Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and heavy metal concentrations

New Phytologist

Volumn 146, Issue 3, 2000, Pages 557-567

  Ahonen Jonnarth, Ulla ^a   Van Hees, Patrick A W ^b   Lundström, Ulla S ^b   Finlay, Roger D ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b MID SWEDEN UNIVERSITY   (Sweden)

Author keywords

Aluminium; Copper; Ectomycorrhiza; Extramatrical mycelium; Heavy metals; Oxalic acid; Pinus sylvestris (Scots pine); Toxicity

Indexed keywords

PAXILLUS INVOLUTUS; PINUS SYLVESTRIS; RHIZOPOGON ROSEOLUS; SUILLUS VARIEGATUS;

EID: 0033922523     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1469-8137.2000.00653.x     Document Type: Article

References (57)

1. Bergkvist B. 1987. Leaching of metals from forest soils as influenced by tree species and management. Forest Ecology and Management 22: 29-56.
2. Blaudez D, Chalot M, Dizengremel P, Botton B. 1998. Structure and function of the ectomycorrhizal associations between Paxillus involutus and Betula pendula. New Phytologist 138: 543-552.
3. Cannon JP, Allen EB, Allen MF, Dudley LM, Jurinak JJ. 1995. The effects of oxalates produced by Salsola tragus on the phosphorus nutrition of Stipa pulchra. Oecologia 102: 265-272.
4. 2 fixation and root exudation of organic acids from wheat cultivars of different aluminium tolerance. Plant and Soil 139: 167-174.
5. Cromack K Jr, Sollins KP, Graustein WC, Speidel T, Todd AW, Spyker G, Li CY, Todd RL. 1979. Calcium oxalate accumulation and soil weathering in mats of the hypogeous fungus Hysterangium crassum. Soil Biology and Biochemistry 11: 463-468.
6. Delhaize E, Ryan PR. 1995. Aluminum toxicity and tolerance in plants. Plant Physiology 107: 315-321.
7. Duchesne LC, Ellis BE, Peterson, RL. 1989. Disease suppression by ectomycorrhizal fungus Paxillus involutus: contribution of oxalic acid. Canadian Journal of Botany 67: 2726-2730.
8. Dutton MV, Evans CS. 1996. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Canadian Journal of Microbiology 42: 881-895.
9. Fink S. 1992. Occurrence of calcium oxalate crystals in non-mycorrhizal fine roots of Picea abies. Journal of Plant Physiology 140: 137-140.
10. Finlay RD. 1989. Functional aspects of phosphorus uptake and carbon translocation in compatible ectomycorrhizal associations between Pinus sylvestris and Boletinus cavipes. New Phytologist 112: 185-192.
11. Fox TR, Comerford NB. 1990. Low-molecular-weight organic acids in selected forest soils of the southerneastern USA. Soil Science Society of America Journal 54: 1139-1144.
12. Godbold DL, Fritz E, Hütterman A. 1988. Aluminum toxicity and forest decline. Proceedings of the National Academy of Sciences, USA 85: 3888-3892.
13. Godbold DL, Horst WJ, Collins JC, Thurman DA, Marschner H. 1984. Accumulation of zinc and organic acids in roots of zinc tolerant and non-tolerant ecotypes of Deschampsia caespitosa. Journal of Plant Physiology 116: 59-69.
14. Göransson A, Eldhuset TD. 1991. Effects of aluminium on growth and nutrient uptake of small Picea abies and Pinus sylvestris. Trees 5: 136-142.
15. Griffiths RP, Baham JE, Caldwell BA. 1994. Soil solution chemistry of ectomycorrhizal mats in forest soil. Soil Biology and Biochemistry 26: 331-337.
16. Harmens H, Koevoets PLM, Verkleij JAC, Ernst WHO. 1994. The role of low molecular organic acids in the mechanism of increased zinc tolerance in Silene vulgaris. New Phystologist 126: 615-621.
17. Hentschel E, Godbold D, Marschner P, Schlegel H, Jentschke G. 1993. The effect of Paxillus involutus Fr. on aluminium sensitivity of Norway spruce seedlings. Tree Physiology 12: 379-390.
18. Homer FA, Reeves RD, Brooks RR, Baker AJM. 1991. Characterization of the nickel-rich extract from the nickel hyperaccumulator Dichapetalum gelonoiodes. Phytochemistry 30: 2141-2145.
19. Huang JW, Pellet DM, Papernik LA, Kochian LV. 1996. Aluminum interactions with voltage-dependent calcium transport in plama-membrane vesicles isolated from roots of aluminium-sensitive and -resistant wheat cultivars. Plant Physiology 110: 561-569.
20. Hue NV, Craddock GR, Adams F. 1986. Effect of organic acids on aluminum toxicity in subsoils. Soil Science Society of America Journal 50: 28-34.
21. Ingestad T. 1979. Mineral nutrient requirements of Pinus silvestris and Picea abies seedlings. Physiologia Plantarum 45: 373-380.
22. Jentschke G, Godbold DL. 2000. Metal toxicity and ectomycorrhizas. Physiologia Plantarum. (In press.)
23. Jones DL. 1998. Organic acids in the rhizosphere - a critical review. Plant and Soil 205: 25-40.
24. Jones DL, Darrah PR. 1994. Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant and Soil 166: 247-257.
25. Jones DL, Prabowo AM, Kochian LV. 1996. 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 and Soil 182: 239-247.
26. Jongmans AG, van Breemen N, Lundström U, Finlay RD, van Hees PAW, Giesler R, Melkerud P-A, Olsson M, Srinivasan M, Unestam T. 1997. Rock-eating fungi. Nature 389: 683-684.
27. Knight WG, Dudley LM, Jurinak JJ. 1992. Oxalate effects on solution phophorus in a calcaerous soil. Arid Soil Research and Rehabilitation 6: 11-20.
28. Kochian LV. 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 46: 237-260.
29. Lapeyrie F, Picatto C, Gerard J, Dexheimer J. 1990. TEM study of intracellular and extracellular calcium oxalate accumulation by ectomycorrhizal fungi in pure culture or in association with Eucalyptus seedlings. Symbiosis 9: 163-166.
30. Lundström US. 1994. Significance of organic acids for weathering and the podsolization process. Environment International 20: 21-30.
31. Ma JF, Zheng SJ, Matsumoto H. 1997a. Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant and Cell Physiology 38: 1019-1025.
32. Ma JF, Zheng SJ, Matsumoto H, Hiradate S. 1997b. Detoxifying aluminium with buckwheat. Nature 390: 569-570.
33. Malajczuk N, Cromack K Jr. 1982. Accumulation of calcium oxalate in the mantle of ectomycorrhizal roots of Pinus radiata and Eucalyptus marginata. New Phytologist 92: 527-531.
34. Matzner E, Prenzel J. 1992. Acid deposition in the German Solling area: effects on soil solution chemistry and Al mobilization. Water Air Soil Pollution 61: 221-234.
35. Nowotny J, Schwanz J, Rothe GM. 1998. Influence of soil acidification and liming on selected enzymes of the carbohydrate metabolism and the contents of two major organic acids of mycorrhizal roots of Norway spruce (Picea abies). Plant and Soil 199: 41-51.
36. Paris F, Bonnaud P, Ranger J, Robert M, Lapeyrie F. 1995. Weathering of ammonium- or calcium-saturated 2: phyllosilicates by ectomycorrhizal fungi in vitro. Soil Biology and Biochemistry 27: 1237-1244.
37. Parker DR, Pedler JF. 1998. Probing the 'malate hypothesis' of differential aluminium tolerance in wheat by using other rhizotoxic ions as proxes for Al. Planta 205: 389-396.
38. Pellet DM, Grunes DL, Kochian LV. 1995. Organic acid exudation as an aluminium-tolerance mechanism in maize (Zea mays). Planta 196: 788-795.
39. Pellet DM, Papernik LA, Jones DL, Darrah PR, Grunes DL, Kochian LV. 1997. Involvement of multiple aluminium exclusion mechanisms in aluminium tolerance in wheat. Plant and Soil 192: 63-68.
40. Rasanayagam S, Jeffries P. 1992. Production of acid is responsible for antibiosis by some ectomycorrhizal fungi. Mycological Research 96: 971-976.
41. Sagner S, Kneer R, Wanner G, Cosson J-P, Deus-Neumann B, Zenk MH. 1998. Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47: 339-347.
42. Schier GA, McQuattie CJ. 1996. Response of ectomycorrhizal and nonmycorrhizal pitch pine (Pinus ngida) seedlings to nutrient supply and aluminium: growth and mineral nutrition. Canadian Journal of Forest Research 26: 2145-2152.
43. Smith SE, Read DJ. 1997. Mycorrhizal symbiosis. London, UK: Academic Press.
44. Snetselaar KM, Whitney KD. 1990. Fungal calcium oxalate in mycorrhizae of Monotropa uniflora. Canadian Journal of Botany 68: 533-543.
45. Stenström E. 1991. The effects of flooding on the formation of ectomycorrhizae in Pinus sylvestris seedlings. Plant and Soil 131: 247-250.
46. Sun Y-P, Unestam T, Lucas SD, Johanson KJ, Kenne KJ, Finlay R. 1999. Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and other microorganisms. Mycorrhiza 9: 137-144.
47. Tamm CO, Andersson F. 1985. Indirect effects of pollutants on plant ecosystems. In: Troyanowski C, ed. Air pollution and plants. Weinheim, Germany: VCH Verlagsgesellschaft mbH, 245-263.
48. Thurman DA, Rankin JL. 1982. The role of organic acids in zinc tolerance in Decharnpsia caespitosa. New Phytologist 91: 629-635.
49. Unestam T. 1991. Water repellency, mat formation, and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1: 13-20.
50. Van Breemen N, Finlay RD, Lundström US, Jongmans AG, Giesler R, Olsson M. 2000a. Mycorrhizal weathering: a true case of mineral plant nutrition? Biogeochemistry 49: 53-67.
51. Van Breemen N, Lundström U, Jongmans AG. 2000b. Do plants drive podzolisation via rock-eating mycorrhizal fungi? Geoderma 94: 163-171.
52. Van Hees PAW, Dahlén J, Lundström US, Borén H, Allard B. 1999. Determination of low molecular weight organic acids in soil solution by HPLC. Talanta 48: 173-179.
53. Wallander H, Nylund J-E. 1992. Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. New Phytologist 120: 495-503.
54. Wallander H, Wickman T. 1999. Biotite and microcline as potassium sources in ectomycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Mycorrhiza 9: 25-32.
55. Wilkins DA. 1991. The influence of sheathing (ecto-)mycorrhizas of trees on the uptake and toxicity of metals. Agriculture, Ecosystems and Environment 35: 245-260.
56. Yang XE, Baligar VC, Foster JC, Martens DC. 1997. Accumulation and transport of nickel in relation to organic acids in ryegrass and maize with different nickel levels. Plant and Soil 196: 271-276.
57. Zheng SJ, Ma JF, Matsumoto H. 1998. High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiology 117: 745-751.