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The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material

Published online by Cambridge University Press:  07 February 2013

S. SAIA ,
E. BENÍTEZ ,
J. M. GARCÍA-GARRIDO ,
L. SETTANNI ,
G. AMATO  and
D. GIAMBALVO
S. SAIA
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi di Palermo, Viale delle Scienze, 90128 Palermo, Italy
E. BENÍTEZ
Affiliation:
Department of Environmental Protection, Estación Experimental del Zaidín, CSIC, c/Prof. Albareda 1, 18008 Granada, Spain
J. M. GARCÍA-GARRIDO
Affiliation:
Department of Soil Microbiology and Symbiotic Systems, Estación Experimental del Zaidín, CSIC, c/Prof. Albareda 1, 18008 Granada, Spain
L. SETTANNI
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi di Palermo, Viale delle Scienze, 90128 Palermo, Italy
G. AMATO*
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi di Palermo, Viale delle Scienze, 90128 Palermo, Italy
D. GIAMBALVO
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi di Palermo, Viale delle Scienze, 90128 Palermo, Italy
*
*To whom all correspondence should be addressed. Email: gaetano.amato@unipa.it
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Summary

Arbuscular mycorrhizal (AM) fungi increase nitrogen (N) uptake by their host plants, but their role in plant N capture from soil organic material is still unclear. In particular, it is not clear if AM fungi compete with the host plant for the N coming from the decomposing organic matter (OM), especially when the AM extraradical mycelium (ERM) and plant roots share the same soil volume. The goal of the present research was to study the effects of AM fungi on wheat N capture after the addition of 15N-labelled OM to soil. Durum wheat (Triticum durum) was grown under controlled conditions in a sand:soil mix and the following treatments were applied: (1) AM inoculation with Glomus mosseae and uninoculated control; and (2) soil amended with 15N-enriched maize leaves and unamended soil. The addition of OM reduced plant growth and N uptake. The AM fungi increased both plant growth and N uptake compared with uninoculated control plants and the effect was enhanced when wheat was grown in soil amended with OM compared with the unamended control. Although AM fungi increased soil N mineralization rates and total plant N uptake, they strongly reduced wheat N recovery from OM, suggesting that AM fungi have marked effects on competition between plants and bacteria for the different N sources in soil.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 152 , Issue 3 , June 2014 , pp. 370 - 378
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Al-Karaki, G. & Al-Omoush, M. (2002). Wheat response to phosphogypsum and mycorrhizal fungi in alkaline soil. Journal of Plant Nutrition 25, 873–883.Google Scholar
Ames, R. N., Reid, C. P. P., Porter, L. K. & Cambardella, C. (1983). Hyphal uptake and transport of nitrogen from two 15N-labelled sources by Glomus mosseae, a vesicular arbuscular mycorrhizal fungus. New Phytologist 95, 381–396.Google Scholar
Andrade, G. (2004). Role of functional groups of microorganisms on the rhizosphere microcosm dynamics. In Plant Surface Microbiology (Eds Varma, A., Abbott, L., Werner, D. & Hampp, R.), pp. 51–69. Berlin: Springer.Google Scholar
Atul-Nayyar, A., Hamel, C., Hanson, K. & Germida, J. (2009). The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19, 239–246.Google Scholar
Azcón, R. & Ocampo, J. A. (1981). Factors affecting the vesicular arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytologist 87, 677–685.CrossRefGoogle Scholar
Azcón, R., Ruiz-Lozano, J. M. & Rodríguez, R. (2001). Differential contribution of arbuscular mycorrhizal fungi to plant nitrate uptake (15N) under increasing N supply to the soil. Canadian Journal of Botany 79, 1175–1180.Google Scholar
Barea, J. M., Werner, D., Azcón-Aguilar, C. & Azcón, R. (2005). Interactions of arbuscular mycorrhiza and nitrogen fixing simbiosis in sustainable agriculture. In Nitrogen Fixation in Agriculture, Forestry, Ecology, and the Environment (Eds Werner, D. & Newton, W. E.), pp. 199–222. The Netherlands: Springer.Google Scholar
Cappellazzo, G., Lanfranco, L., Fitz, M., Wipf, D. & Bonfante, P. (2008). Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiology 147, 429–437.Google Scholar
Cliquet, J. B., Murray, P. J. & Boucaud, J. (1997). Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne. New Phytologist 137, 345–349.Google Scholar
Faure, S., Cliquet, J.-B., Thephany, G. & Boucaud, J. (1998). Nitrogen assimilation in Lolium perenne colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. New Phytologist, 138, 411–417.Google Scholar
Gamper, H., Peter, M., Jansa, J., Lüscher, A., Hartwig, U. A. & Leuchtmann, A. (2004). Arbuscular mycorrhizal fungi benefit from 7 years of free air CO2 enrichment in well-fertilized grass and legume monocultures. Global Change Biology 10, 189–199.Google Scholar
García, C., Hernandez, T., Costa, F., Ceccanti, B. & Ganni, A. (1993). Hydrolases in the organic matter fractions of sewage sludge: changes with composting. Bioresource Technology 45, 47–52.Google Scholar
García-Garrido, J. M., García-Romera, I. & Ocampo, J. A. (1992). Cellulase production by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol and Gerd) Gerd and Trappe. New Phytologist 121, 221–226.Google Scholar
García-Romera, I., García-Garrido, J. M., Martinez-Molina, E. & Ocampo, J. A. (1991). Production of pectolytic enzymes in lettuce root colonized by Glomus mosseae. Soil Biology and Biochemistry 23, 597–601.Google Scholar
Geisseler, D. & Horwath, W. R. (2009). Relationship between carbon and nitrogen availability and extracellular enzyme activities in soil. Pedobiologia 53, 87–98.Google Scholar
Gill, P. P. & Modi, V. V. (1981). Induction of extracellular proteases by egg-white in Aspergillus nidulans. Folia Microbiologica 26, 78–82.CrossRefGoogle ScholarPubMed
Giovannetti, M. & Mosse, B. (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection roots. New Phytologist 84, 489–500.Google Scholar
Hawkins, H. J., Johansen, A. & George, E. (2000). Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant and Soil 226, 275–285.Google Scholar
Hoagland, D. R. & Arnon, D. I. (1950). Water-culture Method for Growing Plants without Soil. California Agricultural Experiment Station Circular 347. Berkeley, CA, USA: University of California.Google Scholar
Hodge, A. (2003). Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytologist 157, 303–314.Google Scholar
Hodge, A., Stewart, J., Robinson, D., Griffiths, B. S. & Fitter, A. H. (1998). Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytologist 139, 479–494.Google Scholar
Hodge, A., Robinson, D. & Fitter, A. H. (2000 a). An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytologist 145, 575–584.Google Scholar
Hodge, A., Robinson, D. & Fitter, A. H. (2000 b). Are microorganisms more effective than plants at competing for nitrogen? Trends in Plant Science 5, 304–308.Google Scholar
Hodge, A., Campbell, C. D. & Fitter, A. H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297–299.Google Scholar
Hodge, A., Helgason, T. & Fitter, A. H. (2010). Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecology 3, 267–273.Google Scholar
Jackson, L. E., Schimel, J. P. & Firestone, M. K. (1989). Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland. Soil Biology and Biochemistry 21, 409–415.Google Scholar
Johansen, A., Jakobsen, I. & Jensen, E. S. (1993). Hyphal transport by a vesicular–arbuscular mycorrhizal fungus of N applied to the soil as ammonium or nitrate. Biology and Fertility of Soils 16, 66–70.CrossRefGoogle Scholar
Jones, D. L., Healey, J. R., Willett, V. B., Farrar, J. F. & Hodge, A. (2005). Dissolved organic nitrogen uptake by plants: an important N uptake pathway? Soil Biology and Biochemistry 37, 413–423.Google Scholar
Kandeler, E. & Gerber, H. (1988). Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils 6, 68–72.CrossRefGoogle Scholar
Kaye, J. P. & Hart, S. C. (1997). Competition for nitrogen between plants and soil microorganisms. Trends in Ecology and Evolution 12, 139–143.Google Scholar
Killham, K. (1994). Soil Ecology. Cambridge, UK: Cambridge University Press.Google Scholar
Ladd, J. N. & Butler, J. H. A. (1972). Short-term assays of soil proteolytic enzyme activities using proteins and dipeptides derivatives as substrates. Soil Biology and Biochemistry 4, 19–30.Google Scholar
Leigh, J., Hodge, A. & Fitter, A. H. (2009). Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181, 199–207.Google Scholar
Leigh, J., Fitter, A. H. & Hodge, A. (2011). Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiology Ecology 76, 428–438.Google Scholar
Li, H. Y., Zhu, Y., Marschner, P., Smith, F. A. & Smith, S. E. (2005). Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant and Soil 277, 221–232.Google Scholar
Li, H., Smith, S. E., Holloway, R. E., Zhu, Y. & Smith, F. A. (2006). Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytologist 172, 536–543.Google Scholar
Marschner, P. & Crowley, D. E. (1996). Root colonization of mycorrhizal and non-mycorrhizal pepper (Capsicum annuum) by Pseudomonas fluorescens 2–79RL. New Phytologist 134, 115–122.Google Scholar
Miyasaka, S. C. & Habte, M. (2001). Plant mechanisms and mycorrhizal symbioses to increase phosphorus uptake efficiency. Communications in Soil Science and Plant Analysis 32, 1101–1147.Google Scholar
Phillips, J. M. & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.Google Scholar
Ravnskov, S., Nybroe, O. & Jakobsen, I. (1999). Influence of an arbuscular mycorrhizal fungus on Pseudomonas fluorescens DF57 in rhizosphere and hyphosphere soil. New Phytologist 142, 113–122.Google Scholar
Reynolds, H. L., Hartley, A. E., Vogelsang, K. M., Bever, J. D. & Schultz, P. A. (2005). Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytologist 167, 869–880.Google Scholar
Schimel, J. P. & Weintraub, M. N. (2003). The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology and Biochemistry 35, 549–563.Google Scholar
Schüßler, A., Schwarzott, D. & Walker, C. (2001). A new fungal phylum, the Glomeromycota, phylogeny and evolution. Mycological Research 105, 1413–1421.Google Scholar
Secilia, J. & Bagyaraj, D. J. (1987). Bacteria and actinomycetes associated with pot cultures of vesicular–arbuscular mycorrhizas. Canadian Journal of Microbiology 33, 1069–1073.Google Scholar
Seeley, H. W. & VanDemark, P. J. (1981). Microbes in Action: a Laboratory Manual of Microbiology. 3rd edn.San Francisco, USA: W. H. Freeman and Company.Google Scholar
Seligman, N. G., Feigenbaum, S., Feinerman, D. & Benjamin, R. W. (1986). Uptake of nitrogen from high C-to-N ratio, 15N-labelled organic residues by spring wheat grown under semi-arid conditions. Soil Biology and Biochemistry 18, 303–307.Google Scholar
Smith, S. E. & Read, D. J. (2008). Mycorrhizal Symbiosis. San Diego, CA, USA: Academic Press.Google Scholar
Staddon, P. L., Jakobsen, I. & Blum, H. (2004). Nitrogen input mediates the effect of free-air CO2 enrichment on mycorrhizal fungal abundance. Global Change Biology 10, 1678–1688.Google Scholar
Tabatabai, M. A. (1994). Soil enzymes. In Methods of Soil Analysis. Part 2. Microbial and Biochemical Properties (Eds Weaver, R. W., Angel, J. S. & Bottomley, P. S.), pp. 775–833. Madison, WI, USA: Soil Science Society of America.Google Scholar
Tisserant, B., Gianinazzi-Pearson, V., Gianinazzi, S. & Gollote, A. (1993). In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycological Research 97, 245–250.Google Scholar
Tobar, R., Azcón, R. & Barea, J. M. (1994). Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytologist 126, 119–122.Google Scholar
Toljander, J. F., Lindahl, B. D., Paul, L. R., Elfstrand, M. & Finlay, R. D. (2007). Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiology Ecology 61, 295–304.Google Scholar
Vierheilig, H. & Ocampo, J. A. (1991). Receptivity of various wheat cultivars to infection by VA-mycorrhizal fungi as influenced by inoculum potential and the relation of VAM-effectiveness to succinic dehydrogenase activity of the mycelium in the roots. Plant and Soil 133, 291–296.CrossRefGoogle Scholar
Vierheilig, H., Schweiger, P. & Brundrett, M. (2005). An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiologia Plantarum 125, 393–404.Google Scholar
Wamberg, C., Christensen, S., Jakobsen, I., Müller, A. K. & Sørensen, S. J. (2003). The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biology and Biochemistry 35, 1349–1357.Google Scholar
Whiteside, M. D., Treseder, K. K. & Atsatt, P. R. (2009). The brighter side of soils: quantum dots track organic nitrogen through fungi and plants. Ecology 90, 100–108.Google Scholar