived organic-acids on the kinetics of Al dissolution. Plant Soil 182, 221-228.
79. Jones D L, Shaff J E and Kochian L V 1995 Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. 1. Inhibition of tip growth by aluminum. Planta 197, 672-680.
80. Jones D L, Darrah P R and Kochian L V 1996a Critical-evaluation of organic-acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180, 57-66.
81. Jones D L, Prabowo A M and Kochian L V 1996b Aluminum-organic acid interactions in acid soils. 2. Influence of solid-phase sorption on organic acid-Al complexation and Al rhizotoxicity. Plant Soil 182, 229-237.
82. Jones D L, Prabowo A M and Kochian L V 1996c Kinetics of malate transport and decomposition in acid soils and isolated bacterial-populations - the effect of microorganisms on root exudation of malate under Al stress. Plant Soil 182, 239-247.
83. 4, oxalate and fulvate. Eur. J. Soil Sci. 49, 113-120.
84. Keerthisinghe G, Hocking PJ, Ryan P R and Delhaize E 1998 Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.) Plant Cell Environ. 21. (In press).
85. Klein D A, Frederick B A, Biondini M and Trlica M J 1988 Rhizosphere microorganism effects on soluble amino acids, sugars and organic-acids in the root zone of Agropyron cristatum, Agropyron smithii and Bouteloua gracilis. Plant Soil 110, 19-25.
86. Kochian L V 1995 Cellular mechanisms of aluminum toxicity and resistance in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 46, 237-260.
87. Kochian L V and Jones D L 1997 Aluminum toxicity and resistance in plants. In Research Issues in Aluminum Toxicity. Eds. R A Yokel and M S Golub. Taylor and Francis Publishers, Bristol, PA.
88. Kraffczyk I, Trolldenier G and Beringer H 1984 Soluble root exudates of maize: Influence of potassium supply and rhizosphere microorganisms. Soil Biol. Biochem. 16, 315-322.
89. Krzyszowska A J, Blaylock M J, Vance G F and David M B 1996 Ion-chromatographic analysis of low molecular weight organic acids in spodosol forest floor solutions. Soil Sci. Soc. Am. J. 60, 1565-1571.
90. Laheurte F and Berthelin J 1988 Effect of a phosphate solubilising bacteria on maize growth and root exudation over four levels of labile phosphorus. Plant Soil 105, 11-17.
91. Lan M, Comerford N B and Fox T R 1995 Organic anions effect on phosphorus release from spodic horizons. Soil Sci. Soc. Am. J. 59, 1745-1749.
92. Landsberg E C 1981 Organic acid synthesis and release of hydrogen ions in response to Fe deficiency stress of mono- and dicotyledonous plant species. J. Plant Nutr. 3, 579-591.
93. Lipton D S, Blanchar R W and Blevins D G 1987 Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol. 85, 315-317.
94. Lo T C Y, Rayman M K and Sanwal B D 1972 Transport of succinate in E. coli. I. Biochemical and genetic studies of transport in whole cells. J. Biol. Chem. 247, 6323-6331.
95. Lopez-Hernandez D, Siegert G and Rodriguez J V 1986 Competitive adsorption of phosphate with malate and oxalate by tropical soils. Soil Sci. Soc. Am. J. 50, 1460-1462.
96. Lundström U S 1993 The role of organic-acids in the soil solution chemistry of a podzolized soil. J. Soil Sci. 44, 121-133.
97. Lundström U S 1994 Significance of organic-acids for weathering and the podzolization process. Environ. Int. 20, 21-30.
98. Lundström U S and Öhman L O 1990 Dissolution of feldspars in the presence of natural, organic solutes. J. Soil Sci. 41, 359-369.
99. Lundström U S, Van Breemen N and Jongmans A G 1995 Evidence for microbial decomposition of organic acids during podzolization. Eur. J. Soil Sci. 46, 489-496.
100. Lüttge U and Smith J A C 1984 Mechanism of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoe daigremontiana. J. Memb. Biol. 81, 149-158.
101. Ma J F, Hiradate S, Nomoto K, Iwashita T and Matsumoto H 1997 Internal detoxification mechanism of Al in Hydrangea - Identification of Al form in the leaves. Plant Physiol. 113, 1033-1039.
102. Madsen E L and Alexander M 1985 Effects of chemical speciation on the mineralization of organic compounds by microorganisms. Appl. Environ. Microbiol. 50, 342-349.
103. Marschner H 1995 Mineral Nutrition of Higher Plants. Academic Press, London.
104. Martell A E and Smith R M 1976-1989. Critical Stability Constants, 6 vol. Plenum Press, New York.
105. Matsumoto H, Okada K and Takahashi E 1979 Excretion products of maize roots from seedling to seed development stage. Plant Soil 53, 17-26.
106. Mawdsley J L, Burns R G 1994 Root colonization by a Flavobacterium species and the influence of percolating water. Soil Biol. Biochem. 26, 861-870.
107. McAllister C F and Lepo J E 1983 Succinate transport by free-living forms of Rhizobium japonicum. J. Bacteriol. 153, 1155-1162.
108. Mench M and Martin E 1991 Mobilization of cadmium and other metals from two soils by root exudates of Zea mays L, Nicotiana tabacum L and Nicotiana rustica L. Plant Soil 132, 187-196.
109. Meyer J M 1992 Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa: possible involvement of porin OprF in iron translocation. J. Gen. Microbiol. 138, 951-958.
110. Micales J A 1997 Localization and induction of oxalate decarboxylase in the brown-rot wood decay fungus Postia placenta. Int. Biodeterioration Biodegrad. 39, 125-132.
111. Millet M, Wortham H, Sanusi A and Mirabel P 1997 Low molecular weight organic acids in fogwater in an urban area: Strasbourg (France). Sci. Tot. Environ. 206, 57-65.
112. Miyasaka S C, Buta J G, Howell R K and Foy C D 1991 Mechanism of aluminum tolerance in snapbeans: root exudation of citric acid. Plant Physiol. 96, 737-743.
113. Moghimi A, Tate M E and Oades J M 1978 Characterization of rhizosphere products especially 2-ketogluconic acid. Soil Biol. Biochem. 10, 283-287.
114. Nagarajah S, Posner A M and Quirk J P 1970 Competitive adsorptions of phosphate with polygalacturonate and other anions on kaolinite and oxide surfaces. Nature 228, 83-84.
115. Nobel P S 1991 Physiochemical and Environmental Plant Physiology. Academic Press, London.
116. Ohwaki Y and Sugahara K 1997 Active extrusion of protons and exudation of carboxylic acids in response to iron deficiency by roots of chickpea (Cicer arietinum L.).Plant Soil 189, 49-55.
117. Olsen E B, Russell J B and Henick-Kling T 1991 Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation. J. Bacteriol. 173, 6199-6206.
118. Olsson S, Bååth E and Söderström B 1987 Growth of Verticillium dahliae Kleb. hyphae and of bacteria along the roots of rape (Brassica-napus L.) seedlings. Can. J. Microbiol. 33, 916-919.
119. Osmond C B 1976 Ion absorption and carbon metabolism in cells of higher plants. In Encyclopedia of Plant Physiology, New Series, Vol. 2, Part A. Eds. U Lüttge and M G Pitman. pp 347-372. Springer-Verlag, Berlin.
120. Osmond C B and Laties G G 1969 Compartmentation of malate in relation to ion absorption in beet. Plant Physiol. 44, 7-14.
121. Osothsilp C and Subden R E 1986 Malate transport in Schizosaccharomyces pombe. J. Bacteriol. 168, 1439-1443.
122. Papernik L A and Kochian L V 1997 Possible involvement of Al-induced electrical signals in Al tolerance in wheat. Plant Physiol. 115, 657-667.
123. Parker D R, Chaney R L and Norvell W A 1995 Chemical equilibria models: Applications to plant research. In Chemical Equilibria and Reaction Models, Special Publication 42. Eds. R H Loeppert, A P Schwab and S Goldberg. pp 163-200. SSSA-ASA, Madison, WI.
124. Patel D D, Barlow P W and Lee R B 1990 Development of vacuolar volume in the root-tips of pea. Ann. Bot. 65, 159-169.
125. Pellet D M, Grunes D L and Kochian L V 1995 Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196, 788-795.
126. Pellet D M, Papernik L A, Jones D L, Darrah P R, Granes D L and Kochian LV 1997 Involvement of multiple aluminium exclusion mechanisms in aluminium tolerance in wheat. Plant Soil 192, 63-68.
127. Pohlman A A and McColl J G 1986 Kinetics of metal dissolution from forest soils by soluble organic acids. J. Environ. Qual. 15, 86-92.
128. Pohlman A A and McColl J G 1988 Soluble organics from forest litter and their role in metal dissolution. Soil Sci. Soc. Am. J. 52, 265-271.
129. +-ATPase and reductase activities in Fe-deficient cucumber roots. Physiol. Plant. 90, 779-785.
130. Ratnayake M, Leonard R T and Menge J A 1978 Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal infection. New Phytol. 81, 543-552.
131. Ricard B, Couee I, Raymond P, Saglio P H, Saintges V and Pradet A 1994 Plant-metabolism under hypoxia and anoxia. Plant Physiol. Biochem. 32, 1-10
132. Ritchie G S P 1994 Role of dissolution and precipitation of minerals in controlling soluble aluminum in acidic soils. Adv. Agron. 53, 47-83.
133. Rivoal J and Hanson A D 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.
134. Rózycki H 1985 Production of organic acids by bacteria isolated from soil, rhizosphere and mycorrhizosphere of pine (Pinus sylvestris L.). Acta Microbiol. Polon. 34, 301-308.
135. Rózycki H and Strzelczyk E 1986 Organic acids production by Streptomyces spp isolated from soil, rhizosphere and mycorrhizosphere of pine (Pinus sylvestris L.). Plant Soil 96, 337-345.
136. Ryan P R, Delhaize E and Randall P J 1995a Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust. J. Plant Physiol. 122, 531-536.
137. Ryan P R, Delhaize E and Randall P J 1995b Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103-110.
138. Ryan P R, Skerrett M, Findlay G P, Delhaize E and Tyerman S D 1997 Aluminum activates an anion channel in the apical cells of wheat roots. Proc. Natl. Acad. Sci. Am. 94, 6547-6552.
139. +-ATPase in barley roots and effects of K nutrition. Plant Physiol. 99, 1509-1514.
140. SanFrancisco M J D and Jacobson G R 1985 Uptake of succinate and malate in cultured-cells and bacteroids of two slow-growing species of Rhizobium. J. Gen. Microbiol. 131, 765-773.
141. Schwab S M, Menge J A and Leonard R T 1983 Quantitative and qualitative effects of phosphorus on extracts and exudates of sudangrass roots in relation to vesicular-arbuscular mycorrhiza formation. Plant Physiol. 73, 761-765.
142. Shaw J G and Kelly D J 1991 Binding protein dependent transport of C4 dicarboxylates in Rhodobacter capsulatus. Arch. Microbiol. 155, 466-472.
143. Shen Y, Ström L, Jonsson J A and Tyler G 1996 Low-molecular organic-acids in the rhizosphere soil solution of beech forest (Fagus sylvatica L.) cambisols determined by ion chromatography using supported liquid membrane enrichment technique. Soil Biol. Biochem. 28, 1163-1169.
144. Smucker A J M and Erickson A E 1987 Anaerobic stimulation of root exudates and disease of peas. Plant Soil 99, 423-433.
145. Ström L 1997 Root exudation of organic acids: importance to nutrient availability and the calcifuge and calcicole behaviour of plants. Oikos 80, 459-466.
146. Ström L, Olsson T and Tyler G 1994 Differences between calcifuge and acidifuge plants in root exudation of low molecular organic-acids. Plant Soil 167, 239-245.
147. Stumpf D K and Burris R H 1981 Organic-acid contents of soybean: Age and source of nitrogen. Plant Physiol. 68, 989-991.
148. Takao S 1965 Organic acid production by basidiomycetes I. Screening of organic acid producing strains. Appl. Microbiol. 13, 732-737.
149. Tarasov A L, Zvyagintseva I S and Plakunov V K 1991 Citrate transport in Halobacterium distributum cells. Microbiology 60, 19-23.
150. Tourdot-Marechal R, Cavin J F, Dricicachon Z and Divies C 1993 Transport of malic-acid in Leuconostoc oenos strains defective in malolactic fermentation: A model to evaluate the kinetic-parameters. Appl. Microbiol. Biotech. 39, 499-505.
151. Tyler G and Ström L 1995 Differing organic-acid exudation pattern explains calcifuge and acidifuge behavior of plants. Ann. Bot. 75, 75-78.
152. Van der Rest M E, Abee T, Molenaar D and Konings W N 1991 Mechanism and energetics of a citrate-transport system of Klebsiella pneumoniae. Eur. J. Biochem. 195, 71-77.
153. +-dependent citrate transport in Klebsiella pneumoniae. J. Bacteriol. 174, 4893-4898.
154. Van Hees P A W, Andersson A M T and Lundström U S 1996 Separation of organic low-molecular-weight aluminum complexes in soil solution by liquid-chromatography. Chemosphere 33, 1951-1966.
155. Von Wiren N, Romheld V, Shioiri T and Marschner H 1995 Competition between microorganisms and roots of barley and sorghum for iron accumulated in the root apoplasm. New Phytol. 130, 511-521.
156. Welch R M, Norvell W A, Schaefer S C, Shaff J E and Kochian L V 1993 Induction of iron(III) and copper(II) reduction in pea (Pisum sativum L.) roots by Fe and Cu status - does the root-cell plasmalemma Fe(III)-chelate reductase perform a general role in regulating cation uptake? Planta 190, 555-561.
157. Wiehe W, Hechtbuchholz C and Hoflich G 1994 Electron-microscopic investigations on root colonization of Lupinus albus and Pisum sativum with two associative plant-growth promoting rhizobacteria, Pseudomonas fluorescens and Rhizobium leguminosarum bv trifolii. Symbiosis 17, 15-31.
158. Willecke K and Pardee A B 1971 Inducible citrate transport in the gram positive bacterium Bacillus subtilis. J. Biol. Chem. 246, 1032-1040.
159. Willecke K, Fries E M and Oehr P 1972 Coupled transport of citrate and Mg in Bacillus subtilis. J. Biol. Chem. 248, 807-811.
160. Xia J H and Roberts J K M 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 Physiol. 105, 651-657.
161. Xia J H and Saglio P H 1992 Lactic acid efflux as a mechanism of hypoxic acclimation of maize root tips to anoxia. Plant Physiol. 100, 40-46.
162. Zabowski D 1989 Limited release of soluble organics from roots during the centrifugal extraction of soil solutions. Soil Sci. Soc. Am. J. 53, 977-979.
163. Zheng X Y and Sinclair J B 1996 Chemotactic response of Bacillus megaterium strain B153-2-2 to soybean root and seed exudates. Physiol. Mol. Plant Path. 48, 21-35.