Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales

Annual Review of Plant Biology

Volumn 62, Issue , 2011, Pages 227-250

  Smith, Sally E ^a   Smith, F Andrew ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

mycorrhizal growth responses; nitrogen uptake; phosphorus uptake; plant nutrient uptake pathways

Indexed keywords

NITROGEN; PHOSPHORUS;

ARTICLE; BIOLOGICAL MODEL; ECOSYSTEM; FUNGUS HYPHAE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT; PLANT ROOT; SIGNAL TRANSDUCTION; SYMBIOSIS;

ECOSYSTEM; HYPHAE; MODELS, BIOLOGICAL; MYCORRHIZAE; NITROGEN; PHOSPHORUS; PLANT ROOTS; PLANTS; SIGNAL TRANSDUCTION; SYMBIOSIS;

ARBUSCULAR; EMBRYOPHYTA;

EID: 79955614493     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042110-103846     Document Type: Article

References (153)

1. Ames RN, Reid CPP, Porter L, Cambardella C. 1983. Hyphal uptake and transport of nitrogen from two 15N-labeled sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol. 95:381-96.
2. Avio L, Pellegrino E, Bonari E, Giovannetti M. 2006. Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol. 172:347-57. (Pubitemid 44414121)
3. Bago B, Azcón-Aguilar C. 1997. Changes in the rhizospheric pH induced by arbuscular mycorrhiza formation in onion (Allium cepa L.). Zt. Pflanzenern. Bdkde 160:333-9. (Pubitemid 127705767)
4. Bago B, Azcón-Aguilar C, Goulet A, Pich́e Y. 1998. Branched adsorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytol. 139:375-88. (Pubitemid 28320655)
5. Bago B, Pfeffer P, Shachar-Hill Y. 2001. Could the urea cycle be translocating nitrogen in the arbuscular mycorrhizal symbiosis? New Phytol. 149:4-8. (Pubitemid 32099888)
6. Bago B, Vierheilig H, Pich́e Y, Azcón-Aguilar C. 1996. Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol. 133:273-80. (Pubitemid 126572511)
7. Balestrini R, Bonfante P. 2005. The interface compartment in arbuscular mycorrhizae: A special type of plant cell wall? Plant Biosyst. 139:8-15. (Pubitemid 40554744)
8. Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P. 2007. Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter are contemporaneously present in arbusculated cells. Mol. Plant-Microbe Interact. 20:1055-62. (Pubitemid 47281772)
9. Bethlenfalvay GJ, Bayne HC, Pacovsky RS. 1983. Parasitic and mutualistic association between a mycorrhizal fungus and soybean. Physiol. Plant. 57:543-49.
10. Bonfante P, Genre A. 2008. Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci. 13:292-98.
11. Branscheid A, Sieh D, Pant BD, May P, Devers EA, et al. 2010. Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol. Plant-Microbe Interact. 23:915-26.
12. Bucher M. 2007. Functional biology of plant phosphate uptake at root andmycorrhiza interfaces. New Phytol. 173:11-26. (Pubitemid 44924237)
13. Capellazzio G, Lanfranco L, Fitz M, Wipf D, Bonfante P. 2008. Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol. 147:429-37. (Pubitemid 352844369)
14. Cavagnaro TR, Gao L-L, Smith FA, Smith SE. 2001. Morphology of arbuscular mycorrhizas is influenced by fungal identity. New Phytol. 151:469-75. (Pubitemid 32722370)
15. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, et al. 2006. Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209-25. (Pubitemid 43961537)
16. Cavagnaro TR, Smith FA, Ayling SM, Smith SE. 2003. Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytol. 157:127-34. (Pubitemid 36128456)
17. Cavagnaro TR, Smith FA, HayG, Carne-Cavagnaro VL, Smith SE. 2004. 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 Phytol. 161:485-94. (Pubitemid 38126960)
18. Christophersen HM, Smith FA, Smith SE. 2009. Arbuscular mycorrhizal colonization reduces arsenate uptake in barley via downregulation of transporters in the direct epidermal phosphate uptake pathway. New Phytol. 184:962-74.
19. Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, et al. 2007. Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol. 114:782-92. (Pubitemid 46944743)
20. Daram P, Brunner S, Persson BL, Amrhein N, Bucher M. 1998. Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta 206:225-33. (Pubitemid 28403795)
21. Dickson S. 2004. The Arum-Paris continuum of mycorrhizal symbioses. New Phytol. 163:187-200. (Pubitemid 38826186)
22. Dickson S, Smith FA, Smith SE. 2007. Structural differences in arbuscular mycorrhizal symbioses: More than 100 years after Gallaud, where next? Mycorrhiza 17:375-93. (Pubitemid 46988236)
23. Drew EA, Murray RS, Smith SE, Jakobsen I. 2003. Beyond the rhizosphere: growth and function of arbuscular mycorrhizal external hyphae in sands of varying pore sizes. Plant Soil 251:105-14. (Pubitemid 36684538)
24. Drissner D, KunzeG,CallewaertN,Gherig P,Tamasloukht MB, et al. 2007. Lyso-phosphatidylcholine is a signal in the arbuscular mycorrhizal symbiosis. Science 318:265-68. (Pubitemid 47574852)
25. Dupŕe de Boulos H, Voets L, Delvaux B, Jakobsen I, Declerk S. 2006. Transport of radiocaesium by arbuscular mycorrhizal fungi to Medicago truncatula under in vitro conditions. Environ.Microbiol. 8:1926-34. (Pubitemid 44506889)
26. Ezawa T, Smith SE, Smith FA. 2002. P metabolism and transport in AM fungi. Plant Soil 244:221-30.
27. Facelli E, Smith SE, Facelli JM, Christophersen HM, Smith FA. 2010. Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytol. 185:1050-61.
28. Feddermann N, Finlay R, Boller T, Elfstrand M. 2010. Functional diversity in arbuscular mycorrhiza- the role of gene expression, phosphorus nutrition and symbiotic efficiency. Fungal Ecol. 3:1-8.
29. Ferrol N, Barea JM, Azcón-Aguilar C. 2000. The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr. Genet. 37:112-18. (Pubitemid 30160523)
30. Fitter AH. 2006. What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytol. 172:3-6. (Pubitemid 44268107)
31. Francis R, Read DJ. 1995. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can. J. Bot. 73:S1301-9. (Pubitemid 26452285)
32. Gallaud I. 1905. Études sur lesmycorrhizes endotrophes. Rev. Ǵen. Bot. 17:5-48, 66-83, 123-35, 223-39, 313-25, 425-33, 79-500.
33. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. 2008. Prepenetration apparatus asssembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortext of both Medicago truncatula and Daucus carota. Plant Cell 20:1407-20. (Pubitemid 352844191)
34. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. 2005. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489-99.
35. George E, Haeussler K-U, VetterleinD,Gorgus E, MarschnerH. 1992. Water and nutrient translocation by hyphae of Glomus mosseae. Can. J. Bot. 70:2130-37.
36. George E, Marschner H, Jakobsen I. 1995. Role of arbuscular mycorrizal fungi in uptake of phosphorus and nitrogen from soil. Crit. Rev. Biotechnol. 15:257-70.
37. Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M, Gianinazzi S. 2000. Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211:609-13.
38. Gianinazzi-Pearson V, Smith SE,Gianinazzi S, Smith FA. 1991. Enzymatic studies on themetabolism of vesicular-arbuscular mycorrhizas. V. IsH+-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces? New Phytol. 117:61-74.
39. Gordon-Weeks R, Tong YP, Davies TGE, Leggewie G. 2003. Restricted spatial expression of a highaffinity phosphate transporter in potato roots. J. Cell Sci. 116:3135-44. (Pubitemid 37038962)
40. GovindarajuluM, Pfeffer P, JinH, Abubaker J, Douds D, et al. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819-23. (Pubitemid 40839732)
41. 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 Phytol. 181:938-49.
42. Grace EJ, Smith FA, Smith SE. 2009. Deciphering the arbuscular mycorrhizal pathway of P uptake in nonresponsive host plant species. In Mycorrhizas-Functional Processes and Ecological Impact, ed. C Azcón-Aguilar, JM Barea, S Gianinazzi, V Gianinazzi-Pearson, pp. 89-106. Berlin: Springer.
43. Graham JH. 2008. Scaling-up evaluation of field functioning of arbuscular mycorrhizal fungi. New Phytol. 180:1-2.
44. Graham JH, Abbott LK. 2000. Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207-18. (Pubitemid 30392646)
45. Graham JH, Leonard RT, Menge JA. 1982. Interaction of light intensity and soil temperature with phosphorus inhibition of vesicular arbuscular mycorrhiza formation. New Phytol. 91:683-90.
46. Gu M, Chen AQ, Zhu YY, Tang GL, et al. 2010. Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol. Plant. 138:226-37.
47. Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P. 2009. A mycorrhizalspecific ammonium transporter from Lotus japonicus aquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 150:73-83.
48. Guo BZ, An ZQ, Hendrix JW. 1994. A mycorrhizal pathogen (Glomus macrocarpum Tul. & Tul.) of tobacco: effects of long- and short-term cropping on the mycorrhizal fungal community and stunt disease. Appl. Soil Ecol. 1:269-76.
49. GuttenbergerM. 2000. Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211:299-304.
50. Harrison MJ. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev. Microbiol. 59:19-42. (Pubitemid 41507422)
51. Harrison MJ, Dewbre GR, Liu JY. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413-29. (Pubitemid 35235287)
52. Harrison MJ, van Buuren ML. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626-32.
53. Hawkins HJ, George E. 2001. Reduced 15N-nitrogen transport through arbuscular mycorrhizal hyphae to Triticum aestivum L. supplied with ammonium versus nitrate nutrition. Ann. Bot. 87:303-11. (Pubitemid 32608145)
54. Hawkins HJ, Johansen A, George E. 2000. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275-85. (Pubitemid 32100688)
55. Hetrick BAD, Wilson GWT, Schwab AP. 1994. Mycorrhizal activity in warm- and cool-season grasses: variation in nutrient uptake strategies. Can. J. Bot. 72:1002-8. (Pubitemid 2138889)
56. Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T. 2010. Polyphosphate has a central role in the rapid andmassive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol. 186:285-89.
57. Hodge A. 2001. Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytol. 151:725-34. (Pubitemid 32812105)
58. Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297-99. (Pubitemid 32905848)
59. Hodge A, Robinson D, Fitter AH. 2000. An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytol. 145:575-84. (Pubitemid 30165923)
60. Jackson LE, Burger M, Cavagnaro TR. 2008. Roots, nitrogen transformations, and ecosystem services. Annu. Rev. Plant Biol. 59:341-63.
61. Jakobsen I. 1999. Transport of phosphorus and carbon in arbuscularmycorrhizas. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology, ed. A Varma, B Hock, pp. 309-32. Berlin: Springer.
62. Jakobsen I. 2004. Hyphal fusion to plant species connections-giant mycelia and community nutrient flow. New Phytol. 164:4-7. (Pubitemid 39260322)
63. Jakobsen I, Abbott LK, Robson AD. 1992. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytol. 120:509-16. (Pubitemid 23396559)
64. Janos D. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75-91. (Pubitemid 46363645)
65. Jansa J, Mozafar A, Frossard E. 2003. Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481-88. (Pubitemid 37110538)
66. Jansa J, Smith FA, Smith SE. 2008. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol. 177:779-89.
67. Javot H, Penmetsa RV, Terzaghi N, Cooke DR, Harrison MJ. 2007. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 104:1720-25. (Pubitemid 46214657)
68. Javot H, Pumplin N, Harrison MJ. 2007. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ. 30:310-22. (Pubitemid 46184432)
69. Jin H, Pfeffer P, Douds D, Piotrowski E, Lammers P, Shachar Hill Y. 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 168:687-96.
70. Johansen A, Finlay RD, Olsson PA. 1996. Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 133:705-12. (Pubitemid 126548865)
71. Johansen A, Jakobsen I, Jensen ES. 1992. Hyphal transport of 15N-labeled nitrogen by a vesiculararbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol. 122:281-88. (Pubitemid 23399550)
72. Johansen A, Jakobsen I, Jensen ES. 1993. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 3. Hyphal transport of 32P and 15N. New Phytol. 124:61-68.
73. Johansen A, Jakobsen I, Jensen ES. 1993. Hyphal transport by a vesicular-arbuscular mycorrhizal fungus of N applied to the soil as ammonium or nitrate. Biol. Fertil. Soils 16:66-70.
74. Johnson NC. 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas accross scales. New Phytol. 185:631-47.
75. Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135:575-86. (Pubitemid 28013891)
76. Jones MD, Smith SE. 2004. Exploring functional definitions of mycorrhizas: Are mycorrhizas always mutualisms? Can. J. Bot. 82:1089-109. (Pubitemid 39501016)
77. Kaldorf M, Schmelzer E, Bothe H. 1998. Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol. Plant-Microbe Interact. 11:439-48. (Pubitemid 28244569)
78. Karandashov V, Nagy R, Wegmüller S, Amrhein N, Bucher M. 2004. Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 101:6285-90. (Pubitemid 38520566)
79. Kiers ET, van der Heijden MGA. 2006. Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87:1627-36. (Pubitemid 44141542)
80. Klironomos JN. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292-301.
81. Koide RT. 2000. Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol. 147:233-35.
82. Kothari SK, Marschner H, George E. 1990. Effect of VA mycorrhizal fungi and rhizosphere microorganisms on root and shoot morphology, growth and water relations in maize. New Phytol. 116:303-11.
83. Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P. 2002. Mtha1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol. 4:754-61. (Pubitemid 36333193)
84. Kunze R, Frommer WB, Flugge U-I. 2002. Metabolic engineering of plants: the role of membrane transport. Metab. Eng. 4:57-66. (Pubitemid 34850203)
85. Landis FC, Fraser LH. 2008. A new model of carbon and phosphorus transfers in arbuscular mycorrhizas. New Phytol. 177:466-79. (Pubitemid 350295776)
86. Leigh J, Hodge A, Fitter AH. 2008. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol. 181:199-207.
87. Li H-Y, 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 Phytol. 172:536-43. (Pubitemid 44571080)
88. Li H-Y, Smith FA, Dickson S, Holloway RE, Smith SE. 2008. Plant growth depressions in arbuscular mycorrhizal symbiosis: Not just caused by carbon drain? New Phytol. 178:852-62. (Pubitemid 351670100)
89. Li H-Y, Smith SE, Ophel-Keller K, Holloway RE, Smith FA. 2008. Naturally occurring arbuscular mycorrhizal fungi can replace direct P uptake by wheat when roots cannot access added P fertiliser. Funct. Plant Biol. 35:125-34.
90. Li H-Y, Zhu Y-G, 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 Soil 277:221-32. (Pubitemid 41728850)
91. Li X-L, George E, Marschner H. 1991. Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol. 119:397-404.
92. Lopez-Pedrosa A, Gonzalez-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N. 2006. GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet. Biol. 43:102-10. (Pubitemid 43227995)
93. MacLeod WJ, Robson AD, Abbott LK. 1986. Effects of phosphate supply and inoculation with a vesicular-arbuscular mycorrhizal fungus on the death of the root cortex of wheat, rape and subterranean clover. New Phytol. 103:349-57.
94. M̈ader P, Vierheilig H, Streitwolf-Engel R, Boller T, Frey B, et al. 2000. Transport of 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol. 146:155-61. (Pubitemid 30228608)
95. Marschner H. 1995. Mineral Nutrition of Higher Plants. London: Academic. 889 pp.
96. McDowell WH,Magill AH, Aitkenead-Peterson JA, Aber JD, Merriam JL, Kaushal SS. 2004. Effects of chronic nitrogen amendment on dissolved organic matter and inorganic nitrogen in soil solution. For. Ecol. Manag. 196:29-41. (Pubitemid 38847883)
97. Mikkelsen BL, Rosendahl S, Jakobsen I. 2008. Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol. 180:890-98.
98. Modjo HS, Hendrix JW. 1986. The mycorrhizal fungus Glomus macrocarpum as a cause of tobacco stunt disease. Phytopathology 76:668-91.
99. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I. 2004. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 164:357-64. (Pubitemid 39384748)
100. Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, et al. 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 J. 42:236-50. (Pubitemid 40589385)
101. Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M. 2008. Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol. 181:950-59.
102. Newsham KK, Fitter AH, Watkinson AR. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol. 10:407-11. (Pubitemid 26447959)
103. Olsson PA, Jakobsen I, Wallander H. 2002. Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. In Mycorrhizal Ecology, ed.MGAvan derHeijden, IR Sanders, pp. 93-115. Berlin: Springer.
104. OrfanoudakisM,Wheeler CT,Hooker JE. 2010. Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20:117-26.
105. Parniske M. 2004. Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 7:414-21. (Pubitemid 38871615)
106. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763-75.
107. Paszkowski U. 2006. A journey through signaling in arbuscular mycorrhizal symbioses. New Phytol. 172:35-46. (Pubitemid 44268111)
108. PoulsenKH, Nagy R, Gao LL, Smith SE, Bucher M, et al. 2005. Physiological andmolecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytol. 168:445-53.
109. Preuss CP, Huang CY, Gilliham M, Tyerman SD. 2010. Channel-like characteristics of the low-affinity barley phosphate transporter PHT1;6 when expressed in Xenopus oocytes. Plant Physiol. 152:1431-41.
110. Pumplin N, Harrison MJ. 2009. Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol. 151:809-19.
111. Rae AL, Jarmey JM, Mudge SR, Smith FW. 2004. Over-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates. Funct. Plant Biol. 31:141-48. (Pubitemid 38448951)
112. Raven JA, Smith FA. 1976. Nitrogen assimilation and transport in vascular land plants in relation to intracellular pH regulation. New Phytol. 76:415-31.
113. Ravnskov S, Jakobsen I. 1995. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol. 129:611-18.
114. Read DJ, Perez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems-A journey towards relevance? New Phytol. 157:475-92. (Pubitemid 36339234)
115. Reynolds HL, Hartley AE, Vogelsang KM, Bever JD, Schultz PA. 2005. Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytol. 167:869-80. (Pubitemid 43923822)
116. Rosewarne GM, Smith FA, Schachtman DP, Smith SE. 2007. Localization of proton-ATPase genes expressed in arbuscular mycorrhizal tomato plants. Mycorrhiza 17:249-58. (Pubitemid 46632430)
117. Rouached H, Arpat AB, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol. Plant 3:288-99.
118. Ruzicka DR, Barrios-Masias PH, Hausemann NT, Jackson LE, Schachtman DP. 2010. Tomato root transcriptome response to a nitrogen-enriched soil patch. BMC Plant Biol. 10:75-94.
119. Ryan MH, Graham JH. 2002. Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263-71.
120. Ryan MH, McCully ME, Huang CX. 2003. Location and quantification of phosphorus and other elements in fully hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytol. 160:429-41. (Pubitemid 37298620)
121. Ryan MH, McCully ME, Huang CX. 2007. Relative amounts of soluble and insoluble forms of phosphorus and other elements in intraradical hyphae and arbuscules of arbuscular mycorrhizas. Funct. Plant Biol. 34:457-64. (Pubitemid 46788602)
122. 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 colonisation by arbuscular mycorrhizal fungi. Plant Soil 270:275-86. (Pubitemid 40870392)
123. Sanders FE, Tinker PB. 1973. Phosphate flow into mycorrhizal roots. Pestic. Sci. 4:385-95.
124. Schachtman DP, Reid RJ, Ayling SM. 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116:447-53. (Pubitemid 128482269)
125. Silberbush M, Barber SA. 1983. Sensitivity of simulated phosphate uptake parameters used by a mechanistic mathematical model. Plant Soil 74:93-100.
126. Smith FA, Grace EJ, Smith SE. 2009. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol. 182:347-58.
127. Smith FA, Jakobsen I, Smith SE. 2000. Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytol. 147:357-66.
128. Smith FA, Smith SE. 1997. Structural diversity in (vesicular)-arbuscular mycorrhizal symbiosis. New Phytol. 137:373-88. (Pubitemid 28117954)
129. Smith FA, Smith SE, Timonen S. 2003. Mycorrhizas. In Root Ecology, ed. H de Kroon, EJW Visser, Vol. 168, pp. 257-95. Berlin: Springer.
130. Smith SE. 1980. Mycorrhizas of autotrophic higher plants. Biol. Rev. 55:475-510.
131. Smith SE, ChristophersenHM, Pope S, Smith FA. 2010. Arsenic uptake and toxicity in plants: integrating mycorrhizal influences. Plant Soil 327:1-21.
132. Smith SE, Gianinazzi-Pearson V. 1988. Physiological interactions between symbionts in vesiculararbuscular mycorrhizal plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39:221-44.
133. Smith SE, Gianinazzi-Pearson V. 1990. Phosphate uptake and arbuscular activity in mycorrhizal Allium cepa L.: effects of photon irradiance and phosphate nutrition. Aust. J. Plant Physiol. 17:177-88.
134. Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis. New York, London: Academic. 787 pp. 3rd ed.
135. Smith SE, Robson AD, Abbott LK. 1992. The involvement of mycorrhizas in assessment of genetically dependent efficiency of nutrient uptake and use. Plant Soil 146:169-79.
136. Smith SE, Smith FA. 1990. Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114:1-38.
137. Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133:16-20. (Pubitemid 37144076)
138. 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 Phytol. 162:511-24. (Pubitemid 38503718)
139. Smith SE, St. John BJ, Smith FA, Bromley JL. 1986. Effects of mycorrhizal infection on plant growth, nitrogen and phosphorus nutrition of glasshouse-grown Allium cepa L. New Phytol. 103:359-73.
140. Smith SE, St. John BJ, Smith FA, Nicholas DJD. 1985. Activity of glutamine synthetase and glutamate dehydrogenase in Trifolium subterraneum L. and Allium cepa L.: effects of mycorrhizal infection and phosphate nutrition. New Phytol. 99:211-27.
141. 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 Phytol. 103:117-31.
142. Solaiman MZ,EzawaT,KojimaT, SaitoM. 1999. Polyphosphates in intraradical and extraradical hyphae of an arbuscular mycorrhizal fungus, Gigaspora margarita. Appl. Environ. Microbiol. 65:5604-6. (Pubitemid 129520659)
143. Solaiman MZ, Saito M. 2001. Phosphate efflux from intraradical hyphae of Gigaspora margarita in vitro and its implication for phosphorus translocation. New Phytol. 151:525-33. (Pubitemid 32722375)
144. Son CL, Smith SE. 1988. Mycorrhizal growth responses: interactions between photon irradiance and phosphorus nutrition. New Phytol. 108:305-14.
145. Tanaka Y, Yano K. 2005. Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ. 28:1247-54. (Pubitemid 44028908)
146. Tinker PB. 1975. Soil chemistry of phosphorus and mycorrhizal effects on plant growth. In Endomycorrhizas, ed. FE Sanders, B Mosse, PB Tinker, pp. 353-71. London: Academic.
147. Tobar RM, Azćon R, Barea JM. 1994. Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol. 126:119-22. (Pubitemid 2040281)
148. Toussaint JP, St-ArnaudM, Charest C. 2004. Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can. J. Microbiol. 50:251-60.
149. Urcelay C, Diaz S. 2003. Themycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity. Ecol. Lett. 6:388-91. (Pubitemid 36573101)
150. Vierek N, Hansen PE, Jakobsen I. 2004. Phosphate pool dynamics in the arbuscular mycorrhizal fungus Glomus intraradices studied by in vivo 31P NMR spectroscopy. New Phytol. 162:783-94. (Pubitemid 38700189)
151. Wang B, Qiu Y-L. 2006. Phylogenetic distribution and evolution of mycorrhizae in land plants. Mycorrhiza 16:299-363. (Pubitemid 44078603)
152. Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, et al. 2007. Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J. Exp. Bot. 58:2491-501. (Pubitemid 47357556)
153. 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 (Pubitemid 36726332)