Arbuscular mycorrhizal symbiosis and ecosystem processes: Prospects for future research in tropical soils

Abstract Full-Text HTML XML Download Download as PDF (Size:172KB) PP. 11-22
DOI: 10.4236/oje.2014.41002    5,693 Downloads   10,299 Views   Citations


Arbuscular mycorrhizal fungi (AMF) are more widely distributed and can associate with a wide range of plant species. AMF are keystone organisms that form an interface between soils and plant roots. They are also sensitive to environmental changes. AMF are important microbial symbioses for plants under conditions of P-limitation. The AMF are crucial for the functioning of terrestrial ecosystems as they form symbiotic interactions with plants. Mycorrhizal fungi are known to influence plant diversity patterns in a variety of ecosystems globally. AMF hyphae form an extensive network in the soil. The length is a common parameter used to quantifying fungal hyphae. The mycelial network of AM fungi extends into the soil volume and greatly increases the surface area for the uptake of immobile nutrients. Also, AM symbioses improve plants tolerance to drought and enhance plants’ tolerance of or resistance to root pathogens. Also, the networks of AM hyphae play a crucial role in the formation of stable soil aggregates and in the building up of a macroporous structure of soil that allows penetration of water and air and thereby prevents erosion. The functioning of AMF symbiosis is mediated by direct and indirect effects of biotic and abiotic factors of the surrounding rhizosphere, the community, and the ecosystem. AMF have great potential in the restoration of disturbed land and low fertility soil. However, despite the importance of AMF to terrestrial ecosystems, little is known about the effects of environmental changes on AMF abundance, activity and the impact of these changes on the ecosystem services. Therefore, it is important to gain a clearer understanding of the effects of environmental changes on the AM fungal species to guide conservation and restoration efforts.

Cite this paper

Soka, G. and Ritchie, M. (2014) Arbuscular mycorrhizal symbiosis and ecosystem processes: Prospects for future research in tropical soils. Open Journal of Ecology, 4, 11-22. doi: 10.4236/oje.2014.41002.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Smith, S.E. and Read, D.J. (2008) Mycorrhizal symbiosis. 3rd Edition, Academic Press, New York.
[2] Redecker, D., Kodner, R. and Graham, L.E. (2000) Glomalean fungi from the Ordovician. Science, 289, 1920-1921.
[3] Fitter, A.H. (2005) Darkness visible, reflections on underground ecology. Journal of Ecology, 93, 231-243.
[4] Santos-González, J.C., Finlay, R.D. and Tehler, A. (2007) Seasonal dynamics of arbuscular mycorrhizal root colonization in a semi-natural grassland. Applied and Environmental Microbiology, 73, 5613-5623.
[5] Brundrett, M. (2004) Diversity and classification of mycorrhizal associations. Biol. Rev., 79, 473-495.
[6] Power, M.E. and Mills, L.S. (1995) The keystone cops meet in Hilo. Tree, 10, 182-184.
[7] Atayese, M.O., Awotoye, O.O., Osonubi, O. and Mulongo, K. (1993) Comparison of the influence of hedgerow woody legumes and cassava at the top and base of a hill slope in alley cropping system. Biology and Fertility of Soils, 16, 198-204.
[8] Sieverding, E. (1991) Vesicular-arbuscular mycorrhiza man-agement in tropical agro-systems. German Technical Cooperation (GTZ), Eschborn.
[9] Smith, S.E. and Read, D.J. (1997) Mycorrhizal symbiosis. 2nd Edition, Academic Press, New York.
[10] Borowicz, V. (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology, 82, 3057-3068.
[11] Van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Mou-Toglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A. and Sanders, I.R. (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69-72.
[12] Marschner, H. and Dell, B. (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil, 159, 89-102.
[13] Johnson, N.C., Wilson, G.W.T., Bowker, M.A., Wilson, J.A. and Miller, R.A. (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PNAS, 107, 2093-2098.
[14] Smith, F.A., Grace, E.J. and Smith, S.E. (2009) More than a carbon economy: Nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist, 182, 347-358.
[15] Reinhardt, D. (2007) Programming good relations—Development of the arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology, 10, 98-105.
[16] Bonfante, P. and Genre, A. (2008) Plants and arbuscular mycorrhizal fungi: An evolutionary developmental perspective. Trends in Plant Science, 13, 492-498.
[17] Jefwa, J.M., Mwangi, L.M., Odee, D. and Mugambi, G. (2004) Prelimi-nary studies on mycorrhizal symbiosis in plant conser-vation forestry and farming systems in Kenya. Journal of Tropical Microbiology, 3, 48-62.
[18] Rilling, C.M. (2004) Arbuscular Mycorrhizae and terrestrial ecosystem process. Ecology Letters, 7, 740-754.
[19] Hu, Y., Rillig, M.C., Xiang, D., Hao, Z. and Chen, B. (2013) Changes of AM fungal abundance along environmental gradients in the arid and semi-arid grasslands of northern China. PLOS ONE, 8, 1-10.
[20] Klironomos, J.N. (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature, 417, 67-70.
[21] McGuire, K.L., Henkel, T.W., Granzowdela, C.I., Villa, G., Edmund, F. and Andrew, C. (2008) Dual mycorrhizal colonization of forest-dominating tropical trees and the mycorrhizal status of non-dominant tree and liana species. Mycorrhiza, 18, 217-222.
[22] IPCC, Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., van der Linden, J.P. and Xiaosu, D. (2001) The scientific basis. Cambridge University Press, Cambridge.
[23] Yang, W., Zheng, Y., Gao, C., He, X., Ding, Q., Kim, Y., Rui, Y., Wang, S. and Guo, L. (2013) The arbuscular mycorrhizal fungal community response to warming and grazing differs between soil and roots on the QinghaiTibetan Plateau. PLOS ONE, 8, 1-11.
[24] Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K. and Barea, J.M. (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biology and Fertility of Soils, 37, 1-16.
[25] O’Halloran, I.P., Miller, M.H. and Arnold, G. (1986) Absorption of P by corn (Zea mays L.) as influenced by soil disturbance. Canadian Journal of Plant Science, 66, 287-302.
[26] Oehl, F., Sieverding, E., Ineichen, K., Mider, P., Boller, T. and Wiemken, A. (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agro-ecosystems of Central Europe. Applied and Environmental Microbiology, 69, 2816-2824.
[27] Borie, F., Rubio, R., Rouanet, J.L., Morales, A., Borie, G. and Rojas, C. (2006) Effects of tillage systems on soil characteristics, glomalin and mycorrhizal propagules in a Chilean Ultisol. Soil & Tillage Research, 88, 253-261.
[28] Leake, J., Johnson, D., Donnelly, D., Muckle, G., Boddy, L. and Read, D. (2004) Networks of power and influence: The role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany, 82, 1016-1045.
[29] Langley, J.A. and Hungate, B.A. (2003) Mycorrhizal controls on belowground litter quality. Ecology, 84, 2302-2312.
[30] Auge, R.M. (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 11, 3-42.
[31] Cavagnaro, T.R., Jackson, L.E., Six, J., Ferris, H., Goyal, S., Asami, D. and Scow, K.M. (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant and Soil, 282, 209-225.
[32] Rillig, M.C., Wright, S.F. and Eviner, V.T. (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: Comparing effects of five plant species. Plant and Soil, 238, 325-333.
[33] Tisdall, J.M. and Oades, J.M. (1980) The effect of crop rotation on aggregation in a red-brown earth. Australian Journal of Soil Research, 18, 423-433.
[34] Le Tacon, F., Zeller, B., Plain, C., Hossann, C., Bréchet, C. and Robin, C. (2013) Carbon transfer from the host to tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique. PLoS ONE, 8, Article ID: e64626.
[35] Zhu, Y.G. and Miller, R.M. (2003) Carbon cycling by arbuscular my-corrhizal fungi in soil-plant systems. Trends in Plant Science, 8, 407-409.
[36] Graham, J.H. (2000) Assessing costs of arbuscular mycorrhizal symbiosis in agroecosystems. In: Podila, G.K. and Douds Jr., D.D., Eds., Current Advances in Mycorrhizae Research, The American Phytopahthological Society Press, St. Paul, 127-140.
[37] Olsson, P.A., Jakobsen, I. and Wallander, H. (2002) Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. Ecological Studies, 157, 93-115.
[38] Johnson, N.C., Rowland, D.L., Corkidi, L., Egerton-Warburton, L. and Allen, E.B. (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grass-lands. Ecology, 84, 1895-1908.[1895:NEAMAA]2.0.CO;2
[39] Bever, J.D., Schultz, P.A., Pringle, A. and Morton, J.B. (2001) Arbuscular mycorrhizal fungi: More diverse than meets the eye, and the ecological tale of why. BioScience, 51, 923-932.[0923:AMFMDT]2.0.CO;2
[40] Hawksworth, D.L. (2001) The magnitude of fungal diversity: The 1.5 million species estimate revisited. Mycological Research, 105, 1422-1432.
[41] Sanders, I.R. (2010) ‘Designer’ mycorrhizas? Using natural genetic variation in AM fungi to increase plant growth. ISME Journal, 4, 1081-1083.
[42] Cardoso, I.M. and Kuyper, T.W. (2006) Mycorrhizas and tropical soil fertility. Agriculture, Ecosystems & Environment, 116, 72-84.
[43] O'Neill, E.G., O’Neill, R.V. and Norby, R.J. (1991) Hierarchy theory as a guide to mycorrhizal research on largescale problems. Environmental Pollution, 73, 271-284.
[44] Johnson, N.C., Graham, J.H. and Smith, F.A. (1997) Mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist, 135, 575-586.
[45] Linderman, R.G. (1988) Mycorrhizal interactions with the rhizosphere microflora: The mycorrhizosphere effect. Phytopathology, 78, 366-371.
[46] Reinhard, S., Weber, E., Martin, P. and Marschner, H. (1994) Influence of phosphorus supply and light intensity on mycorrhizal response in Pisum-Rhizobium-Glomus symbiosis. Experientia, 50, 890-896.
[47] Wellings, N.P., Wearing, A.H. and Thompson, J.P. (1991) Vesicular-arbuscular mycorrhizae (VAM) improve phosphorus and zinc nutrition and growth of pigeon pea in a Vertisol. Australian Journal of Agricultural Research, 42, 835-845.
[48] Corrêa, A., Hampp, R., Magel, E. and Martins-Loucao, M. (2011) Carbon allocation in ectomycorrhizal plants at limited and optimal N supply: An attempt at unraveling conflicting theories. Mycorrhiza, 21, 35-51.
[49] Tuomi, J., Kytoviita, M. and Hardling, R. (2001) Cost efficiency of nutrient acquisition and the advantage of mycorrhizal symbiosis for the host plant. Oikos, 92, 62-70.
[50] Janos, D.P. (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza, 17, 75-91.
[51] Hynes, M.M., Zasoski, R.J. and Bledsoe, C.S. (2008) Evaluation of two techniques for quantification of hyphal biomass. In: Merenlender, A., McCreary, D. and Purcell, K.L., Eds., 2008. Proceedings of the 6th California oak Symposium: Today’s Challenges, Tomorrow’s Opportunities. General Technical ReportsPSW-GTR-217. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, 139-148.
[52] Giasson, P., Karam, A. and Jaouich, A. (2008) Arbuscular mycorrhizae and alleviation of soil stresses on plant growth. In: Siddiqui, Z.A., Akhtar, M.S. and Futai, K., Eds., Mycorrhizae: Sustainable Agriculture and Forestry, Springer and Business Media B.V., 99-134.
[53] Tisdall, J.M. and Oades, J.M. (1979) Stabilization of soil aggregates by the root systems of ryegrass. Australian Journal of Soil Research, 17, 429-441.
[54] Olsson, P.A., Thingstrup, I., Jakobsen, I. and Baath, E. (1999) Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biology and Biochemistry, 31, 1879-1887.
[55] Read, D.J., Koucheki, H.K. and Hodgson, J. (1976) Vesicular-arbuscular mycorrhiza in natural vegetation systems. New Phytologist, 77, 641-653.
[56] Abbott, L.K. and Robson, A.D. (1991) Factors influencing the occurrence of vesicular-arbuscular mycorrhizas. Agriculture, Ecosystems & Environment, 35, 121-150.
[57] Hunt, G.A. and Fogel, R. (1983) Fungal hyphal dynamics in a western Oregon Douglas-fir stand. Soil Biology and Biochemistry, 15, 641-649.
[58] Brito, I., De Carvalho, M. and Goss, M.J. (2011) Summer survival of arbuscular mycorrhiza extraradical mycelium and the potential for its management through tillage options in Mediterranean cropping systems. Soil Use and Management, 27, 350-356.
[59] Dodd, J.C. (2000) The role of arbuscular Mycorrhizal Fungi in agroand natural ecosystems. Outlook on Agriculture, 29, 55-62.
[60] Utobo, E.B., Ogbodo, E.N. and Nwogbaga, A.C. (2011) Techniques for extraction and quantification of arbuscular mycorrhizal fungi. Libyan Agriculture Research Center Journal International, 2, 68-78.
[61] Quilambo, O.Q. (2003) The vesicular-arbuscular mycorrhizal symbiosis. African Journal of Biotechnology, 2, 539-546.
[62] Miller, R.M., Reinhardt, D.R. and Jastrow, J.D. (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tall grass prairie communities. Oecologia, 103, 17-23.
[63] Klironomos, J.N., McCune, J., Hart, M. and Neville, J. (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecology Letters, 3, 137-141.
[64] Egerton-Warburton, L.M., Johnson, N.C. and Allen, E.B. (2007) Mycorrhizal community dynamics following nitrogen fertilization: A cross-site test in five grasslands. Ecological Monographs, 77, 527-544.
[65] Porras-Alfaro, A., Herrera, J., Natvig, D.O. and Sinsabaugh, R.L. (2007) Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant and Soil, 296, 65-75.
[66] Lekberg, Y., Koide, R.T., Rohr, J.R., Aldrich-Wolfe, L. and Morton, J.B. (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology, 95, 95-105.
[67] Oehl, F., Laczko, E., Bogenrieder, A., Stahr, K., Bosch, R., van der Heijden, M. and Sieverding, E. (2010) Soil type and land use intensity determine the composition of arbuscular Mycorrhizal Fungal communities. Soil Biology and Biochemistry, 42, 724-738.
[68] Schnoor, T.K., Lekberg, Y., Rosendahl, S. and Olsson, P.A. (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza, 21, 211-220.
[69] Lilleskov, E.A., Fahey, T.J. and Lovett, G.M. (2001) Ectomycorrhizal fungal aboveground community change over an atmospheric nitrogen deposition gradient. Ecological Applications, 11, 397-410.[0397:EFACCO]2.0.CO;2
[70] Wallenda, T. and Kottke, I. (1998) Nitrogen deposition and ectomycorrhizas. New Phytologist, 139, 169-187.
[71] Egerton-Warburton, L.M. and Allen, E.B. (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecological Applications, 10, 484-496.[0484:SIAMCA]2.0.CO;2
[72] Eom, A.H., Harnett, D.C., Wilson, G.W.T. and Figge, D.A.H. (1999) The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. American Midland Naturalist, 142, 55-70.[0055:TEOFMA]2.0.CO;2
[73] Klironomos, J.N., McCune, J. and Moutoglis, P. (2004) Species of arbuscular mycorrhizal fungi affect mycorrhizal responses to simulated herbivory. Applied Soil Ecology, 26, 133-141.
[74] Brundrett, M.C., Piche, Y. and Peterson, R.L. (1984) A new method for observing the morphology of vesiculararbuscular mycorrhizae. Canadian Journal of Botany, 62, 2128-2134.
[75] Biermann, B. and Linderman, R.G. (1983) Use of vesiculararbuscular mycorrhizal roots, intraradical vesicles and extraradical vesicles as inoculum. New Phytologist, 95, 97-105.
[76] Jabaji-Hare, S.H., Piche, Y. and Fortin, J.A. (1986) Isolation and structural characterization of soil-borne auxiliary cells of Gigaspora margarita Becker and Hall, a vesicular arbuscular mycorrhizal fungus. New Phytologist, 103, 777-784.
[77] Jasper, D.A., Abbot, L.K. and Robson, A.D. (1989) Hyphae of a vesicular-arbuscular mycorrhizal fungus maintain infectivity in dry soil, except when the soil is disturbed. New Phytologist, 112, 101-107.
[78] Azcon, R., Rubio, R. and Barea, J.M. (1991) Selective interactions between different species of mycorrhizal fungi and Rhizobium meliloti strains, and their effects on growth, N2-fixation (N15) and nutrition of Medicago sativa L. New Phytologist, 117, 399-404.
[79] Frank, D.A. and McNaughton, S.J. (1993) Evidence for the promotion of aboveground grassland production by native large herbivores in Yellowstone National Park. Oecologia, 96, 157-161.
[80] Eom, A.H., Wilson, G.W.T. and Hartnett, D.C. (2001) Effects of ungulate grazers on arbuscular mycorrhizal symbiosis and fungal community structure in tallgrass prairie. Mycologia, 92, 233-242.
[81] Bai, G., Bao, Y.Y., Du, G.X. and Qi, Y.L. (2013) Arbuscular mycorrhizal fungi associated with vegetation and soil parameters under rest grazing management in a desert steppe ecosystem. Mycorrhiza, 23, 289-301.
[82] Trent, J.D., Wallace, L.L., Svejcar, T.J. and Christiansen, S. (1988) Effect of grazing on growth, carbohydrate pools, and mycorrhizae in winter wheat. Canadian Journal of Plant Science, 68, 115-120.
[83] Frank, D.A., Kuns, M.M. and Guido, D.R. (2002) Consumer control of grassland plant production. Ecology, 83, 602-606.[0602:CCOGPP]2.0.CO;2
[84] Gehring, C.A. and Whitham, T.G. (2002) Mycorrhizae herbivore interactions: Population and community consequences. In: van der Heijden, M.G.A. and Sanders, I.R. Eds., Mycorrhizal Ecology, Springer, Berlin, 295-320.
[85] McNaughton, S.J. (1979) Grazing as an optimization process: Grass ungulate relationships in the Serengeti. American Naturalist, 113, 691-703.
[86] Gange, A.C. (2007) Insect-mycorrhizal interactions: Patterns, processes, and consequences. In: Ohgushi, T., Craig, T.P. and Price, P.W., Eds., Ecological Communities: Plant Mediation in Indirect Interaction Webs. Cambridge University Press, London, 124-143.
[87] Schnyder, H., Locher, F. and Auerswald, K. (2010) Nutrient redistribution by grazing cattle drives patterns of topsoil N and P stocks in a low-input pasture ecosystem. Nutrient Cycling in Agroecosystems, 88, 183-195.
[88] van der Waal, C., et al. (2011) Large herbivores may alter vegetation structure of semi-arid savannas through soil nutrient mediation. Oecologia, 165, 1095-1107.
[89] Powell, C.L. (1981) Inoculation of barley with efficient mycorrhizal fungi stimulates seed yield. Plant and Soil, 59, 487-489.
[90] Habte, M. (1989) Impact of simulated erosion on the abundance and activity of indigenous vesicular-arbuscular mycorrhizal endophytes in an oxisol. Biology and Fertility of Soils, 7, 164-167.
[91] Mulligan, M.F., Smucker, A.J.M. and Safir, G.F. (1985) Tillage modifications of dry edible bean root colonization by VAM fungi. Agronomy Journal, 77, 140-142.
[92] Sagan, C., Toon, O.B. and Pollack, J.B. (1979) Anthropogenic albedo changes and the earth’s climate. Science, 206, 1363-1368.
[93] Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E. Bloomfield, J., et al. (2000) Biodiversity-global biodiversity scenarios for the year 2100. Science, 287, 1770-1774.
[94] Trimble, S.W. and Crosson, P. (2000) Land use US soil erosion rates: Myth and reality. Science, 289, 248-250.
[95] Vitousek, P.M., Mooney, H.A., Lubchenco, J. and Melillo, J.M. (1997) Human domination of earth’s ecosystems. Science, 277, 494-499.
[96] Odada, E.O., Ochola, W.O. and Olago, D.A. (2009) Drivers of ecosystem change and their impacts on human well-being in Lake Victoria basin. African Journal of Ecology, 47, 46-54.
[97] Lambin, E.F., Geist, H.J. and Lepers, E. (2003) Dynamics of land-use and land-cover change in tropical regions. Annual Review of Environment and Resources, 28, 205-241.
[98] Ramankutty, N. and Foley, J.A. (1999) Estimating historical changes in global land cover: Croplands from 1700 to 1992. Global Biogeochemical Cycles, 13, 997-1027.
[99] Meyer, W.B. and Turner, B.L. (1992) Human population growth and global land-use/cover change. Annual Review of Ecology and Systematics, 23, 39-61.
[100] Eriksson, A. (2001) Arbuscular mycorrhiza in relation to management history, soil nutrients and plant species diversity. Plant Ecology, 155, 129-137.
[101] Hartnett, D.C. and Wilson, G.W.T. (2002) The role of mycorrhizas in plant community structure and dynamics: Lessons from grasslands. Ecology, 80, 1187-1195.[1187:MIPCSA]2.0.CO;2
[102] Hoeksema, J.D. and Schwartz, M.W. (2003) Expanding comparative advantage biological market models: Contingency of mutualism on partners’ resource requirements and acquisition trade-offs. Proceeding of the Royal Society of London B, 270, 913-919.
[103] Jones, M.D. and Smith, S.E. (2004) Exploring functional definitions of mycorrhizas: Are mycorrhizas always mutualisms? Canadian Journal of Botany, 82, 1089-1109.
[104] Pimentel, D. (2006) Soil erosion: A food and environmental threat. Environment, Development and Sustainability, 8, 119-137.
[105] Verbruggen, E., Van Der Heijden, M.G., Weedon, J.T., Kowalchuk, G.A. and Roling, W.F. (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Molecular Ecology, 21, 2341-2353.
[106] Siddiqui, Z.A. and Pichtel, J. (2008) Mycorrhixae: An overview. In: Siddiqui, Z.A., Akhtar, M.S. and Futai, K., Eds., Mycorrhizae: Sustainable Agriculture and Forestry, Springer, Berlin, 1-35.
[107] Barber, N.A., Kiers, E.T., Theis, N., Hazzard, R.V. and Adler, L.S. (2013) Linking agricultural practices, mycorrhizal fungi, and traits mediating plant-insect interactions. Ecological Applications, 23, 1519-1530.
[108] Jansa, J., Mozafar, A., Anken, T., Ruh, R., Sanders, I.R. and Frossard, E. (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza, 12, 225-234.
[109] Nichols, K.A. and Wright, S.F. (2004) Contributions of soil fungi to organic matter in agricultural soils. In: Magdoff, F. and Weil, R., Eds., Functions and Management of Soil Organic Matter in Agro-ecosystems. CRC, Washington, DC, 179-198.
[110] Douds, D.D. and Millner, P.D. (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agriculture, Ecosystems & Environment, 74, 77-93.
[111] Schenck, N.C. and Kinloch, R.A. (1980) Incidence of mycorrhizal fungi on six field crops in monoculture on a newly cleared woodland site. Mycologia, 72, 445-456.
[112] Smithson, P.C. and Giller, K.E. (2002) Appropriate farm management practices for alleviating N and P deficiencies in low-nutrient soils of the tropics. Plant and Soil, 245, 169-180.
[113] Habte, M. and Osorio, N.W. (2001) Arbuscular mycorrhizas: Producing and applying arbuscular mycorrhizal inoculum. Department of Tropical Plant and Soil Sciences, College of Tropical Agriculture and Human Resources, University of Hawaii, Honolulu, 47.
[114] Daniell, T.J., Husband, R., Fitter, A.H. and Young, J.P.W. (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiology Ecology, 36, 203-209.
[115] Johnson, N.C. and Pfleger, F.L. (1992) Vesicular-arbuscular mycorrhizae and cultural stress. In: Bethlenfalvay, G.J. and Lindennan, R.G., Eds., Mycorrhizae in Sustainable Agriculture, American Society of Agronomy, Special Publication 54, American Society of Agronomy, 71-99.
[116] Newman, E.I., Heap, A.J. and Lawley, R.A. (1981) Abundance of mycorrhizas and root-surface micro-organisms of Plantago lanceolata in relation to soil and vegetation: A multivariate approach. New Phytologist, 89, 95-108.
[117] Jeffries, P., Spyropoulos, T. and Vardavarkis, E. (1988) Vesicular-arbuscular mycorrhizal status of various crops in different agricultural soils of northern Greece. Biology and Fertility of Soils, 5, 333-337.
[118] Porter, W.M., Robson, A.D. and Abbott, L.K. (1987) Field survey of the distribution of VA mycorrhizal fungi in relation to soil pH. Journal of Applied Ecology, 24, 659-662.
[119] Bolgiano, N.C., Safir, G.R. and Warncke, D.D. (1983) Mycorrhizal infection and growth of onion in the field in relation to phosphorus and water availability. Journal of the American Society for Horticultural Science, 108, 819-825.
[120] Morita, A. and Konishi, S. (1989) Relationship between vesicular-arbuscular mycorrhizal infection and soil phosphorus concentration in tea fields. Soil Science and Plant Nutrition, 35, 139-143.
[121] Thomson, B.D., Robson, A.D. and Abbott, L.K. (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.
[122] Mosse, B., Powell, C.L. and Hayman, D.S. (1976) Plant growth responses to vesicular-arbuscular mycorrhiza. IX. Interactions between vesicular-arbuscular mycorrhiza, rock phosphate and symbiotic nitrogen fixation. New Phytologist, 76, 331-342.
[123] Treseder, K.K. (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist, 164, 347-355.
[124] Johnson, N.C. (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecological Applications, 3, 749-757.
[125] Parrent, J.L. and Vilgalys, R. (2007) Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization. New Phytologist, 176, 164-174.
[126] Abbott, L.K., Robson, A.D. and De Boer, G. (1984) The effect of phosphorus on the formation of hyphae in soil by the vesicular-arbuscular mycorrhizal fungus, Glomus fasciculatum. New Phytologist, 97, 437-446.
[127] Miranda, J.C.C. and Harris, P.J. (1994) Effects of soil phosphorus on spore germination and hyphal growth of arbuscular mycorrhizal fungi. New Phytologist, 128, 103-108.
[128] Miranda, J.C.C. and Harris, P.J. (1994) The effect of soil phosphorus on the external mycelium growth of arbuscular mycorrhizal fungi during the early stages of mycorrhiza formation. Plant and Soil, 166, 271-280.
[129] George, E., Marschner, H. and Jakobsen, I. (1995) Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Critical Reviews in Biotechnology, 15, 257-270.
[130] Howeler, R.H., Sieverding, E. and Saif, S. (1987) Practical aspects of mycorrhizal technology in some tropical crops and pastures. Plant and Soil, 100, 249-283.
[131] Amijee, F., Tinker, P.B. and Stribley, D.P. (1989) The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on colonization. New Phytologist, 111, 435-446.
[132] Schroeder, M.S. and Janos, D.P. (2004) Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas. Plant and Soil, 264, 335-348.
[133] Read, D.J. and Perez-Moreno, J. (2003) Mycorrhizas and nutrient cycling in ecosystems—A journey towards relevance? New Phytologist, 157, 475-492.

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.