Abstract
Arbuscular mycorrhizal (AM) fungi are key components of most agricultural ecosystems. Therefore, understanding the impact of agricultural practices on their community structure is essential to improve nutrient mobilization and reduce plant stress in the field. The effects of five different organic or mineral sources of phosphorus (P) for a maize–soybean rotation system on AM fungal diversity in roots and soil were assessed over a 3-year period. Total DNA was extracted from root and soil samples collected at three different plant growth stages. An 18S rRNA gene fragment was amplified and taxa were detected and identified using denaturing gradient gel electrophoresis followed by sequencing. AM fungal biomass was estimated by fatty acid methyl ester analysis. Soil P fertility parameters were also monitored and analyzed for possible changes related with fertilization or growth stages. Seven AM fungal ribotypes were detected. Fertilization significantly modified soil P flux, but had barely any effect on AM fungi community structure or biomass. There was no difference in the AM fungal community between plant growth stages. Specific ribotypes could not be significantly associated to P treatment. Ribotypes were associated with root or soil samples with variable detection frequencies between seasons. AM fungal biomass remained stable throughout the growing seasons. This study demonstrated that roots and soil host distinct AM fungal communities and that these are very temporally stable. The influence of contrasting forms of P fertilizers was not significant over 3 years of crop rotation.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-012-0459-6/MediaObjects/572_2012_459_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-012-0459-6/MediaObjects/572_2012_459_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00572-012-0459-6/MediaObjects/572_2012_459_Fig3_HTML.gif)
Similar content being viewed by others
References
Allen MF, Smith WK, Moore TS, Christensen M (1981) Comparative water relation and photosynthesis of mycorrhizal and non-mycorrhizal Bouteloua gracilis. New Phytol 88:683–693
Anonymous (1976) Inorganic phosphorus in water and wastewater. Industrial method no. 93–70W/B. Technicon Industrial Systems, Tarrytown, NY
Appoloni S, Lekberg Y, Tercek MT, Zabinski CA, Redecker D (2008) Molecular community analysis of arbuscular mycorrhizal fungi in roots of geothermal soils in Yellowstone National Park (USA). Microbial Ecol 56:649–659
Balser TC, Treseder KK, Ekenler M (2005) Using lipid analysis and hyphal length to quantify AM and saprotrophic fungal abundance along a soil chronosequence. Soil Biol Biochem 37:601–604
Beauregard M-S (2010) Impacts de la fertilisation phosphatée sur la biodiversité microbienne de sols agricoles. Ph.D. thesis, Université de Montréal
Beauregard M-S, Hamel C, Atul-Nayyar S-AM (2010) Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol 59:379–389
Bedini S, Avio L, Argese E, Giovannetti M (2007) Effects of long-term land use on arbuscular mycorrhizal fungi and glomalin-related soil protein. Agric Ecosyst Environ 120:463–466
Bhadalung NN, Suwanarit A, Dell B, Nopamornbodi O, Thamchaipenet A, Rungchuang J (2005) Effects of long-term NP-fertilization on abundance and diversity of arbuscular mycorrhizal fungi under a maize crop** system. Plant Soil 270:371–382
Błaszkowski J, Wubet T, Harikumar VS, Ryszka P, Buscot F (2010) Glomus indicum, a new arbuscular mycorrhizal fungus. Botany 88:132–143
Boon E, Zimmerman E, Lang BF, Hijri M (2010) Intra-isolate genome variation in arbuscular mycorrhizal fungi persists in the transcriptome. J Evol Biol 23:1519–1527
Cruz AF, Hamel C, Hanson K, Selles F, Zentner RP (2009) Thirty-seven years of soil nitrogen and phosphorus fertility management shapes the structure and function of the soil microbial community in a brown chernozem. Plant Soil 315:173–184
Dai M, Hamel C, St Arnaud M, He Y, Grant C, Lupway N, Janzen H, Malhi SS, Yang X, Zhou Z (2012) Arbuscular mycorrhizal fungi assemblages in Chernozem great groups revealed by massively parallel pyrosequencing. Can J Microbiol 58:81–92
Farrell M, Griffith GW, Hobbs PJ, Perkins WT, Jones D (2010) Microbial diversity and activity are increased by compost amendment of metal-contaminated soil. FEMS Microbiol Ecol 71:94–105
Galván GA, Parádi I, Burger K, Baar J, Kuyper TW, Scholten OE, Kik C (2009) Molecular diversity of arbuscular mycorrhizal fungi in onion roots from organic and conventional farming systems in the Netherlands. Mycorrhiza 19:317–328
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113:17–35
Graham JH, Abbott LK (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218
Hamel C (2007) Extraradical arbuscular mycorrhizal mycelia: shadowy figures in the soil. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production. Haworth, Binghampton, pp 1–36
Hamel C, Hanson K, Selles F, Cruz AF, Lemke R, McConkey B, Zentner R (2006) Seasonal and long-term resource-related variations in soil microbial communities in wheat-based rotations of the Canadian prairie. Soil Biol Biochem 38:2104–2116
Hassan SED, Boon E, St-Arnaud M, Hijri M (2011) Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol Ecol 20:3469–3483
He JZ, Zheng Y, Chen CR, He YQ, Zhang LM (2008) Microbial composition and diversity of an upland red soil under long-term fertilization treatments as revealed by culture-dependent and culture-independent approaches. J Soils Sediments 8:349–358
Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385
Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938
Henry A, Kosola KR (1999) Root age and phosphorus effects on colonization of Andropogon gerardii by mycorrhizal fungi. Soil Biol Biochem 31:1657–1660
Hijri M, Hosny M, van Tuinen D, Dulieu H (1999) Intraspecific ITS polymorphism in Scutellospora castanea (Glomales, Zygomycota) is structured within multinucleate spores. Fungal Genet Biol 26:141–151
Imboden DM (1974) Phosphorus model of lake eutrophication. Limnol Oceanogr 19:297–304
INVAM (2008) Voucher specimens of Glomus fasciculatum. International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi. Available at http://invamcafwvuedu/fungi/taxonomy/Glomaceae/Glomus/fasciculatum/fascichtm
Johnson NC, Zak DR, Tilman D, Pfleger FL (1991) Dynamics of vesicular–arbuscular mycorrhizae during old field succession. Oecologia 86:349–358
Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515
Joner EJ (2000) The effect of long-term fertilization with organic or inorganic fertilizers on mycorrhiza-mediated phosphorus uptake in subterranean clover. Biol Fertil Soils 32:435–440
Kabir Z, O’Halloran IP, Fyles JW, Hamel C (1997) Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization: hyphal density and mycorrhizal root colonization. Plant Soil 192:285–293
Kernaghan G (2005) Mycorrhizal diversity: cause and effect? Pedobiologia 49:511–520
Kirchmann H, Thorvaldsson G (2000) Challenging targets for future agriculture. Europ J Agron 12:145–161
Kowalchuk GA, De Souza FA, van Veen JA (2002) Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol Ecol 11:571–581
Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748
Lee J-E, Eom A-H (2009) Effect of organic farming on spore diversity of arbuscular mycorrhizal fungi and glomalin in soil. Mycobiology 37:272–276
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349
Liang Z, Drijber RA, Lee DJ, Dwiekat IM, Harris SD, Wedin DA (2008) A DGGE-cloning method to characterize arbuscular mycorrhizal community structure in soil. Soil Biol Biochem 39:956–966
Liu F, Liang W, Zhang X, Jiang Y, Wang J (2008) Changes in soil microbial biomass and bacterial community in a long-term fertilization experiment during the growth of maize. Adv Environ Biol 2:1–8
Mathimaran N, Ruh R, Vullioud P, Frossard E, Jansa J (2005) Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 16:61–66
Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583
Olsson PA, Thingstrup I, Jakobsen I, Baath F (1999) Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biol Biochem 31:1879–1887
Öpik M, Moora M, Liira J, Koljalg U, Zobel M, Sen R (2003) Divergent arbuscular mycorrhizal fungal communities colonize roots of Pulsatilla spp. in boreal Scots pine forest and grassland soils. New Phytol 160:581–593
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790
Pankhurst CE, Pierret A, Hawke BG, Kirby JM (2002) Microbiological and chemical properties of soil associated with macropores at different depths in a red-duplex soil in NSW Australia. Plant Soil 238:11–20
Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2007) Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant Soil 296:65–75
Read DJ (1998) Plants on the web. Nature 396:22–23
Rosendahl S, Stukenbrock E (2004) Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186
Rubio R, Boriea F, Schalchlia C, Castillo C, Azcón R (2003) Occurrence and effect of arbuscular mycorrhizal propagules in wheat as affected by the source and amount of phosphorus fertilizer and fungal inoculation. Appl Soil Ecol 23:245–255
Ryan MH, Graham JH (2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263–271
Santos JC, Finlay RD, Tehler A (2006) Molecular analysis of arbuscular mycorrhizal fungi colonising a semi-natural grassland along a fertilisation gradient. New Phytol 172:159–168
Schalamuk S, Velazquez S, Chidichimo H, Cabello M (2006) Fungal spore diversity of arbuscular mycorrhizal fungi associated with spring wheat: effects of tillage. Mycologia 98:16–22
Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246
Scheublin TR, Van Logtestijn RSP, Van der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638
Schloter M, Dilly O, Munch JC (2003) Indicators for evaluating soil quality. Agric Ecosyst Environ 98:255–262
Schüßler A, Gehrig H, Schwarzott D, Walker C (2001) Analysis of partial Glomales SSU rRNA gene sequences: implications for primer design and phylogeny. Mycol Res 105:5–15
Sjöberg J, Persson P, Martensson A, Mattsson L, Adholeya A, Alstrom S (2004) Occurrence of Glomeromycota spores and some arbuscular mycorrhiza fungal species in arable fields in Sweden. Acta Agric Scand B Soil Plant Sci 54:202–212
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, San Diego
Soil Classification Working Group (1998) The Canadian system of soil classification. NRC Research Press, Ottawa, 187 p, Publication No. 1646
St-Arnaud M, Vujanovic V (2007) Effects of the arbuscular mycorrhizal symbiosis on plant diseases and pests. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production. Haworth, New York, pp 67–122
Stockinger H, Kruger M, Schußler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474
Sykorova Z, Ineichen K, Wiemken A, Redecker D (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14
Tarkalson DD, Jolley VD, Robbins CW, Terry RE (1998) Mycorrhizal colonization and nutrition of wheat and sweet corn grown in manure-treated and untreated topsoil and subsoil. J Plant Nutr 21:1985–1999
Ter Braak C, Smilauer P (2002) CANOCO reference manual and canodraw for Windows User’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca
Thomas RL, Shearc RW, Moyer JR (1967) Comparison of conventional and automated procedures for nitrogen, phosphorus, and potassium analysis of plant material using a single digestion. Agron J 59:240–243
Toljander JF, Santos-González JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338
Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983
van der Heijden MGA, Klironomos J, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders I (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095
Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular–mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007
Walker C, Koske RE (1987) Taxonomic concepts in the Endogonaceae: IV. Glomus fasciculatum redescribed. Mycotaxon 30:253–262
Yergeau E, Vujanovic V, St-Arnaud M (2006) Changes in communities of Fusarium and arbuscular mycorrhizal fungi as related to different asparagus cultural factors. Microb Ecol 52:104–113
Acknowledgments
The authors are grateful to Saad El Din Hassan and Stéphane Daigle for their help with the phylogenetic and statistical analyses, Keith G. Hanson and Mary-Anne Reeb for their help with the soil and plant variables data; Brian Hohner, George Stasko, Karl Rinas, and the farm crew at the GPCRC for the field plots establishment, management, and samplings. This work was supported by an Agriculture and Agri-Food Canada GAPS team grant allocated to C. Hamel and collaborators and by an NSERC discovery grant to M. St-Arnaud.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Beauregard, M.S., Gauthier, MP., Hamel, C. et al. Various forms of organic and inorganic P fertilizers did not negatively affect soil- and root-inhabiting AM fungi in a maize–soybean rotation system. Mycorrhiza 23, 143–154 (2013). https://doi.org/10.1007/s00572-012-0459-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-012-0459-6