Functioning of mycorrhizal associations along the mutualism-parasitism continuum

New Phytologist

Volumn 135, Issue 4, 1997, Pages 575-585

  Johnson, N C ^a   Graham, J H ^b   Smith, F A ^c  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Cost benefit analysis; Fitness; Mutualism; Mycorrhizal functioning; Parasitism

Indexed keywords

FITNESS; MUTUALISM; MYCORRHIZA; PARASITISM; SYMBIOSIS;

EID: 0031285062     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1469-8137.1997.00729.x     Document Type: Article

References (126)

1. Abbott LK, Robson AD. 1985. Formation of external hyphae in soil by four species of vesicular-arbuscular mycorrhizal fungi. New Phytologist 99: 245-255.
2. Alexander C, Hadley G. 1985. Carbon movement between host and mycorrhizal endophyte during the development of the orchid Goodyera repens Br. New Phytologist 101: 657-665.
3. Allen EB, Allen MF. 1984. Competition between plants of different successional stages: mycorrhizae as regulators. Canadian Journal of Botany 62: 2625-2629.
4. Allen MF, Moore TS, Christensen M. 1980. Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae. I. Cytokinin increases in the host plant. Canadian Journal of Botany 58: 371-374.
5. Allen MF, Allen EB, Friese CF. 1989. Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytologist 111: 45-49.
6. An ZQ, Guo BZ, Hendrix JW. 1993. Mycorrhizal pathogen of tobacco: cropping history and current crop effects on the mycorrhizal fungal community. Crop Protection 12: 527-531.
7. Anderson RC, Hetrick BAD, Wilson GWT. 1994. Mycorrhizal dependence of Andropogon gerardii and Schizachyrium scoparium in two prairie soils. American Midland Naturalist 132: 366-376.
8. Arnolds E. 1991. Decline of ectomycorrhizal fungi in Europe. Agriculture, Ecosystems and Environment 35: 209-244.
9. Baylis GTS 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB, eds. Endomycorrhizas. London: Academic Press, 373-389.
10. Bayne HG, Brown MS, Bethlenfalvay GJ. 1984. Defoliation effects on mycorrhizal colonization, N fixation and photosynthesis in the Glycine-Glomus-Rhizobium symbiosis. Physiologia Plantarum 62: 576-580.
11. Bethlenfalvay GJ, Bayne HG, Pacovsky RS. 1983. Parasitic and mutualistic associations between a mycorrhizal fungus and soybean: the effect of phosphorus on host plant-endophyte interactions. Physiologic. Plantarum 57: 543-548.
12. Bethlenfalvay GJ, Brown MS, Pacovsky RS. 1982. Parasitic and mutualistic associations between a mycorrhizal fungus and soybean: development of the host plant. Phytopathology 72: 889-893.
13. Bethlenfalvay GJ, Franson RL, Brown MS, Mihara KL. 1989. The Glycine-Glomus-Bradyrhizobium symbiosis. IX. Nutritional, morphological and physiological responses of nodulated soybean to geographic isolates of the mycorrhizal fungus Glomus mosseae. Physiologia Plantarum 76: 226-232.
14. Bethlenfalvay GJ, Mihara KL, Schreiner RP. 1994. Mycorrhizae alter protein and lipid contents and yield of pea seeds. Crop Science 34: 998-1003.
15. Björkman E. 1942. Über die Bedingungen der Mykorrhiz-abildung bei Kiefer und Fichte. Symbolae Botanicae Upsaliensis 6: 1-191.
16. Black R, Tinker PB. 1979. The development of endomycorrhizal root systems. II. Effect of agronomic factors and soil conditions on the development of VAM infection in barley and on the endophyte spore density. New Phytologist 83: 401-413.
17. Boucher DH, James S, Keeler KH. 1982. The ecology of mutualism. Annual Review of Ecology and Systematics 13: 315-347.
18. Bougher NL, Grove TS, Malajczuk N. 1990. Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. New Phytologist 114: 77-85.
19. Bowen GD. 1973. Mineral nutrition of mycorrhizas. In: Marks, G. C., Kozlowski T. T. eds. Ectomycorrhizas. New York: Academic Press, 151-201.
20. Bronstein JL. 1994. Our current understanding of mutualism. The Quarterly Review of Biology 69: 31-51.
21. Burgess TI, Malajczuk N, Grove TS. 1993. The ability of 16 ectomycorrhizal fungi to increase growth and phosphorus uptake of Eucalyptus globulus Labill. and E diversicolor F. Muell. Plant and Soil 153: 155-164.
22. Burgess T, Dell B, Malajczuk N. 1994. Variation in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated on to Eucalyptus grandis W. Hill ex Maiden. New Phytologist 127: 731-739.
23. Burkholder PR. 1952. Cooperation and conflict among primitive organisms. American Scientist 40: 601-631.
24. Cherfas J. 1991. Disappearing mushrooms: another mass extinction ? Science 254: 1458.
25. Cushman JH, Beattie AJ. 1991. Mutualisms: assessing the benefits to hosts and visitors. Trends in Ecology and Evolution 6: 193-195.
26. Daft MJ, El-Giahmi AA. 1978. Effect of arbuscular mycorrhiza on plant growth. VIII. Effects of defoliation and light on selected hosts. New Phytologist 80: 365-372.
27. Dawkins R. 1978. The selfish gene. New York: Granada Publishing Company.
28. Dehne H. W. 1982. Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72: 115-1119.
29. Dickson S, Smith SE. 1991. Quantification of active vesicular-arbuscular mycorrhizal infection using image analysis and other techniques. Australian Journal of Plant Physiology 18: 637-648.
30. Dosskey MG, Linderman RG, Boersma L. 1990. Carbon-sink stimulation of photosynthesis in Douglas fir seedlings by some ectomycorrhizae. New Phytologist 115: 269-274.
31. Duckmanton L, Widden P. 1994. Effect of ozone on the development of vesicular-arbuscular mycorrhizae in sugar maple saplings. Mycologia 86: 181-186.
32. Eissenstat DM, Graham JH, Syvertsen JP, Drouillard DL. 1993. Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Annals of Botany 71: 1-10.
33. Fitter AH. 1985. Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytologist 99: 257-265.
34. Fitter AH, 1991. Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47: 350-355.
35. Fitter AH, Garbaye J. 1994. Interactions between mycorrhizal fungi and other soil organisms. Plant and Soil 159: 123-132.
36. Fitter AH, Nichols R. 1988. The use of benomyl to control infection by vesicular-arbuscular mycorrhizal fungi. New Phytologist 110: 201-206.
37. Francis R, Read DJ. 1984. Direct transfer of C between plants connected by vesicular-arbuscular mycorrhizal mycelium Nature 307: 53-56.
38. Francis R, Read DJ. 1994. The contributions of mycorrhizal fungi to the determination of plant community structure. Plant and Soil 159: 11-25.
39. Friese CF, Allen MF. 1991. Tracking the fates of exotic and local VA mycorrhizal fungi: methods and patterns. Agriculture Ecosystems and Environment 34: 87-96.
40. Gange AC, Brown VK. 1992. Interactions between soil-dwelling insects and mycorrhizas during early plant succession. In : Read DJ, Lewis DH, Fitter AH, Alexander IJ, eds. Mycorrhizas in Ecosystems. Oxford: C. A. B. International, 177-182.
41. Garbaye J, Bowen GD. 1987. Effect of different microflora on the success of ectomycorrhizal inoculation of Pinus radiata. Canadian Journal of Forest Research 17: 941-943.
42. Gardes M, Bruns T. 1993. ITS primers with enhanced specificity for basidiomycetes: application to identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
43. Gehring CA, Whitham TG. 1994. Comparisons of ectomycorrhizae on pinyon pines (Pinus edulus; Pinaceae) across extremes of soil type and herbivory. American Journal of Botany 81: 1509-1516.
44. Gehring CA, Whitham TG. 1995. Duration of herbivore removal and environmental stress affect the ectomycorrhizae of pinyon pines. Ecology 76: 2118-2123.
45. Gerdemann JW. 1970. The significance of vesicular-arbuscular mycorrhizae in plant nutrition. In: Toussoun TA, Bega RV, Nelson PE, eds. Root diseases and Soil-borne Plant Pathogens. Berkeley, USA: University of California Press, 125-129.
46. Graham JH. 1988. Interactions of mycorrhizal fungi with soil-borne plant pathogens and other organisms: an introduction. Phytopathology 78: 365-366.
47. Graham JH, Drouillard DL, Hodge NC. 1996. Carbon economy of sour orange in response to different Glomus spp. Tree Physiology 16: 1023-1029.
48. Graham JH, Duncan LW, Eissenstat DM. 1997. Carbohydrate allocation patterns in citrus genotypes as affected by phosphorus nutrition, mycorrhizal colonization and mycorrhizal dependency. New Phytologist 135: 335-343.
49. Graham JH, Eissenstat DM. 1994. Host genotype and the formation and function of VA mycorrhizae. Plant and Soil 159: 179-185.
50. Graham JH, Eissenstat DM. 1996. Field demonstration of carbon cost of mycorrhizae on young Valencia orange trees at high P supply. Program and Abstracts of the First International Conference on Mycorrhizae. August 4-9, 1996. Berkeley, California, USA, 54.
51. Graham JH, Hodge NC, Morton JB. 1995. Fatty acid methyl ester profiles for characterization of Glomalean fungi and their endomycorrhizae. Applied Environmental Microbiology 61: 58-64.
52. Graham JH, Linderman RG, Menge JA. 1982. Development of external hyphae by different isolates of mycorrhizal Glomus spp. in relation to root colonization and growth of Troyer citrange. New Phytologist 91: 183-189.
53. Graham JH, Syvertsen JP. 1985. Host determinants of mycorrhizal dependency of citrus rootstock seedlings. New Phytologist 101: 667-676.
54. Grime JP, Mackey JML, Hillier SH, Read DJ. 1987. Floristic diversity in a model system using experimental microcosms. Nature 328: 420-422.
55. Hahn A, Gianinizzi-Pearson V, Hock B. 1994. Characterization of arbuscular fungi by immunochemical techniques. In: Gianiazzi S, Schuepp H, eds. Impact of Arbuscular Fungi on Sustainable Agriculture and Natural Ecosystems. Basel, Switzerland : Birkhauser, 25-39.
56. Harley JL. 1992. Mycorrhizae. McGraw-Hill Encyclopedia of Science and Technology. Volume 11, 7th edition, 545-546.
57. Hayman DS. 1974. Plant growth responses to VA mycorrhiza VI. Effect of light and temperature. New Phytologist 73: 71-80.
58. Hendrix JW, Jones KJ, Nesmith WC. 1992. Control of pathogenic mycorrhizal fungi in maintenance of soil productivity by crop rotation. Journal of Agriculture Production 5: 383-386.
59. Hendrix JW, Guo BZ, An Z-Q. 1995. Divergence of mycorrhizal fungal communities in crop production systems. Plant and Soil 170: 131-140.
60. Hetrick BAD, Kitt DG, Wilson GWT. 1988. Mycorrhizal dependence and growth habit of warm-season and cool-season tallgrass prairie plants. Canadian Journal of Botany 66: 1376-1380.
61. Hetrick BAD, Wilson GWT. 1991. Effects of mycorrhizal fungus species and metalaxyl application on microbial supression of mycorrhizal symbiosis. Mycologia 83: 97-102.
62. Hetrick BAD, Wilson GWT, Leslie JF. 1991. Root architecture of warm- and cool-season grasses: relationship to mycorrhizal dependence. Canadian Journal of Botany 69: 112-118.
63. Jaenike J. 1991. Mass extinction of European fungi. Trends in Ecology and Evolution 6: 174-175.
64. Jakobsen I. 1991. Carbon metabolism in mycorrhiza. In: Norris JR, Read DJ, Varma AK, eds. Methods in Microbiology, vol. 23. London: Academic Press: 149-180.
65. Jakobsen I. 1994. Research approaches to study the functioning of vesicular-arbuscular mycorrhizas in the field. Plant and Soil 159: 141-147.
66. Jakobsen I, Abbott LK, Robson AD. 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 120: 371-380.
67. Janos DP. 1985. Mycorrhizal fungi: agents or symptoms of tropical community succession ? In: Molina R, ed. Proceedings of the 6th NACOM., Corvallis, OR, USA: Oregon State University, 98-106.
68. Janos D. P. 1987. VA mycorrhizas in humid tropical ecosystems. In: Safir G, ed. VA Mycorrhizae: an Ecophysiological Approach., Boca Raton, EL, USA: CRC Press, 107-134.
69. Janos DP. 1996. Mycorrhizas, succession, and the rehabilitation of deforested lands in the humid tropics. In: Frankland JC, Magan N, Gadd GM, eds. Fungi and Environmental Change. Cambridge, UK: Cambridge University Press, 129-162.
70. Jasper DA, Abbott LK, Robson AD. 1991. The effect of soil disturbance on vesicular-arbuscular mycorrhizal fungi in soils from different vegetation types. New Phytologist 118: 471-476.
71. Johnson, NC. 1993. Can fertilization of soil select less mutualistic mycorrhizae ? Ecological Applications 3: 749-757.
72. Johnson NC, Pfleger FL. 1992. Vesicular-arbuscular mycorrhizae and cultural stresses. In: Bethlenfalvay GJ, Linderman RG, eds. Mycorrhizae in Sustainabie Agriculture. Special Publication no. 54 American Society of Agonomy, Madison, Wisconsin, USA, 71-99.
73. Jones K, Hendrix JW. 1987. Inhibition of root extension in tobacco by the mycorrhizal fungus Glomus macrocarpum and its prevention by benomyl. Soil Biology and Biochemistry 19: 297-300.
74. Kiernan JM, Hendrix JW, Maronek DM. 1983. Fertilizer-induced pathogenicity of mycorrhizal fungi to sweetgum seedlings. Soil Biology and Biochemistry 15: 257-262.
75. Klironomos JN. 1995. Arbuscular mycorrhizae of Acer saccharum in different soil types. Canadian Journal of Botany 73: 1824-1830.
76. Koide R. 1985. The nature of growth depressions in sunflower caused by vesicular-arbuscular mycorrhizal infection. New Phytologist 99: 449-462.
77. Koide RT. 1991. Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytologist 117: 365-386.
78. Koide R, Elliot G. 1989. Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Functional Ecology 3: 252-255.
79. Lambert DH, Cole H. 1980. Effects of mycorrhizae on establishment and performance of forage species in mine spoil. Agronomy Journal 72: 257-260.
80. Leake JR. 1994. The biology of myco-heterotrophic ('saprophytic') plants. New Phytologist 127: 171-216.
81. Lewis DH. 1985. Symbiosis and mutualism: crisp concepts and soggy semantics. In : Boucher DH, ed. The Biology of Mutualism Ecology and Evolution, London: Croom Helm, 29-39.
82. Linderman RG. 1988. Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78: 366-371.
83. Lu X, Koide RT. 1994. The effects of mycorrhizal infection on components of plant growth and reproduction. New Phytologist 128: 211-218.
84. Malajczuk N. 1988. Interaction between Phytophthora cinn- amomi zoospores and microorganisms on nonmycorrhizal and ectomycorrhizal roots of Eucalyptus marginata. Transactions of the British Mycological Society 90: 375-382.
85. Marschner H, Dell B. 1994. Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 159: 89-102.
86. Marx DH. 1972. Ectomycorrhizae as biological deterents to pathogenic root infections. Annual Review of Phytopathology 10: 429-154.
87. McGonigle TP, Fitter AH. 1988. Ecological consequences of arthropod grazing on VA mycorrhizal fungi. Proceedings of the Royal Society of Edinburgh 94b: 25-32.
88. McGonigle TP, Miller MH. 1993. Mycorrhizal development and phosphorus absorption in maize under conventional and reduced tillage. Soil Science Society of America Journal 57: 1002-1006.
89. McGonigle TP, Miller MH. 1996. Mycorrhizae, phosphorus absorption, and yield of maize in response to tillage. Soil Science Society of America Journal 60: 1856-1861.
90. Miller DD, Domoto PA, Walker C. 1985. Colonization and efficacy of different endomycorrhizal fungi with apple seedlings at two phosphorus levels. New Phytologist 100: 393-402.
91. Miller RM, Jarstfer AG, Pillai JK. 1986. Biomass allocation in an Agropyron smithii and Glomus symbiosis. American Journal of Botany 74: 114-122.
92. Miller RM, Jastrow JD. 1990. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biology and Biochemistry 22: 579-584.
93. Miller RM, Jastrow JD. 1992. The application of VA mycorrhizae to ecosystem restoration and reclamation. In: Allen MF, ed. Mycorrhizal Functioning. New York: Chapman & Hall, 438-167.
94. Modjo HS, Hendrix JW. 1986. The mycorrhizal fungus Glomus macrocarpum as a cause of tobacco stunt disease. Phytopathology 76: 688-691.
95. Modjo HS, Hendrix JW, Nesmith WC. 1987. Mycorrhizal fungi in relation to control of tobacco stunt disease with soil fumigants. Soil Biology and Biochemistry 19: 289-295.
96. Molina R. 1979. Ectomycorrhizal inoculation of containerized Douglas-fir and Lodgepole pine seedlings with six isolates of Pisolithus tinctorius. Forest Science 25: 585-590.
97. Mosse B. 1973. Plant growth responses to vesicular-arbuscular mycorrhizas. IV. In soil given additional phosphorus. New Phytologist 72:127-136.
98. Newman EI, Reddell P. 1987. The distribution of mycorrhizas among families of vascular plants. New Phytologist 106: 745-751.
99. Newsham KK, Fitter AH, Watkinson AR. 1994. Root pathogenic and arbscular mycorrhizal fungi determine fecundity of asymptomatic plants in the field. Journal of Ecology 82: 805-814.
100. O'Neill EG, O'Neill RV, Norby RJ. 1991. Hierarchy theory as a guide to mycorrhizal research on large-scale problems. Environmental Pollution 73: 271-284.
101. Pacovsky RS, Bethlenfalvay GJ, Paul EA. 1986. Comparisons between P-fertilized and mycorrhizal plants. Crop Science 26: 151-156.
102. Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC. 1993. Growth depression in mycorrhizal citrus at high-phosphorus supply: analysis of carbon costs. Plant Physiology 101: 1063-1071.
103. Perry DA, Molina R, Amaranthus MP. 1987. Mycorrhizae, mycorrhizospheres, and reforestation: current knowledge and research needs. Canadian Journal of Forest Research 17: 929-940.
104. Perry DA, Amaranthus MP, Borchers JG, Borchers SL, Brainerd RE. 1989. Bootstrapping in ecosystems. Bioscience 39: 230-237.
105. Pope PE, Chaney WR, Rhodes JD, Woodhead SH. 1983. The mycorrhizal dependency of four hardwood tree species. Canadian Journal of Botany 61: 412-417.
106. Rygiewicz PT, Andersen CP. 1994. Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369: 58-60.
107. Rosendahl S. 1992. Influence of 3 vesicular-arbuscular mycorrhizal fungi (Glomaceae) on the activity of specific enzymes in the root system of Cucumis sativus L. Plant and Soil 144: 219-226.
108. Sanders FE, Tinker PB, Black RLE, Palmerley SM. 1977. The development of endomycorrhizal root systems. I. Spread of infection and growth-promoting effects with four species of vesicular-arbuscular mycorrhizas. New Phytologist 78: 257-268.
109. Sanders IR, Alt M, Groupe K, Boller T, Wiemken A. 1995 a. Identification of ribosomal DNA polymorphisms in and among spores of the Glomales-application to studies on the genetic diversity of arbuscular mycorrhizal fungal communities. New Phytologist 130: 419-427.
110. Sanders IR, Clapp JP, Wiemken A. 1996. The genetic diversity of arbuscular mycorrhizal fungi in natural ecosystems-a key to understanding the ecology and functioning of the mycorrhizal symbiosis. New Phytologist 133: 123-134.
111. Sanders IR, Koide RT, Shumway DL. 1995 b. Community-level interactions between plants and vesicular-arbuscular mycorrhizal fungi In: Varma A, Hock B, eds. Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology, Berlin: Springer-Verlag, 607-625.
112. Silberbush M. Barber SA. 1983. Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model. Plant and Soil 74: 93-100.
113. Smith DC, Douglas AE. 1987. The biology of symbiosis. London: Edward Arnold.
114. Smith FA, Smith SE. 1996. Mutualism and parasitism: diversity in function and structure in the 'arbuscular'(VA) mycorrhizal symbiosis. Advances in Botanical Research 22: 1-43.
115. Soberon JM, Martinez del Rio C. 1985. Cheating and taking advantage in mutualistic associations. In : Boucher DH, ed. The Biology of Mutualism Ecology and Evolution. London: Croom Helm, 192-216.
116. Son CL, Smith SE. 1988. Mycorrhizal growth responses: interactions between photon irradiance and phosphorus nutrition. New Phytologist 108: 305-314.
117. Streitwolf-Engel R, Boller T, Wiemken A, Sanders I. 1997. Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from calcareous grasslands. Journal of Ecology, 85: 181-191.
118. Sylvia DM, Wilson DO, Gaham JH, Maddox JJ, Millner P, Morton JB, Skipper HD, Wright SF, Jarstfer AG. 1993. Evaluation of vesicular-arbuscular mycorrhizal fungi in diverse plants and soils. Soil Biology and Biochemistry 25: 705-713.
119. Thompson JP. 1987. Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops and its expression in phosphorus deficiency of sunflower. Australian Journal of Agricultural Research 38: 847-867.
120. Tinker PB, Durall DM, Jones MD. 1994. Carbon use efficiency in mycorrhizas : theory and sample calculations. New Phytologist 128: 115-122.
121. Trappe JM 1994. What is a mycorrhiza ? Proceedings of the fourth European Symposium on Mycorrhizae, Granada, Spain July, 1994.
122. Vitousek PM. 1994. Beyond global warming: ecology and global change. Ecology 75: 1861-1876.
123. Vitousek PM, Matson PA. 1993. Agriculture, the global nitrogen cycle, and trace gas flux. In: Oremland R. S. ed. The Biogeochemistry of Global Change: Radiative Trace Gases. New York: Chapman & Hall 193-208.
124. 4 plants linked by a common mycorrhizal network. Soil Biology and Biochemistry 28: 471-477.
125. Wedin DA, Tilman DG. 1996. Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274: 1720-1723.
126. Wilson G, Hartnett D. 1996. Mycorrhizal influence on floristic composition and diversity in tallgrass prairie. Program and abstracts of the First International Conference on Mycorrhizae. 4-9 August 1996. Berkeley, California, USA, 127.