Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants

Journal of Plant Ecology

Volumn 2, Issue 3, 2009, Pages 107-118

  He, Xinhua ^a,b   Xu, Minggang ^c   Qiu, Guo Yu ^d,e   Zhou, Jianbin ^f  

^a YUNNAN NORMAL UNIVERSITY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d PEKING UNIVERSITY   (China)

^e BEIJING NORMAL UNIVERSITY   (China)

^f NORTHWEST A F UNIVERSITY   (China)

Author keywords

15N enrichment; 15N natural abundance ( 15N); 15N stable isotope; Common mycorrhizal networks (CMNs); Nitrogen transfer

Indexed keywords

ARBUSCULAR; FUNGI; MYCELIUM (GENUS);

EID: 77949436092     PISSN: 17529921     EISSN: 1752993X     Source Type: Journal    
DOI: 10.1093/jpe/rtp015     Document Type: Article

References (164)

1. Albrecht C, Geurts R, Bisseling T (1999) Legume nodulation and mycorrhizae formation: two extremes in host specificity meet. EMBO J 18:281-288
2. Allen MF (1992) Mycorrhizal Functioning: An Integrative Plant-Fungal Process. New York: Chapman and Hall.
3. Ané J-M, Kiss GB, Riely BK, et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364-1367
4. Arnebrant K, Ek H, Finlay RD, et al. (1993) Nitrogen translocation between Alnus glutinosa (L.) Gaertn. seedlings inoculated with Frankia sp. and Pinus contorta Dougl. ex Loud seedlings connected by a common ectomycorrhizal mycelium. New Phytol 124:231-242
5. Bethlenfalvay GJ, Reyes-Solis MG, Camel SB, et al. (1991) Nutrient transfer between the root zones of soybean and maize plants connected by a common mycorrhizal mycelium. Physiol Plant 82:423-432
6. Binkley D, Sollins P, McGill WB (1985) Natural abundance of nitrogen-15 as a tool for tracing Alder-fixed nitrogen. Soil Sci Soc Am J 49:444-447
7. Boddey RM, Peoples MB, Palmer B, et al. (2000) Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosyst 57:235-270
8. Booth MG (2004) Mycorrhizal networks mediate overstoreyunderstorey competition in a temperate forest. Ecol Lett 7:538-546
9. Brady NC, Weil RR (2007) The Nature and Properties of Soils. 14th edn. Upper Saddle River, NJ: Prentice-Hall.
10. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275-304.
11. BrundrettMC(2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37-77.
12. Brundrett MC, Bougher N, Dell B, et al. (1996) Working with Mycorrhizas in Forestry and Agriculture (ACIAR Monograph 32). Canberra, Australia: Australian Centre for International Agricultural Research.
13. Chalk PM (1998) Dynamics of biologically fixed N in legume-cereal rotations: a review. Aust J Agric Res 49:303-316
14. Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21-44.
15. Cheng XM, Baumgartner K (2004) Arbuscular mycorrhizal fungimediated nitrogen transfer from vineyard cover crops to grapevines. Biol Ferti Soils 40:406-412
16. Chiariello N, Hickman JA, Mooney HA (1982) Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217:941-943
17. CSIRO Publishing (1998) Legumes and Cereals (nitrogen-watercycling) [Special issue]. Aust J Agric Res 49:303-564.
18. Dawson TE, Mambelli S, Plamboeck AH, et al. (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507-559
19. Dijkstra P, Ishizu A, Doucett R, et al. (2006) 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257-3266
20. Dixon ROD, Wheeler CT (1983) Biochemical, physiological and environmental aspects of symbiotic nitrogen fixation. In: Gordon JC, Wheeler CT (eds). Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications. Dordrecht, The Netherlands: Nijhoff, 107-171
21. Dubach M, Russelle MP (1994) Forage legumes roots and nodules and their role in nitrogen transfer. Agron J 86:259-266
22. Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473-1483
23. Eissenstat DM (1990) A comparison of phosphorus and nitrogen transfer between plants of different phosphorus status. Oecologia 82:342-347
24. Ek H, Andersson S, Soderstrom B (1996) Carbon and nitrogen flow in silver birch and Norway spruce connected by a common mycorrhizal mycelium. Mycorrhiza 6:465-467
25. Ekblad A, Huss-Danell K (1995) Nitrogen fixation by Alnus incana and nitrogen transfer from A. incana to Pinus sylvestris influenced by macronutrient and ectomycorhiza. New Phytol 131:453-459
26. Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121-126
27. Faber BA, Zasoski RJ, Munns DN (1991) A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can J Bot 69:87-94.
28. Finlay R, Read DJ (1986a) The structure and function of the vegetative mycelium of ectomycorrhizal plants. I. Translocation of 14C-labeled carbon between plants interconnected by a common mycelium. New Phytol 103:143-156
29. Finlay RD, Read DJ (1986b) The structure and function of the vegetative mycelium of ectomycorrhizal plants. II. The up-take and distribution of phosphorus by mycelial strands in the connecting host plants. New Phytol 103:157-165
30. Forrester DI, Bauhus J, Cowie AL, et al. (2006) Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review. For Ecol Manag 233:211-230
31. Francis R, Read DJ (1984) Direct transfer of carbon between plants connected by vesicular-arbuscular mycorrhizal mycelium. Nature 307:53-56
32. Frey B, Brunner I, Christie P, et al. (1998) The use of polytetrafluoroethylene (PTFE) hydrophobic membranes to study transport of 15N by mycorrhiza hyphae. In: Varma A (ed). Mycorrhizas Manual. Berlin, Germany: Springer, 151-158
33. Frey B, Schuepp H (1992) Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrinum L.) to maize via vesicular-arbuscular mycorrhizal hyphae. New Phytol 122:447-454
34. Frey B, Schuepp H (1993) A role of vesicular-arbuscular (VA) mycorrhizal fungi in facilitating interplant nitrogen transfer. Soil Biol Biochem 25:651-658
35. Fujita K, Ofosu-Budu KG, Ogata S (1992) Biological nitrogen fixation in mixed legume-cereal cropping systems. Plant Soil 141:155-175
36. Giller KE, Ormesher J, Awah FM (1991) Nitrogen transfer from Phaseolus bean to intercropped maize measured using 15N-enrichment and 15N-isotope dilution methods. Soil Biol Biochem 23:339-346
37. Giovannetti M, Sbrana C, Avio L, et al. (2004) Patterns of belowground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 165:175-181.
38. Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872-877
39. Hamel C, Barrantes-Cartin U, Furlan V, et al. (1991a) Endomycorrhizal fungi in nitrogen transfer from soybean to maize. Plant Soil 138:33-40.
40. Hamel C, Nesser C, Barrantes-Cartin U, et al. (1991b) Endomycorrhizal fungal species mediate 15N transfer from soybean to maize in nonfumigated soil. Plant Soil 138:41-47
41. Hamel C, Furlan V, Smith DL (1992) Mycorrhizal effects on interspecific plant competition and nitrogen transfer in legume-grass mixtures. Crop Sci 32:991-996
42. Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965-985
43. Handley LL, Scrimgeour CM (1997) Terrestrial plant ecology and d15N natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish old field. Adv Ecol Res 27:134-212.
44. Handley LL, Scrimgeour CM, Raven JA (1998) 15N at natural abundance levels in terrestrial vascular plants: a prè cis. In: Griffiths H (ed). Stable Isotopes: Integration of Biological, Ecological and Geochemical Processes. Oxford, UK: BIOS Scientific Publishers, 89-98.
45. Hansen AP, Pate JS, Hansen A, et al. (1987) Nitrogen economy of postfire stands of shrub legumes in jarrah (Eucalyptus marginata Donn ex Sm.) forest of S.W. Australia. J Exp Bot 38:26-41.
46. Hayman DS (1986) Mycorrhizae of nitrogen-fixing legumes. MIRCEN J Appl Microbiol Biotechnol 2:121-145
47. Haystead A, Malajczuk N, Grove TS (1988) Underground transfer of nitrogen between pasture plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytol 108:417-423
48. He XH (2002) Nitrogen exchange between plants through common mycorrhizal networks. Ph.D. Thesis. Brisbane, Australia: University of Queensland.
49. He XH, Bledsoe CS, Zasoski RJ, et al. (2006) Rapid nitrogen transfer from ectomycorrhizal pines to adjacent ectomycorrhizal and arbuscular mycorrhizal plants in a California oak woodland. New Phytol 170:143-151
50. He XH, Critchley C, Bledsoe CS (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531-567
51. 3) transfer between non-N2-fixing Eucalyptus maculata and N2-fixing Casuarina cunninghamiana linked by the ectomycorrhizal fungus Pisolithus sp. New Phytol 163:629-640
52. He XH, Critchley C, Ng H, et al. (2005) Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. supplied as ammonium nitrate. New Phytol 167:897-912.
53. Heap AJ, Newman BI (1980a) Links between roots by hyphae of vesicular-arbuscular mycorrhizas. New Phytol 85:169-171
54. Heap AJ, Newman BI (1980b) The influence of vesicular-arbuscular mycorrhizas on phosphorus transfer between plants. New Phytol 85:173-179
55. Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1-18.
56. Herrmann AM, Ritz K, Nunan N, et al. (2007) Nano-scale secondary ion mass spectrometry: A new analytical tool in biogeochemistry and soil ecology: A review article. Soil Bio Biochem 39:1835-1850.
57. Hirrel MA, Gerdemann JW (1979) Enhanced carbon transfer between onions infected with a vesicular-arbuscular mycorrhizal fungus. New Phytol 83:731-738
58. Hobbie JE, Hobbie EA (2006) 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87:816-822
59. Hobbie JE, Hobbie EA (2008) Natural abundance of N-15 in nitrogenlimited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11:815-830
60. Hobbie EA, Macko SA, Williams M (2000) Correlation between foliar d15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273-283
61. Högberg P (1997) 15N natural abundance in soil-plant systems. New Phytol 137:179-203.
62. Hogh-Jensen H (2006) The nitrogen transfer between plants: an important but difficult flux to quantify. Plant Soil 282:1-5.
63. 2 fixation. New Phytol 136:375-405.
64. Ikram A, Jensen ES, Jakobsen I (1994) No significant transfer of N and P from Pueraria phaseoloides to Hevea brasiliensis via hyphal links of arbuscular mycorrhiza. Soil Biol Biochem 26:1541-1547
65. Jensen ES (1996) Barley uptake of N deposited in the rhizosphere of associated field pea. Soil Biol Biochem 28:159-168
66. Johansen A, Jensen ES (1996) Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol Biochem 28:73-81.
67. Kaiser J (2001) The other global pollutant: nitrogen proves tough to curb. Science 294:1268-1269
68. Kapulnik Y, Douds DD (2000) Arbuscular Mycorrhizas: Physiology and Function. Dordrecht, The Netherlands: Kluwer Academic Publishers.
69. Kennedy PG, Izzo AD, Bruns TD (2003) There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. J Ecol 91:1071-1080
70. Knowles R, Blackburn TH (1993) Nitrogen Isotope Techniques. San Diego, CA: Academic Press.
71. 2 fixation and N cycling by Dryas along a chronosequence within the forelands of the Athabasca Glacier, Canada. Soil Biol Biochem 26:623-632
72. Laskowski DA, O'Melia FC, Griffith JD, et al. (1975) Effect of 2-chloro-6-(trichloromethyl) pyridine and its hydrolysis product 6-chloropicolinic acid on soil microorganisms. J Environ Qual 4:412-417
73. Leake JR, Johnson D, Donnelly DP, et al. (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016-1045
74. Ledgard SF (2001) Nitrogen cycling in low input legume-based agriculture, with emphasis on legume/grass pastures. Plant Soil 228:43-59.
75. 2 fixation: derivation of the method. Soil Biol Biochem 17:317-321
76. Ledgard SF, Steele KW (1992) Biological nitrogen fixation in mixed legume/grass pastures. Plant Soil 141:137-153
77. Lerat S, Gauci R, Catford JG, et al. (2002) 14C transfer between the spring ephemeral Erythronium americanum and sugar maple saplings via arbuscular mycorrhiza fungi in natural stands. Oecologia 132:181-187
78. Li L, Li SM, Sun JH, et al. (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorusdeficient soils. PNAS 104:11192-11196
79. Li YF, Ran W, Zhang RP, et al. (2009) Facilitated legume nodulation, phosphate uptake and nitrogen transfer by arbuscular inoculation in an upland rice and mung bean intercropping system. Plant Soil 315:285-296
80. Lipson D, Nasholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305-316
81. Mader P, Vierheilig H, Alt M, et al. (1993) Boundaries between soil compartments formed by micoporous hydrophobic membranes (Gore-Tex) can be crossed by vesicular-arbuscular mycorrhizal fungi but not by ions in the soil solution. Plant Soil 152:201-206
82. Mader P, Vierheilig H, Streitwolf-Engel R, 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 146:155-161
83. Malezieux E, Crozat Y, Dupraz C, et al. (2009) Mixing plant species in cropping systems: concepts, tools and models. A review. Agron Sustain Dev 29:43-46
84. Mariotti A (1983) Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements. Nature 303:685-687
85. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89-102.
86. Martin FM, Botton B (1993) Nitrogen metabolism of ectomycorrhizal fungi and ectomycorrhiza. Adv Plant Pathol 9:83-102.
87. Martin FM, Perotto S, Bonfante P (2001) Mycorrhizal fungi: a fungal community at the interface between soil and roots. In: Pinton R, Varanini Z, Nannipieri P (eds). The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface. New York: Marcel Dekker, 263-296
88. McGuire KL (2007)Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567-574
89. McGuire KL, Henkel TW, de la Cerda IG, et al. (2008) Dual mycorrhizal colonization of forest-dominating tropical trees and the mycorrhizal status of non-dominant tree and liana species. Mycorrhiza 18:217-222
90. McKendrick SL, Leake JR, Read DJ (2000) Symbiotic germination and development of myco-heterotrophic plants in nature: transfer of carbon from ectomycorrhizal Salix repens and Betula pendula to the orchid Corallorhiza trifida through shared hyphal connections. New Phytol 145:539-548
91. McKey D (1994) Legumes and nitrogen: the revolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent JI, McKey D (eds). Advances in Legume Systematics. Kew, UK: Royal Botanic Gardens, 211-228
92. 2 fixation by grain legumes. Aust J Agric Res 48:821-828
93. Meding SM, Zasoski RJ (2008) Hyphal-mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland. Soil Biol Biochem 40:126-134
94. Michelsen A, Quarmby C, Sleep D, et al. (1998) Vascular plant 15N natural abundance in health and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115:406-418
95. Miller SL, Allen EB (1992) Mycorrhizae, nutrient translocation, and interactions between plants. In: Allen MF (ed). Mycorrhizal Functioning: An Integrative Plant-Fungal Process. New York: Chapman and Hall, 301-332
96. Moffat AS (1998) Global nitrogen overload problem grows critical. Science 279:988-989.
97. Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In: Allen MF (ed). Mycorrhizal Functioning: An Integrative Plant-Fungal Process. New York: Chapman and Hall, 357-423.
98. Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glominae and Gigasporinae and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 37:471-491
99. Moyer-Henry KA, Burton JW, Israel D, et al. (2006) Nitrogen transfer between plants: a 15N natural abundance study with crop and weed species. Plant Soil J 282:7-20.
100. Nadelhoffer KJ, Fry B (1994) Nitrogen isotope studies in forest ecosystems. In: Lajtha K, Michener R (eds). Stable Isotopes in Ecology. Oxford, UK: Blackwell Scientific, 22-44.
101. Nasholm T, Ekblad A, Nordin A, et al. (1998) Boreal forest plants take up organic nitrogen. Nature 392:914-916
102. Nasholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31-48.
103. Nasholm T, Persson J (2001) Plant acquisition of organic nitrogen in boreal plants. Physiol Plant 111:419-426
104. Newman EI (1988) Mycorrhizal links between plants: their functioning and ecological significance. Adv Ecol Res 18:243-271
105. Newman EI, Devoy ALN, Basen NJ, et al. (1994) Plant species that can be linked by VA mycorrhizal fungi. New Phytol 126:691-693
106. Newman EI, Eason WR, Eissenstat DM, et al. (1992) Interaction between plants: the role of mycorrhizae. Mycorrhiza 1:47-53.
107. Nosengo N (2003) Fertilized to death. Nature 425:894-895
108. Onguene NA, Kuyper TW (2002) Importance of the ectomycorrhizal network for seedling survival and ectomycorrhiza formation in rain forests of south Cameroon. Mycorrhiza 12:13-17
109. Pate JS, Stewart GR, Unkovich M (1993) 15N natural abundance of plant soil components of a Banksia woodland ecosystem in relation to nitrate utilisation, life form, mycorrhizal status and N2-fixing abilities of component species. Plant Cell Environ 16:365-373
110. Paul EA (2006) Soil Microbiology, Ecology and Biochemistry. 3rd edn. San Diego, CA: Academic Press.
111. Pawlowski K (1999) Frankia and actinorhizal plants. In: Pedrosa FO, Hungria M, Yates G, NewtonW(eds). Nitrogen Fixation: From Molecular to Crop Productivity. Dordrecht, The Netherlands: Kluwer Academic Publishers, 451-452
112. Paynel F, Murray PJ, Cliquet JB (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229: 235-243
113. Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and subtropical agriculture. Adv Agron 44:155-223.
114. Peoples MB, Herridge DF (1999) Qualification of biological nitrogen fixation in agricultural system. In: Pedrosa FO, Hungria M, Yates G, NewtonW (eds). Nitrogen Fixation: From Molecular to Crop Productivity. Dordrecht, The Netherlands: Kluwer Academic Publishers, 519-524
115. Perry DA (1998) A moveable feast: the evolution of resource sharing in plant-fungus communities. Trends Ecol Evol 13:432-434
116. Peterson RL, Bonfante P (1994) Comparative structure of vesiculararbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159: 79-88.
117. Rains KC, Bledsoe CS (2007) Rapid uptake of 15N-ammonium and glycine-13C, 15N by arbuscular and ericoid mycorrhizal plants native to a Northern California coastal pygmy forest. Soil Biol Biochem 39:1078-1086
118. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376-391
119. Read DJ (1997) Mycorrhizal fungi: The ties that bind. Nature 388:517-518
120. Read DJ (1998) State of the art. In: Varma A, Hock B (eds). Mycorrhiza: Structure, Function, Molecular Biology, and Biotechnology. Berlin, Germany: Springer, 3-34.
121. Read DJ, Francis R, Finlay RD (1985) Mycorrhizal mycelia and nutrient cycling in plant communities. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds). Ecological Interaction in Soil: Plants, Microbes and Animals. Oxford, UK: Blackwell Scientific Publications, 193-217.
122. Remy W, Taylor TN, Haas H, et al. (1994) Four hundred-millionyear-old vesicular-arbuscular mycorrhizae. PNAS 91:11841-11843
123. Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33: 1-45.
124. Robinson D (2001) d15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153-162
125. Ronsheim ML, Anderson SE (2001) Population-level specificity in the plant-mycorrhizae association alters intraspecific interactions among neighbouring plants. Oecologia 128:77-84.
126. Sanchez PA (2002) Soil fertility and hunger in Africa. Science 295:2019-2020
127. Schmidt S, Stewart GR (1997) Waterlogging and fire impacts on nitrogen availability and utilisation in a subtropical wet heathland (wallum). Plant Cell Environ 20:1231-1241
128. Schmidt S, Stewart GR, Ashwath N (1999) Monitoring plant physiological characteristics to evaluate mine site revegetation: a case study from the wet-dry tropics of northern Australia. Plant Soil 215:73-84.
129. Schwintzer CR, Tjepkema JD (1990) The Biology of Frankia and Actinorhizal Plants. San Diego, CA: Academic Press.
130. Selosse M-A, Richard F, He XH, et al. (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evolution 21:621-628
131. Shearer GB, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13: 699-756.
132. Shen Q, Chu GX (2004) Bi-directonal nitrogen transfer in an intercropping system of peanut with rice cultivated in aerobic soil. Biol Fert Soils 40:81-87
133. Sierra J, Desfontaines L (2009) Role of root exudates and root turnover in the below-ground N transfer from Canavalia ensiformis (jackbean) to the associated Musa acuminata (banana). Crop Pasture Sci 60:289-294
134. Sierra J, Nygren P (2006) Transfer of N fixed by a legume tree to the associated grass in a tropical silvopastoral system. Soil Biol Biochem 38:1893-1903
135. Simard SW, Durall DM(2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140-1165
136. Simard SW, Perry DA, Jones MD, et al. (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579-582
137. Simon L, Bousquet J, Levesque RC, et al. (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67-69
138. Smith SE, Dickson S, Smith FA (2001) Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Aust J Plant Physiol 28:683-694
139. Smith SE, Gianinazzi-Pearson V, Koide R, et al. (1994) Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. Plant Soil 159:103-113
140. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. San Diego, CA: Academic Press.
141. Southworth D, He XH, Swenson WS, et al. (2005) Application of network theory to potential mycorrhizal networks. Mycorrhiza 15: 589-595.
142. Sprent JI (1994) Nitrogen acquisition systems in the Leguminosae. In: Sprent JI, McKeyD (eds). Advances in Legume Systematics. Part 5. Kew, London: Royal Botanic Gardens, 1-23.
143. Sprent JI (2001) Introduction to legumes. In: Sprent JI (ed). Nodulation in Legumes. Kew, London: Royal Botanic Gardens, 1-13.
144. Sprent JI (2005) West African legumes: the role of nodulation and nitrogen fixation. New Phytol 167:326-330.
145. Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575-581
146. Stern WR (1993) Nitrogen fixation and transfer in intercropping systems. Field Crops Res 34:335-356
147. Tjepkema JD, Schwintzer CR, Burris RH (2000) Natural abundance of 15N in actinorhizal plants and nodules. Plant Soil 219:285-289
148. Tomm GO, van Kessel C, Slinkard AE (1994) Bi-directional transfer of nitrogen between alfalfa and bromegrass: Short and long term evidence. Plant Soil 164:77-86.
149. 2 fixation in annual legumes using 15N natural abundance. In: Unkovich M, Pate J, McNeill A, Gibbs DJ (eds). Stable Isotope Techniques in the Study of Biological Processes and Functioning of Ecosystems. Dordrecht, The Netherlands: Kluwer Academic Publishers, 103-118
150. Unkovich M, Pate J, McNeill A, et al. (2001) Stable Isotope Techniques in the Study of Biological Processes and Functioning of Ecosystems. Dordrecht, The Netherlands: Kluwer Academic Publishers.
151. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296-310.
152. van der Heijden MGA, 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
153. van Kessel C, Farrell RE, Roskoski JP, et al. (1994) Recycling of the naturally-occurring 15N in an established stand of Leucaena leucocephala. Soil Biol Biochem 26:757-762
154. Vassilev N, Vassileva M, Azcon R, et al. (2001) Interactions of an arbuscular mycorrhizal fungus with free or co-encapsulated cells of Rhizobium trifolii and Yarrowia lipolytica inoculated into a soil-plant system. Biotechnol Lett 23:149-151
155. Vitousek PM, Aber JD, Howarth RW, et al. (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737-750
156. Wallenda T, Read DJ (1999) Kinetics of amino acid uptake by ectomycorrhizal roots. Plant Cell Environ 22:179-187
157. Wallenda T, Stober C, Hogbom H, et al. (2000) Nitrogen uptake process in roots and mycorrhizas. In: Schulze E-D (ed). Ecological Studies Vol. 142: Carbon and Nitrogen Cycling in Europe Forest Ecosystems. Berlin, Germany: Springer, 122-143
158. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299-363.
159. Whiteside MD, Treseder KK, Atsatt PR (2009) The brighter side of soils: Quantum dots track organic nitrogen through fungi and plants. Ecology 90:100-108.
160. Wilkinson DM (1998) The evolutionary ecology of mycorrhizal networks. OIKOS 82:407-410
161. Wu BY, Nara K, Hogetsu T (2001) Can 14C-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytol 149:137-146
162. Yoneyama T, Murakami T, Boonkerd N, et al. (1990) Natural 15N abundance in shrub and tree legumes, Casuarina, and non-N2-fixing plants in Thailand. Plant Soil 128:287-292
163. Yoneyama T, Muraoka T, Murakami T, et al. (1993) Natural abundance of 15N in tropical plants with emphasis on tree legumes. Plant Soil 153:295-304.
164. Yoneyama T (1996) Characterization of natural 15N abundance of soils. In: Boutton TW, Yamasaki SI (eds). Mass Spectrometry of Soils. New York: Marcel Dekker, 205-223