Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland

Soil Biology and Biochemistry

Volumn 80, Issue , 2015, Pages 283-292

  Bender, S Franz ^a,b   Conen, Franz ^c   Van der Heijden, Marcel G A ^a,b,d  

^a Plant Soil Interactions Institute for Sustainability Sciences Agroscope   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Agriculture; Arbuscular mycorrhizal fungi; Nitrogen; Nitrous oxide; Organic N; Phosphorous; Resource efficiency; Unreactive P

Indexed keywords

NITROGEN;

ARBUSCULAR MYCORRHIZAL FUNGI; NITROUS OXIDE; ORGANIC N; PHOSPHOROUS; RESOURCE EFFICIENCIES;

AGRICULTURE;

ARBUSCULAR MYCORRHIZA; FUNGUS; GRASSLAND; GROWTH RATE; HEATHLAND; LEACHING; NITROGEN CYCLE; NITROUS OXIDE; NUTRIENT CYCLING; NUTRIENT USE EFFICIENCY; PHOSPHORUS CYCLE; SOIL MICROORGANISM;

FUNGI;

EID: 84910024878     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2014.10.016     Document Type: Article

References (88)

1. 15N-labelled sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytologist 1983, 95:381-396.
2. Asghari H.R., Cavagnaro T.R. Arbuscular mycorrhizas enhance plant interception of leached nutrients. Functional Plant Biology 2011, 38:219-226.
3. Asghari H.R., Cavagnaro T.R. Arbuscular mycorrhizas reduce nitrogen loss via leaching. PloS One 2012, 7:e29825.
4. Asghari H.R., Chittleborough D.J., Smith F.A., Smith S.E. Influence of arbuscular mycorrhizal (AM) symbiosis on phosphorus leaching through soil cores. Plant and Soil 2005, 275:181-193.
5. Atalay A. Variation in phosphorus sorption with soil particle size. Soil & Sediment Contamination 2001, 10:317-335.
6. Atul-Nayyar A., Hamel C., Hanson K., Germida J. The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 2009, 19:239-246.
7. 2O emissions from soil. ISME Journal 2014, 8:1336-1345.
8. Bender S.F., van der Heijden M.G.A. Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. Journal of Applied Ecology 2014, in press. 10.1111/1365-2664.12351.
9. Bolan N.S., Robson A.D., Barrow N.J. Effects of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants. Plant and Soil 1987, 99:401-410.
10. Cavagnaro T.R., Barrios-Masias F.H., Jackson L.E. Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant and Soil 2012, 353:181-194.
11. 2. Science 2012, 337:1084-1087.
12. Clark R.B., Zeto S.K. Mineral acquisition by arbuscular mycorrhizal plants. Journal of Plant Nutrition 2000, 23:867-902.
13. Cordell D., Drangert J.-O., White S. The story of phosphorus: global food security and food for thought. Global Environmental Change 2009, 19:292-305.
14. Corkidi L., Merhaut D.J., Allen E.B., Downer J., Bohn J., Evans M. Effects of mycorrhizal colonization on nitrogen and phosphorus leaching from Nursery containers. Hortscience 2011, 46:1472-1479.
15. Daly K., Jeffrey D., Tunney H. The effect of soil type on phosphorus sorption capacity and desorption dynamics in Irish grassland soils. Soil Use and Management 2001, 17:12-20.
16. 2, and N influence inorganic and organic n leaching in grasslands. Ecology 2007, 88:490-500.
17. Eidgenössische Forschungsanstalten FAL, RAC, FAW Schweizerische Referenzmethoden der Eidgenössischen landwirtschaftlichen Forschungsanstalten 1996, Eidg. Forschungsanstalt für Landwirtschaftlichen Pflanzenbau, FAP, Zürich.
18. Elliott E.T., Heil J.W., Kelly E.F., Monger H.C. Soil structural and other physical properties. Standard Soil Methods for Long-term Ecological Research 1999, 74-78. Oxford University Press, New York. G.P. Robertson, C.S. Bledsoe, D.C. Coleman, P. Sollins (Eds.).
19. Feng G., Song Y.C., Li X.L., Christie P. Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in a calcareous soil. Applied Soil Ecology 2003, 22:139-148.
20. Fitter A.H., Helgason T., Hodge A. Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biology Reviews 2011, 25:68-72.
21. Frey B., Schuepp H. Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytologist 1993, 124:221-230.
22. Galloway J.N., Aber J.D., Erisman J.W., Seitzinger S.P., Howarth R.W., Cowling E.B., Cosby B.J. The nitrogen cascade. Bioscience 2003, 53:341-356.
23. George E., Marschner H., Jakobsen I. Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Critical Reviews in Biotechnology 1995, 15:257-270.
24. Ghani A., Muller K., Dodd M., Mackay A. Dissolved organic matter leaching in some contrasting New Zealand pasture soils. European Journal of Soil Science 2010, 61:525-538.
25. Goransson P., Postma J., Falkengren Grerup U., Göransson P., Olsson P. Colonisation by arbuscular mycorrhizal and fine endophytic fungi in four woodland grasses - variation in relation to pH and aluminium. Soil Biology & Biochemistry 2008, 40:2260-2265.
26. Govindarajulu M., Pfeffer P.E., Jin H.R., Abubaker J., Douds D.D., Allen J.W., Bucking H., Lammers P.J., Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435:819-823.
27. Hamel C. Impact of arbuscular mycorrhizal fungi on N and P cycling in the root zone. Canadian Journal of Soil Science 2004, 84:383-395.
28. Hawkins H.J., Johansen A., George E. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant and Soil 2000, 226:275-285.
29. Hodge A., Campbell C.D., Fitter A.H. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 2001, 413:297-299.
30. Hodge A., Fitter A.H. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:13754-13759.
31. Hodge A., Storer K. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil 2014, 1-19.
32. Hofstra N., Bouwman A.F. Denitrification in agricultural soils: summarizing published data and estimating global annual rates. Nutrient Cycling in Agroecosystems 2005, 72:267-278.
33. Jakobsen I., Abbott L.K., Robson A.D. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with trifolium-subterraneum L. 1. Spread of hyphae and phosphorous inflow into roots. New Phytologist 1992, 120:371-380.
34. 2 from fertilized maize fields in southwestern France. Nutrient Cycling in Agroecosystems 1997, 48:91-104.
35. Jansa J., Mozafar A., Anken T., Ruh R., Sanders I.R., Frossard E. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 2002, 12:225-234.
36. Jansa J., Mozafar A., Frossard E. Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant and Soil 2005, 276:163-176.
37. Jayachandran K., Schwab A.P., Hetrick B.A.D. Mineralization of organic phosphorus by vesicular arbuscular mycorrhizal fungi. Soil Biology & Biochemistry 1992, 24:897-903.
38. Johansen A., Jakobsen I., Jensen E.S. Hyphal transport by a vesicular-arbuscular mycorrhizal fungus of N applied to the soil as ammonium or nitrate. Biology and Fertility of Soils 1993, 16:66-70.
39. Johnson N.C. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 2010, 185:631-647.
40. EC value. Soil Biology & Biochemistry 1996, 28:25-31.
41. EN value. Soil Biology & Biochemistry 1996, 28:33-37.
42. Kaye J.P., Hart S.C. Competition for nitrogen between plants and soil microorganisms. Trends in Ecology & Evolution 1997, 12:139-143.
43. Knacker T., van Gestel C.A.M., Jones S.E., Soares A., Schallnass H.J., Forster B., Edwards C.A. Ring-testing and field-validation of a Terrestrial Model Ecosystem (TME) - an instrument for testing potentially harmful substances: conceptual approach and study design. Ecotoxicology 2004, 13:9-27.
44. Koerselman W., Meuleman A.F.M. The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. Journal of applied ecology 1996, 33:1441-1450.
45. Koide R.T., Kabir Z. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytologist 2000, 148:511-517.
46. Koide R.T., Li M.G. Appropriate controls for vesicular arbuscular mycorrhiza research. New Phytologist 1989, 111:35-44.
47. Lazcano C., Barrios-Masias F.H., Jackson L.E. Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biology & Biochemistry 2014, 74:184-192.
48. Liu J., You L., Amini M., Obersteiner M., Herrero M., Zehnder A.J.B., Yang H. Ahigh-resolution assessment on global nitrogen flows in cropland. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:8035-8040.
49. Mäder P., Vierheilig H., Streitwolf-Engel R., Boller T., Frey B., Christie P., Wiemken A. Transport of N-15 from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytologist 2000, 146:155-161.
50. McGonigle T.P., Miller M.H., Evans D.G., Fairchild G.L., Swan J.A. Anew method which gives an objective measure of colonization of roots by vesicular mycorrhizal fungi. New Phytologist 1990, 115:495-501.
51. Neumann A., Torstensson G., Aronsson H. Nitrogen and phosphorus leaching losses from potatoes with different harvest times and following crops. Field Crops Research 2012, 133:130-138.
52. Nyfeler D., Huguenin-Elie O., Suter M., Frossard E., Connolly J., Luscher A. Strong mixture effects among four species in fertilized agricultural grassland led to persistent and consistent transgressive overyielding. Journal of Applied Ecology 2009, 46:683-691.
53. Oehl F., Laczko E., Bogenrieder A., Stahr K., Bosch R., van der Heijden M., Sieverding E. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biology & Biochemistry 2010, 42:724-738.
54. Olsson P.A., Bååth E., Jakobsen I., Söderström B. The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycological research 1995, 99:623-629.
55. Philippot L., Hallin S., Borjesson G., Baggs E.M. Biochemical cycling in the rhizosphere having an impact on global change. Plant and Soil 2009, 321:61-81.
56. Plante A.F. Soil biochemical cycling of inorganic nutrients and metals. Soil Microbiology, Ecology and Biochemistry 2007, 389-432. Springer, New York, New York, USA. E.A. Paul (Ed.).
57. Pote D., Daniel T., DeLaune P. Total phosphorus and total dissolved phosphorus in water samples. Methods of Phosphorus Analysis for Soils, Sediments, Residuals, and Waters 2009, 113-117. Virginia Tech University, Blacksburg, VA, USA. second ed. J. Kovar, G. Pierzynski (Eds.).
58. R Core Team R: a Language and Environment for Statistical Computing 2011, R Foundation for Statistical Computing, Vienna, Austria.
59. Reynolds H.L., Hartley A.E., Vogelsang K.M., Bever J.D., Schultz P.A. Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytologist 2005, 167:869-880.
60. Rillig M.C. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 2004, 7:740-754.
61. Robertson G.P., Groffman P.M. Nitrogen transformations. Soil Microbiology, Biochemistry, and Ecology 2007, 341-364. Springer, New York, New York, USA. E.A. Paul (Ed.).
62. Sanders F.E., Tinker P.B. Mechanism of absorption of phosphate from soil by endogene mycorrhizas. Nature 1971, 233:278.
63. Schlesinger W.H. On the fate of anthropogenic nitrogen. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:203-208.
64. Schoenau J.J., Bettany J.R. Organic-matter leaching as a component of carbon, nitrogen, phosphorus, and sulfur cycles in a forest, grassland, and gleyed soil. Soil Science Society of America Journal 1987, 51:646-651.
65. Schüßler A., Walker C. The Glomeromycota: a Species List with New Families and New Genera 2010.
66. Seitzinger S., Harrison J.A., Bohlke J.K., Bouwman A.F., Lowrance R., Peterson B., Tobias C., Van Drecht G. Denitrification across landscapes and waterscapes: a synthesis. Ecological Applications 2006, 16:2064-2090.
67. Smil V. Nitrogen in crop production: an account of global flows. Global Biogeochemical Cycles 1999, 13:647-662.
68. Smith S.E., Smith F.A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 2011, 227-250. S.S. Merchant, W. Briggs, D. Ort (Eds.).
69. Smith S.E., Smith F.A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 2011, 62:227-250.
70. Smolander A., Kitunen V., Malkonen E. Dissolved soil organic nitrogen and carbon in a Norway spruce stand and an adjacent clear-cut. Biology and Fertility of Soils 2001, 33:190-196.
71. Tanaka Y., Yano K. Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell and Environment 2005, 28:1247-1254.
72. Troelstra S.R., Wagenaar R., Deboer W. Nitrification in Dutch heathland soils. 1. General soil characteristics and nitrification in undisturbed soil cores. Plant and Soil 1990, 127:179-192.
73. Ulén B. Leaching and balances of phosphorus and other nutrients in lysimeters after application of organic manures or fertilizers. Soil Use and Management 1999, 15:56-61.
74. van Aarle I.M., Olsson P.A., Soderstrom B. Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytologist 2002, 155:173-182.
75. van der Heijden M.G.A. Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 2010, 91:1163-1171.
76. van der Heijden M.G.A., Bardgett R.D., van Straalen N.M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 2008, 11:296-310.
77. van der Heijden M.G.A., Streitwolf-Engel R., Riedl R., Siegrist S., Neudecker A., Ineichen K., Boller T., Wiemken A., Sanders I.R. The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytologist 2006, 172:739-752.
78. van der Salm C., Dolfing J., Heinen M., Velthof G.L. Estimation of nitrogen losses via denitrification from a heavy clay soil under grass. Agriculture Ecosystems & Environment 2007, 119:311-319.
79. Van Vuuren D.P., Bouwman A.F., Beusen A.H.W. Phosphorus demand for the 1970-2100 period: a scenario analysis of resource depletion. Global Environmental Change-Human and Policy Dimensions 2010, 20:428-439.
80. Vance C.P. Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiology 2001, 127:390-397.
81. Vance E.D., Brookes P.C., Jenkinson D.S. An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry 1987, 19:703-707.
82. Veresoglou S.D., Chen B.D., Rillig M.C. Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology & Biochemistry 2012, 46:53-62.
83. Vierheilig H., Coughlan A.P., Wyss U., Piche Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 1998, 64:5004-5007.
84. Wagg C., Bender S.F., Widmer F., van der Heijden M.G.A. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences 2014, 111:5266-5270.
85. 3 extracts from soil 1. Soil Science Society of America Journal 1965, 29:677-678.
86. Weaver D.M., Ritchie G.S.P., Anderson G.C., Deeley D.M. Phosphorus leaching in sandy soils.I. Short-term effects of fertilizer applications and environmental conditions. Australian Journal of Soil Research 1988, 26:177-190.
87. Whiteside M.D., Garcia M.O., Treseder K.K. Amino acid uptake in arbuscular mycorrhizal plants. PloS One 2012, 7.
88. Whiteside M.D., Treseder K.K., Atsatt P.R. The brighter side of soils: quantum dots track organic nitrogen through fungi and plants. Ecology 2009, 90:100-108.