More than a carbon economy: Nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses

New Phytologist

Volumn 182, Issue 2, 2009, Pages 347-358

  Smith, F Andrew ^a   Grace, Emily J ^a   Smith, Sally E ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Arbuscular mycorrhizas; Ecological sustainability; Phosphorus (P) uptake; Plant competition; Plant growth depressions; Rhizosphere; Symbiosis

Indexed keywords

PHOSPHORUS;

ARBUSCULAR MYCORRHIZA; COLONIZATION; EVOLUTIONARY BIOLOGY; FUNGUS; GROWTH RATE; GROWTH RESPONSE; INTERSPECIFIC COMPETITION; NUTRIENT UPTAKE; PHOSPHATE; PHOSPHORUS; RHIZOSPHERE; SUSTAINABILITY;

FUNGUS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT; REVIEW; SIGNAL TRANSDUCTION; SYMBIOSIS;

FUNGI; MYCORRHIZAE; PHOSPHORUS; PLANTS; SIGNAL TRANSDUCTION; SYMBIOSIS;

ARBUSCULAR; FUNGI;

EID: 63449117985     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02753.x     Document Type: Review

References (85)

1. Azcón R, Ocampo JA. 1981. Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytologist 87 : 677 685.
2. Baon JB, Smith SE, Alston AM. 1993. Mycorrhizal responses of barley cultivars differing in P efficiency. Plant and Soil 157 : 97 105.
3. de Bary HA. 1879. Die Erscheinung der Symbiose. Strassburg, Germany : Karl J Trübner.
4. Bethlenfalvay GJ, Brown MS, Pacovsky RS. 1982a. Parasitic and mutualistic asssociations between a mycorrhizal fungus and soybean: development of the host plant. Phytopathology 72 : 889 893.
5. Bethlenfalvay GJ, Pacovsky RS, Brown MS. 1982b. Parasitic and mutualistic asssociations between a mycorrhizal fungus and soybean: development of the endophyte. Phytopathology 72 : 894 897.
6. Bryla D, Koide RT. 1998. Mycorrhizal response of two tomato genotypes relates to their ability to acquire and utilize phosphorus. Annals of Botany 82 : 849 857.
7. Burleigh SH, Cavagnaro TR, Jakobsen I. 2002. Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. Journal of Experimental Botany 53 : 1593 1601.
8. Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE. 2004a. Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytologist 161 : 485 494.
9. Cavagnaro TR, Smith FA, Smith SE. 2004b. Interactions between arbuscular mycorrhizal fungi and a mycorrhiza-defective mutant tomato: does a noninfective fungus alter the ability of an infective fungus to colonise the roots - and vice versa? New Phytologist 164 : 485 491.
10. Crush JR. 1973. The effect of Rhizophagus tenuis mycorrhizas on ryegrass, cocksfoot and sweet vernal. New Phytologist 72 : 965 973.
11. Daram P, Brunner S, Persson BL, Amrhein N, Bucher M. 1998. Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta 206 : 225 233.
12. Egger KN, Hibbett DS. 2004. The evolutionary implications of exploitation in mycorrhizas. Canadian Journal of Botany 82 : 1110 1121.
13. Facelli E, Facelli JM, Smith SE, McLaughlin MJ. 1999. Interactive effects of arbuscular mycorrhizal symbiosis, intraspecific competition and resource availability on Trifolium subterraneum cv. Mt Barker. New Phytologist 141 : 535 547.
14. Fitter AH. 1977. Influence of mycorrhizal infection on competition for phosphorus and potassium by two grasses. New Phytologist 79 : 119 125.
15. Fitter AH. 1985. Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytologist 99 : 257 265.
16. Fitter AH. 1991. Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47 : 350 355.
17. Fitter AH. 2006. What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytologist 172 : 3 6.
18. Francis R, Read DJ. 1995. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Canadian Journal of Botany 73 : S1301 S1309.
19. Gao L-L, Delp G, Smith SE. 2001. Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytologist 151 : 477 491.
20. +-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces? New Phytologist 117 : 61 74.
21. Glassop D, Godwin RM, Smith SE, Smith FW. 2007. Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Canadian Journal of Botany 85 : 644 651.
22. Glassop D, Smith SE, Smith FW. 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222 : 688 698.
23. Gordon-Weeks R, Tong YP, Davies TGE, Leggewie G. 2003. Restricted spatial expression of a high-affinity phosphate transporter in potato roots. Journal of Cell Science 116 : 3135 3144.
24. Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE. 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytologist 181 : 938 949.
25. Graham JH. 2008. Scaling-up evaluation of field functioning of arbuscular mycorrhizal fungi. New Phytologist 180 : 1 2.
26. Graham JH, Abbott LK. 2000. Wheat responses to aggressive and nonaggressive arbuscular mycorrhizal fungi. Plant and Soil 220 : 207 218.
27. Graham JH, Leonard RT, Menge JA. 1982. Interaction of light intensity and soil temperature with phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. New Phytologist 91 : 683 690.
28. Harrison MJ, Dewbre GR, Liu JY. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. The Plant Cell 14 : 2413 2429.
29. Hartnett DC, Wilson GWT. 2002. The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant and Soil 244 : 319 331.
30. van der Heijden MGA, Boller T, Wiemken A, Sanders IR. 1998. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79 : 2082 2091.
31. Hetrick BAD, Wilson GWT, Cox TS. 1992. Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Canadian Journal of Botany 70 : 2032 2040.
32. Hetrick BAD, Wilson GWT, Todd TC. 1996. Mycorrhizal response in wheat cultivars: relationship to phosphorus. Canadian Journal of Botany 74 : 19 25.
33. Jakobsen I, Smith SE, Smith FA. 2002. Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. In : van der Heijden MGA, Sanders IR, eds. Mycorrhizal ecology. Berlin, Heidelberg, Germany : Springer-Verlag, 75 92.
34. Janos DP. 1985. Mycorrhizal fungi: agents or symptoms of tropical community composition? In : Molina R, ed. 6th North American Conference on Mycorrhizae. Bend, OR, USA : Forest Research Laboratory, 98 103.
35. Janos DP. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17 : 75 91.
36. Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135 : 575 586.
37. Joner EJ, Magid J, Gahoonia TS, Jakobsen I. 1995. P depletion and activity of phosphatases in the rhizosphere of mycorrhizal and nonmycorrhizal cucumber (Cucumis sativus L.). Soil Biology and Biochemistry 27 : 1145 1151.
38. Jones MD, Smith SE. 2004. Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Canadian Journal of Botany 82 : 1089 1109.
39. Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF. 2000. Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Science 40 : 358 364.
40. Karandashov V, Nagy R, Wegmüller S, Amrhein N, Bucher M. 2004. Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 101 : 6285 6290.
41. Kiers ET, van der Heijden MGA. 2006. Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87 : 1627 1636.
42. Klironomos JN. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84 : 2292 2301.
43. Koide RT. 1991a. Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytologist 117 : 365 386.
44. Koide RT. 1991b. Density-dependent response to mycorrhizal infection in Abutilon theophrasti Medic. Oecologia 85 : 389 395.
45. Koide RT, Schreiner RP. 1992. Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology 43 : 557 581.
46. Li HY, Smith FA, Dickson S, Holloway RE, Smith SE. 2008. Plant growth depressions in arbuscular mycorrhizal symbiosis: not just caused by carbon drain? New Phytologist 178 : 852 862.
47. Li HY, Smith SE, Holloway RE, Zhu Y-G, Smith FA. 2006. Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytologist 172 : 536 543.
48. Li HY, Zhu YG, Marschner P, Smith FA, Smith SE. 2005. Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant and Soil 277 : 221 232.
49. Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG. 1998. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiology 116 : 91 99.
50. Liu H, Trieu AT, Blaylock LA, Harrison MJ. 1998. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and response to colonization by arbuscular mycorrhizal (AM) fungi. Molecular Plant-Microbe Interactions 11 : 14 22.
51. Manjunath A, Habte M. 1991. Root morphological characteristics of host species having distinct mycorrhizal dependency. Canadian Journal of Botany 69 : 671 676.
52. Modjo HS, Hendrix JW. 1986. The mycorrhizal fungus Glomus macrocarpum as a cause of tobacco stunt disease. Phytopathology 76 : 668 691.
53. Mosse B. 1973. Plant growth responses to vesicular-arbuscular mycorrhiza. IV. In soil given additional phosphate. New Phytologist 72 : 127 136.
54. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I. 2004. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytologist 164 : 357 364.
55. Nagy F, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu GH, Jakobsen I, Levy AA, Amrhein N, Bucher M. 2005. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant Journal 42 : 236 250.
56. Neumann E, George E. 2005. Does the presence of arbuscular mycorrhizal fungi influence growth and nutrient uptake of a wild-type tomato cultivar and a mycorrhiza-defective mutant, cultivated with roots sharing the same soil volume? New Phytologist 166 : 601 609.
57. Newsham KK, Fitter AH, Watkinson AR. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends in Ecology and Evolution 10 : 407 411.
58. Paszkowski U, Kroken S, Roux C, Briggs SP. 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 99 : 13324 13329.
59. 33P. New Phytologist 124 : 489 494.
60. 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.
61. Plenchette C, Fortin JA, Furlan V. 1983a. Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. I. Mycorrhizal dependency under field conditions. Plant and Soil 70 : 199 209.
62. Plenchette C, Fortin JA, Furlan V. 1983b. Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. II. Soil fumigation induced stunting of plants corrected by reinoculation of the wild endomycorrhiza flora. Plant and Soil 70 : 211 217.
63. Poulsen KH, Nagy R, Gao LL, Smith SE, Bucher M, Smith FA, Jakobsen I. 2005. Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytologist 168 : 445 453.
64. Pringle A, Bever JD. 2008. Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytologist 180 : 162 175.
65. Rausch C, Daram P, Brunner S, Jansa J, Lalol M, Leggewie G, Amrhein N, Bucher M. 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414 : 462 466.
66. Ravnskov S, Jakobsen I. 1995. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytologist 129 : 611 618.
67. Ravnskov S, Larsen J, Olsson PA, Jakobsen I. 1999. Effects of various organic compounds on growth and phosphorus uptake of an arbuscular mycorrhizal fungus. New Phytologist 141 : 517 524.
68. Read DJ. 2002. Towards ecological relevance - progress and pitfalls in the path towards and understanding of mycorrhizal functions in nature. In : van der Heijden MGA, Sanders IR, eds. Mycorrhizal ecology. Berlin, Heidelberg, Germany : Springer-Verlag, 3 29.
69. Ryan MH, van Herwaarden AF, Angus JF, Kirkegaard JA. 2005. Reduced growth of autumn-sown wheat in a low-P soil is associated with high colonization by arbuscular mycorrhizal fungi. Plant and Soil 270 : 275 286.
70. Sawers RJH, Guthjahr C, Paszkowski U. 2008. Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends in Plant Science 13 : 93 97.
71. Schweiger PF, Jakobsen I. 1999. Direct measurement of arbuscular mycorrhizal phosphorus uptake into field-grown winter wheat. Agronomy Journal 91 : 998 1002.
72. Smith DC. 1991. Forward. In : Margulis L, Fester R, eds. Symbiosis as a source of evolutionary innovation. Cambridge, MA, USA : Massachusetts Institute of Technology Press, ix x.
73. 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.
74. Smith SE, Gianinazzi-Pearson V. 1990. Phosphate uptake and arbuscular activity in mycorrhizal Allium cepa L.: effects of photon irradiance and phosphate nutrition. Australian Journal of Plant Physiology 17 : 177 188.
75. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. London, UK : Academic Press.
76. Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133 : 16 20.
77. Smith SE, Smith FA, Jakobsen I. 2004. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist 162 : 511 524.
78. Smith SE, Tester M, Walker NA. 1986. The development of mycorrhizal root systems in Trifolium subterraneum l.: growth of roots and the uniformity of spatial distribution of mycorrhizal infection units in young plants. New Phytologist 103 : 117 131.
79. Son CL, Smith SE. 1988. Mycorrhizal growth responses: interactions between photon irradiance and phosphorus nutrition. New Phytologist 108 : 305 314.
80. Tawaraya K. 2003. Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Science and Plant Nutrition 49 : 655 668.
81. Thomson BD, Robson AD, Abbott LK. 1986. Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytologist 103 : 751 765.
82. Tinker PB. 1975. Soil chemistry of phosphorus and mycorrhizal effects on plant growth. In : Sanders FE, Mosse B, Tinker PB, eds. Endomycorrhizas. London, UK : Academic Press, 353 371.
83. Urcelay C, Diaz S. 2003. The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity. Ecology Letters 6 : 388 391.
84. West HM, Fitter AH, Watkinson AR. 1993. Response of Vulpia ciliata ssp. ambigua to removal of mycorrhizal infection and to phosphate application under natural conditions. Journal of Ecology 81 : 351 358.
85. Zhu YG, Smith FA, Smith SE. 2003. Phosphorus efficiencies and responses of barley (Hordeum vulgare L.) to arbuscular mycorrhizal fungi grown in highly calcareous soil. Mycorrhiza 13 : 93 100.