Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown

Mycorrhiza

Volumn 25, Issue 7, 2015, Pages 499-515

  Correa A ^a,b   Cruz, C ^b   Ferrol, N ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

Arbuscular mycorrhiza; Carbon; Mycorrhizal growth responses; Nitrogen; Symbiosis cost benefit

Indexed keywords

ARBUSCULAR MYCORRHIZA; CARBON; FUNGUS; GROWTH RESPONSE; HOST PLANT; NITROGEN; NUTRIENT DYNAMICS; SYMBIONT;

FUNGI;

CARBON; NITROGEN;

GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT; PLANT DEVELOPMENT; SYMBIOSIS;

CARBON; MYCORRHIZAE; NITROGEN; PLANT DEVELOPMENT; PLANTS; SYMBIOSIS;

EID: 84941876847     PISSN: 09406360     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00572-015-0627-6     Document Type: Review

References (156)

1. 2. New Phytol 167:859–868. doi:10.1111/j.1469-8137.2005.01458.x
2. 2. Plant Soil 296:159–172. doi:10.1007/s11104-007-9306-5
3. Aleklett K, Wallander H (2012) Effects of organic amendments with various nitrogen levels on arbuscular mycorrhizal fungal growth. Appl Soil Ecol 60:71–76. doi:10.1016/j.apsoil.2012.03.007
4. Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from Two 15 N-labelled sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol 95:381–396
5. Antunes P, Lehmann A, Hart M et al (2012) Long-term effects of soil nutrient deficiency on arbuscular mycorrhizal communities. Funct Ecol 26:532–540. doi:10.1111/j.1365-2435.2011.01953.x
6. Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19:239–246. doi:10.1007/s00572-008-0215-0
7. Azcón-Aguilar C, Alba C, Montilla M, Barea JM (1993) Isotopic (15 N) evidence of the use of less available N forms by VA mycorrhizas. Symbiosis 15:39–48
8. Bååth E, Spokes J (1989) The effect of added nitrogen and phosphorus on mycorrhizal growth response and infection in Allium schoenoprasum. Can J Bot 67:3227–3232. doi:10.1139/b89-402
9. 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
10. Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant-Microbe Interact 20:1055–1062. doi:10.1094/MPMI-20-9-1055
11. 15N dilution technique. Soil Biol Biochem 21:581–589
12. Becerra A, Arrigo N, Bartoloni N et al (2007) Arbuscular mycorrhizal colonization of Alnus acuminata Kunth in northwestern Argentina in relation to season and soil parameters. Ciencias Suelo (Argentina) 25:7–13
13. Bi Y, Li X, Christie P (2003) Influence of early stages of arbuscular mycorrhiza on uptake of zinc and phosphorus by red clover from a low-phosphorus soil amended with zinc and phosphorus. Chemosphere 50:831–837
14. Blanke V, Renker C, Wagner M et al (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992. doi:10.1111/j.1469-8137.2005.01374.x
15. Blanke V, Wagner M, Renker C et al (2011) Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343:379–392. doi:10.1007/s11104-011-0727-9
16. Bressan W (2001) Effect of phosphorus and nitrogen on“in vitro” spore germination of Glomus etunicatum Becker & Gerdemann, root growth and mycorrhizal colonization. Braz J Microbiol 32:276–280
17. Breuillin F, Schramm J, Hajirezaei M et al (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017. doi:10.1111/j.1365-313X.2010.04385.x
18. Bücking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol 165:899–911. doi:10.1111/j.1469-8137.2004.01274.x
19. Busby R, Gebhart D, Stromberger M et al (2011) Early seral plant species’ interactions with an arbuscular mycorrhizal fungi community are highly variable. Appl Soil Ecol 48:257–262. doi:10.1016/j.apsoil.2011.04.014
20. Büscher M, Zavalloni C, de Boulois H et al (2012) Effects of arbuscular mycorrhizal fungi on grassland productivity are altered by future climate and below-ground resource availability. Environ Exp Bot 81:62–71. doi:10.1016/j.envexpbot.2012.03.003
21. Cavagnaro T, Jackson L, Six J et al (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225. doi:10.1007/s11104-005-5847-7
22. Chambers C, Smith S, Smith F (1980) Effects of ammonium and nitrate ions on mycorrhizal infection, nodulation and growth of Trifolium subterraneum. New Phytol 85:47–62. doi:10.1111/j.1469-8137.1980.tb04447.x
23. Chen M, Yin H, O’Connor P et al (2009) C:N:P stoichiometry and specific growth rate of clover colonized by arbuscular mycorrhizal fungi. Plant Soil 326:21–29. doi:10.1007/s11104-009-9982-4
24. Chulan HA (1991) Effect of fertilizer and encomycorrhizal inoculum on growth and nutrient uptake of cocoa (Theobroma cacao L.) seedlings. Biol Fertil Soils 11:250–254
25. Clark R, Zeto S (1996) Mineral acquisition by mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1495–1503. doi:10.1016/S0038-0717(96)00163-0
26. Clark R, Zobel R, Zeto S (1999) Effects of mycorrhizal fungus isolates on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176. doi:10.1007/s005720050302
27. Cliquet J, Murray P, Boucaud J (1997) Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne. New Phytol 137:345–349
28. Compant S, van der Heijden M, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214. doi:10.1111/j.1574-6941.2010.00900.x
29. Cooperband L, Boerner R, Logan T (1994) Humid tropical leguminous tree and pasture grass responsiveness to vesicular-arbuscular mycorrhizal infection. Mycorrhiza 4:233–239
30. Corrêa A, Strasser R, Martins-Loução M (2008) Response of plants to ectomycorrhiza in N-limited conditions: which factors determine its variation? Mycorrhiza 18:413–427. doi:10.1007/s00572-008-0195-0
31. Corrêa A, Gurevitch J, Martins-Loução M, Cruz C (2012) C allocation to the fungus is not a cost to the plant in ectomycorrhiza. Oikos 121:449–463. doi:10.1111/j.1600-0706.2011.19406.x
32. Corrêa A, Cruz C, Pérez-Tienda J, Ferrol N (2014) Shedding light onto nutrient responses of arbuscular mycorrhizal plants: nutrient interactions may lead to unpredicted outcomes of the symbiosis. Plant Sci 221–222:29–41. doi:10.1016/j.plantsci.2014.01.009
33. Craine JM, Elmore AJ, Aidar MPM et al (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992. doi:10.1111/j.1469-8137.2009.02917.x
34. Cruz C, Green J, Watson C et al (2004) Functional aspects of root architecture and mycorrhizal inoculation with respect to nutrient uptake capacity. Mycorrhiza 14:177–184. doi:10.1007/s00572-003-0254-5
35. Cruz C, Egsgaard H, Trujillo C et al (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792. doi:10.1104/pp. 106.090522
36. Cruz C, Fegghi Z, Martins-Loução M, Varma A (2013) Plant nitrogen use efficiency may be improved through symbiosis with Piriformospora indica. In: Varma A, Kost G, Oelmüller R (eds) Soil Biol. Vol. 33. Piriformospora indica. Sebacinales their Biotechnol. Appl. Springer, pp 285–293
37. Cuenca G, Azcón R (1994) Effects of ammonium and nitrate on the growth of vesicular-arbuscular mycorrhizal Erythrina poeppigiana 0.I. Cook seedlings. Biol Fertil Soils 18:249–254
38. Cui M, Caldwell M (1996) Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. I. Roots and hyphae exploiting the same soil volume. New Phytol 133:453–460
39. Douds D, Galvez L, Bécard G, Kapulnik Y (1998) Regulation of arbuscular mycorrhizal development by plant host and fungus species in alfalfa. New Phytol 138:27–35
40. Douds DD, Nagahashi G, Shenk JE, Demchak K (2008) Inoculation of strawberries with AM fungi produced on-farm increased yield. Biol Agric Hortic 26:209–219. doi:10.1080/01448765.2008.9755084
41. Edathil TT, Manian S, Udaiyan K (1996) Interaction of multiple VAM fungal species on root colonization, plant growth and nutrient status of tomato seedlings (Lycopersicon esculentum Mill.). Agric Ecosyst Environ 59:63–68
42. Eom A, Hartnett D, Wilson G, Figge D (1999) The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. Am Midl Nat 142:55–70
43. Fay P, Mitchell D, Osborne B (1996) Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. New Phytol 132:425–433. doi:10.1111/j.1469-8137.1996.tb01862.x
44. Fellbaum C, Gachomo E, Beesetty Y et al (2011) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. PNAS 109:2666–2671. doi:10.1073/pnas.1118650109/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1118650109
45. Fellbaum CR, Mensah JA, Cloos AJ et al (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656. doi:10.1111/nph.12827
46. Ferrol N, Pérez-Tienda J (2009) Coordinated nutrient exchange in arbuscular mycorrhiza. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas - funct process ecol. Impact. Springer, Berlin Heidelberg, pp 73–87
47. Fitter A (2006) What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytol 172:3–6. doi:10.1111/j.1469-8137.2006.01865.x
48. Fonseca H, Berbara R, Daft M (2001) Shoot d15 N and d13 C values of non-host Brassica rapa change when exposed to Glomus etunicatum inoculum and three levels of phosphorus and nitrogen. Mycorrhiza 11:151–158. doi:10.1007/s005720100125
49. Frey B, Schuepp H (1993) Acquisition of arbuscular Zea of nitrogen mycorrhizal by external fungi hyphae associated with Zea mays L. New Phytol 124:221–230
50. Furlan V, Bernier-Cardou M (1989) Effects of N, P, and K on formation of vesicular-arbuscular mycorrhiza, growth and mineral content of onion. Plant Soil 174:167–174
51. Gabriel-Neumann E, Neumann G, Leggewie G, George E (2011) Constitutive overexpression of the sucrose transporter SoSUT1 in potato plants increases arbuscular mycorrhiza fungal root colonization under high, but not under low, soil phosphorus availability. J Plant Physiol 168:911–919
52. Gange A, Ayres R (1999) On the relation between arbuscular and colonization plant ‘benefit’. Oikos 87:615–621
53. Gao X, Kuyper T, Zou C et al (2006) Mycorrhizal responsiveness of aerobic rice genotypes is negatively correlated with their zinc uptake when nonmycorrhizal. Plant Soil 290:283–291. doi:10.1007/s11104-006-9160-x
54. George E, Häussler K, Vetterlein D et al (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70:2130–2137. doi:10.1139/b92-265
55. Goicoechea N, Antolin M, Sánchez-Díaz M (1997) Influence of arbuscular mycorrhiza and Rhizobium on nutrient content and water relations in drought stressed alfalfa. Plant Soil 192:261–268
56. Gomez SK, Javot H, Deewatthanawong P et al (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9:10. doi:10.1186/1471-2229-9-10
57. Govindarajulu M, Pfeffer PE, Jin H et al (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823. doi:10.1038/nature03610
58. Grace E, Cotsaftis O, Tester M et al (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 181:938–949. doi:10.1111/j.1469-8137.2008.02720.x
59. Graham J, Abbott L (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218
60. Graham J, Eissenstat D (1994) Host genotype and the formation and function of VA mycorrhiza. Plant Soil 159:179–185
61. Graham J, Eissenstat D (1998) Field evidence for the carbon cost of citrus mycorrhizas. New Phytol 140:103–110
62. Graham J, Duncan L, Eissenstat D (1997) Carbohydrate allocation patterns in citrus genotypes as affected by phosphorus nutrition, mycorrhizal colonization and mycorrhizal dependency. New Phytol 135:335–343
63. Guether M, Neuhäuser B, Balestrini R et al (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83. doi:10.1104/pp. 109.136390
64. Hamel C, Smith D (1991) Interspecific N-transfer and plant development in a mycorhizal field-grown mixture. Soil Biol Biochem 23:661–665
65. Hartwig UA, Wittmann P, Braun R et al (2002) Arbuscular mycorrhiza infection enhances the growth response of Lolium perenne to elevated atmospheric pCO(2). J Exp Bot 53:1207–1213
66. Hawkins H, George E (1999) Effect of plant nitrogen status on the contribution of arbuscular mycorrhizal hyphae to plant nitrogen uptake. Physiol Plant 105:694–700. doi:10.1034/j.1399-3054.1999.105414.x
67. 15N-nitrogen transport through arbuscular mycorrhizal hyphae to Triticum aestivum L. supplied with ammonium vs. nitrate nutrition. Ann Bot 87:303–311. doi:10.1006/anbo.2000.1305
68. Hawkins H, Cramer M, George E (1999) Root respiratory quotient and nitrate uptake in hydroponically grown non-mycorrhizal and mycorrhizal wheat. Mycorrhiza 9:57–60. doi:10.1007/s005720050263
69. Hawkins H, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285
70. Hays R, Reid C, St John T, Coleman D (1982) Effects of nitrogen and phosphorus on blue grama growth and mycorrhizal infection. Oecologia 54:260–265. doi:10.1007/BF00378401
71. Helgason T, Fitter A (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480. doi:10.1093/jxb/erp144
72. Hepper C (1983) The effect of nitrate and phosphate on the vesicular-arbuscular mycorrhizal infection of lettuce. New Phytol 93:389–399
73. Hodge A, Fitter A (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci 107:13754–13759. doi:10.1073/pnas.1005874107/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1005874107
74. Hoeksema JD, Chaudhary VB, Gehring CA et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. doi:10.1111/j.1461-0248.2009.01430.x
75. 15N. New Phytol 133:487–494
76. Jackson L, Miller D, Smith S (2002) Arbuscular mycorrhizal colonization and growth of wild and cultivated lettuce in response to nitrogen and phosphorus. Sci Hortic Amst 94:205–218. doi:10.1016/S0304-4238(01)00341-7
77. Janos D (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91. doi:10.1007/s00572-006-0094-1
78. Javot H, Penmetsa R, Terzaghi N et al (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 104:1720–1725. doi:10.1073/pnas.0608136104
79. Javot H, Penmetsa RV, Breuillin F et al (2011) Medicago truncatula MtPt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965. doi:10.1111/j.1365-313X.2011.04746.x
80. Jensen A, Jakobsen I (1980) The occrrence of vesicular-arbuscular mycorrhiza in barley and wheat grown in some Danish soils with different fertilizer treatments. Plant Soil 55:403–414
81. Jia Y, Gray V, Straker C (2004) The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann Bot 94:251–258. doi:10.1093/aob/mch135
82. Jin H, Pfeffer P, Douds D et al (2005) The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168:687–696. doi:10.1111/j.1469-8137.2005.01536.x
83. Johansen A (1999) Depletion of soil mineral N by roots of Cucumis sativus L. colonized or not by arbuscular mycorrhizal fungi. Plant Soil 209:119–127
84. Johansen A, Jakobsen I, Jensen E (1994) Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at three nitrogen levels. Plant Soil 160:1–9
85. Johnson C (1984) Phosphorus nutrition on mycorrhizal colonization, photosynthesis, growth and nutrient composition of Citrus aurantium. Plant Soil 80:35–42
86. Johnson N (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. doi:10.1111/j.1469-8137.2009.03110.x
87. Johnson N, Graham J, Smith F (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–585. doi:10.1046/j.1469-8137.1997.00729.x
88. Johnson N, Rowland D, Corkidi L et al (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908
89. Jongen M, Fay P, Jones M (1996) Effects of elevated carbon dioxide and arbuscular mycorrhizal infection on Trifolium repens. New Phytol 132:413–423
90. Jumpponen A, Trowbridge J, Mandyam K, Johnson L (2005) Nitrogen enrichment causes minimal changes in arbuscular mycorrhizal colonization but shifts community composition—evidence from rDNA data. Biol Fertil Soils 41:217–224. doi:10.1007/s00374-005-0845-8
91. Karagiannidis N, Nikolaou N, Ipsilantis I, Zioziou E (2007) Effects of different N fertilizers on the activity of Glomus mosseae and on grapevine nutrition and berry composition. Mycorrhiza 18:43–50. doi:10.1007/s00572-007-0153-2
92. Kaschuk G, Kuyper T, Leffelaar P et al (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244. doi:10.1016/j.soilbio.2009.03.005
93. Kaschuk G, Leffelaar P, Giller K et al (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol Biochem 42:125–127. doi:10.1016/j.soilbio.2009.10.017
94. Kiers E, Duhamel M, Beesetty Y et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(80):880–882
95. Kim K, Cho Y, Sohn B et al (2002) Cold-storage of mixed inoculum of Glomus intraradices enhances root colonization, phosphorus status and growth of hot pepper. Plant Soil 238:267–272
96. Klironomos J (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
97. Kobae Y, Tamura Y, Takai S et al (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415. doi:10.1093/pcp/pcq099
98. Koegel S, Ait Lahmidi N, Arnould C et al (2013) The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol 198:853–865. doi:10.1111/nph.12199
99. Kyllo D, Velez V, Tyree M (2003) Combined effects of arbuscular mycorrhizas and light on water uptake of the neotropical understory shrubs, Piper and Psychotria. New Phytol 160:443–454. doi:10.1046/j.1469-8137.2003.00896.x
100. Landis FC, Fraser LH (2008) A new model of carbon and phosphorus transfers in arbuscular mycorrhizas. New Phytol 177:466–479. doi:10.1111/j.1469-8137.2007.02268.x
101. Leigh J, Hodge A, Fitter A (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207. doi:10.1111/j.1469-8137.2008.02630.x
102. Li H, Smith S, Holloway R et al (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 172:536–543. doi:10.1111/j.1469-8137.2006.01846.x
103. Li H, Smith F, Dickson S et al (2008) Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytol 178:852–862. doi:10.1111/j.1469-8137.2008.02410.x
104. Liu Y, Shi G, Mao L et al (2012) Direct and indirect influences of 8 years of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523–535. doi:10.1111/j.1469-8137.2012.04050.x
105. 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol 146:155–161
106. Maiti D, Toppo N, Variar M (2011) Integration of crop rotation and arbuscular mycorrhiza (AM) inoculum application for enhancing AM activity to improve phosphorus nutrition and yield of upland rice (Oryza sativa L.). Mycorrhiza 21:659–667. doi:10.1007/s00572-011-0376-0
107. Miller R, Miller S, Jastrow J, Rivetta C (2002) Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. New Phytol 155:149–162
108. Moora M, Öpik M, Sen R, Zobel M (2004) Native arbuscular mycorrhizal fungal communities differentially influence the seedling performance of rare and common Pulsatilla species. Funct Ecol 18:554–562. doi:10.1111/j.0269-8463.2004.00876.x
109. Müller J, Mohr U, Sprenger N et al (1999) Pool sizes of fructans in roots and leaves of mycorrhizal and non-mycorrhizal barley. New Phytol 142:551–559
110. Ning J, Cumming J (2001) Arbuscular mycorrhizal fungi alter phosphorus relations of broomsedge (Andropogon virginicus L.) plants. J Exp Bot 52:1883–1891
111. Nordin A, Schmidt I, Shaver G (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 85:955–962
112. Nouri E, Breuillin-Sessoms F, Feller U, Reinhardt D (2014) Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS ONE 9:e90841. doi:10.1371/journal.pone.0090841
113. Oliver AJ, Smith SE, Nicholas DJD, Wallace W (1983) Activity of nitrate reductase in Trifollium subterraneum: effects of mycorrhizal infection and phosphate nutrition. New Phytol 94:63–79
114. Olsson P, Van Aarle I, Allaway W et al (2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol 130:1162–1171. doi:10.1104/pp. 009639.the
115. Olsson P, Burleigh S, van Aarle I (2005) The influence of external nitrogen on carbon allocation to Glomus intraradices in monoxenic arbuscular mycorrhiza. New Phytol 168:677–686. doi:10.1111/j.1469-8137.2005.01532.x
116. Olsson P, Rahm J, Aliasgharzad N (2010) Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol Ecol 72:125–131. doi:10.1111/j.1574-6941.2009.00833.x
117. Pérez-Tienda J, Testillano P, Balestrini R et al (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055. doi:10.1016/j.fgb.2011.08.003
118. + transporters and GS/GOGAT pathway in arbuscular mycorrhizal rice roots. Plant Physiol Biochem 75:1–8. doi:10.1016/j.plaphy.2013.11.029
119. Perner H, Schwarz D, Bruns C et al (2007) Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants. Mycorrhiza 17:469–474. doi:10.1007/s00572-007-0116-7
120. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. doi:10.1016/j.pbi.2007.05.004
121. Quintero-Ramos M, Espinoza-Victoria D, Ferrera-Cerrato R, Bethlenfalvay G (1993) Fitting plants to soil through mycorrhizal fungi: mycorrhiza effects on plant growth and soil organic matter. Biol Fertil Soils 15:103–106. doi:10.1007/BF00336426
122. Reynolds H, Hartley A, Vogelsang K et al (2005) Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytol 167:869–880. doi:10.1111/j.1469-8137.2005.01455.x
123. Ruzicka D, Hausmann N, Barrios-Masias F et al (2011) Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil 350:145–162. doi:10.1007/s11104-011-0890-z
124. Ryan M, Angus J (2003) Arbuscular mycorrhiza in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250:225–239
125. Ryan M, Tibbett M, Edmonds-Tibbett T et al (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35:2170–2180. doi:10.1111/j.1365-3040.2012.02547.x
126. Schroeder-Moreno M, Greaver T, Wang S et al (2011) Mycorrhizal-mediated nitrogen acquisition in switchgrass under elevated temperatures and N enrichment. Glob Chang Biol Bioenergy 4:266–276. doi:10.1111/j.1757-1707.2011.01128.x
127. Sikes B, Maherali H, Klironomos J (2012) Arbuscular mycorrhizal fungal communities change among three stages of primary sand dune succession but do not alter plant growth. Oikos 121:1791–1800. doi:10.1111/j.1600-0706.2012.20160.x
128. Smith F, Smith S (2011a) What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant Soil 348:663–679. doi:10.1007/s11104-011-0865-0
129. Smith S, Smith F (2011b) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. doi:10.1146/annurev-arplant-042110-103846
130. Smith S, St. John B, Smith F, Bromley J (1986) Effects of mycorrhizal infection on plant growth, nitrogen and phosphorus nutrition in glasshouse-grown Allium cepa L. New Phytol 103:359–373
131. Smith S, Smith F, 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 162:511–524. doi:10.1111/j.1469-8137.2004.01039.x
132. Smith F, Grace E, Smith S (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358. doi:10.1111/j.1469-8137.2008.02753.x
133. Subramanian K, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9:69–75. doi:10.1007/s005720050002
134. Sylvia DM, Neal LH (1990) Nitrogen affects the phosphorus response of VA mycorrhiza. New Phytol 115:303–310. doi:10.1111/j.1469-8137.1990.tb00456.x
135. Syvertsen J, Graham J (1990) Influence of vesicular arbuscular mycorrhiza and leaf age on net gas exchange of citrus leaves. Plant Physiol 94:1424–1428
136. Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254
137. Tian C, Kasiborski B, Koul R et al (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 153:1175–1187. doi:10.1104/pp. 110.156430
138. 2 in field studies. New Phytol 164:347–355. doi:10.1111/j.1469-8137.2004.01159.x
139. 2 and nitrogen deposition. New Phytol 147:189–200
140. Tu C, Booker F, Watson D et al (2006) Mycorrhizal mediation of plant N acquisition and residue decomposition: impact of mineral N inputs. Glob Chang Biol 12:793–803. doi:10.1111/j.1365-2486.2006.01149.x
141. Vaast P, Zasoski R (1992) Effects of VA-mycorrhiza and nitrogen sources on rhizosphere soil characteristics, growth and nutrient acquisition of coffee seedlings (Coffea arabica L.). Plant Soil 147:31–39. doi:10.1007/BF00009368
142. Van der Heijden M, Wiemken A, Sanders I (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578. doi:10.1046/j.1469-8137.2003.00688.x
143. Van der Heijden M, Streitwolf-Engel R, Riedl R et al (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752. doi:10.1111/j.1469-8137.2006.01862.x
144. Veiga R, Jansa J, Frossard E, van der Heijden M (2011) Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS ONE 6:e27825. doi:10.1371/journal.pone.0027825
145. Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62. doi:10.1016/j.soilbio.2011.11.018
146. Walder F, Niemann H, Natarajan M et al (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797. doi:10.1104/pp. 112.195727
147. Walder F, Niemann H, Lehmann MF et al (2013) Tracking the carbon source of arbuscular mycorrhizal fungi colonizing C3 and C4 plants using carbon isotope ratios (δ13C). Soil Biol Biochem 58:341–344. doi:10.1016/j.soilbio.2012.12.008
148. Wallace L, McNaughton S, Coughenour M (1982) The effects of clipping and fertilization on nitrogen nutrition and allocation by mycorrhizal and nonmycorrhizal Panicum coloratum L., a C4 grass. Oecologia 54:68–71. doi:10.1007/BF00541110
149. Watts-Williams S, Cavagnaro T (2011) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294. doi:10.1007/s00374-011-0621-x
150. Wehner J, Antunes P, Powell J et al (2010) Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia Jena 53:197–201. doi:10.1016/j.pedobi.2009.10.002
151. Wellings N, Wearing A, Thompson J (1991) Vesicular-arbuscular mycorrhiza (VAM) improve phosphorus and zinc nutrition and growth of pigeonpea in a vertisol. Aust J Agric Res 42:835–845
152. Wilson G, Hartnett D (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738
153. Wright D, Scholes J, Read D, Rolfe S (2005) European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. New Phytol 167:881–896. doi:10.1111/j.1469-8137.2005.01472.x
154. Xiao T, Yang Q, Ran W et al (2010) Effect of inoculation with arbuscular mycorrhizal fungus on nitrogen and phosphorus utilization in upland rice-mungbean intercropping system. Agric Sci China 9:528–535. doi:10.1016/S1671-2927(09)60126-7
155. Yoshida L, Allen E (2001) Response to ammonium and nitrate by a mycorrhizal annual invasive grass and native shrub in southern California. Am J Bot 88:1430–1436
156. Youpensuk S, Lordkaew S, Rerkasem B (2006) Comparing the effect of arbuscular mycorrhizal fungi on upland rice and Macaranga denticulata in soil with different levels of acidity. Sci Asia 32:121–126