Abstract
Short-term effects of soil physical disturbance by ploughing and nitrogen and phosphate fertilisation on arbuscular mycorrhizal fungal (AMF) communities and on intraspecific populations of Rhizophagus irregularis in a buffer strip surrounded by arable fields were studied. Pre-grown Plantago lanceolata plantlets were transplanted into fertilised and/or ploughed experimental plots. After 3 months, the glomeromycotan communities in the roots of these trap plants were analysed using 454 pyrosequencing of a fragment of the RNA polymerase II gene (RPB1). Intraspecific populations of R. irregularis were studied by restriction fragment length polymorphism (RFLP) analysis of the mitochondrial large ribosomal subunit (mtLSU) gene. Soil disturbance significantly increased the diversity of species-level molecular taxa (MTs) and altered community structure, whilst fertilisation alone had no significant effect, unless coupled with ploughing. At the population level, the expected shift from genotypes of R. irregularis typically found in grasslands to those usually found in arable sites was only partially observed. In conclusion, in the short-term, physical soil disturbance, as well as nitrogen fertilisation when coupled with physical soil disturbance, affected AMF community and to a smaller extent population composition.
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References
Alguacil MM, Lumini E, Roldan A, Salinas-Garcia JR, Bonfante P, Bianciotto V (2008) The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol Appl 18:527–536. doi:10.1890/07-0521.1
Alguacil MM, Lozano Z, Campoy JM, Roldán A (2010) Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol Biochem 1114–1122. doi:10.1016/j.soilbio.2010.03.012
Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565. doi:10.1111/j.1365-294X.2010.04898.x
Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR (2010) Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Curr Biol 20:1216–1221. doi:10.1016/j.cub.2010.05.031
Avio L, Castaldini M, Fabiani A, Bedini S, Sbrana C, Turrini A, Giovannetti M (2013) Impact of nitrogen fertilisation and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem. Soil Biol Biochem 67:285–294. doi:10.1016/j.soilbio.2013.09.005
Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64:269–285. doi:10.1016/j.ecolecon.2007.03.004
Berger SA, Stamatakis A (2011) Aligning short reads to reference alignments and trees. Bioinformatics 27:2068–2075. doi:10.1093/bioinformatics/btr320
Boddington CL, Dodd JC (2000) The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. II. Studies in experimental microcosms. Plant Soil 218:145–157. doi:10.1023/A:1014911318284
Bonfield JK, Smith KF, Staden R (1995) A new DNA sequence assembly program. Nucl Acids Res 23:4992–4999. doi:10.1093/nar/23.24.4992
Borriello R, Lumini E, Girlanda M, Bonfante P, Bianciotto V (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol Fertil Soils 48:911–922. doi:10.1007/s00374-012-0683-4
Börstler B, Raab PA, Thiéry O, Morton JB, Redecker D (2008) Genetic diversity of the arbuscular mycorrhizal fungus Glomus intraradices as determined by mitochondrial large subunit rRNA gene sequences is considerably higher than previously expected. New Phytol 180:452–465. doi:10.1111/j.1469-8137.2008.02574.x
Börstler B, Thiéry O, Sýkorová Z, Berner A, Redecker D (2010) Diversity of mitochondrial large subunit rDNA haplotypes of Glomus intraradices in two agricultural field experiments and two semi-natural grasslands. Mol Ecol 19:1497–1511. doi:10.1111/j.1365-294X.2010.04590.x
Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3546–3659. doi:10.1111/gcb.12618
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. doi:10.1093/bioinformatics/btp636
Caporaso JG, Kuczynski J, Stombaugh J et al (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303
Dai M, Bainard LD, Hamel C, Gan Y, Lynch D (2013) Impact of land use on arbuscular mycorrhizal fungal communities in rural Canada. Appl Environ Microbiol 79:6719–6729. doi:10.1128/AEM.01333-13
Daniell TJ, Husband R, Fitter AH, Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36:203–209. doi:10.1111/j.1574-6941.2001.tb00841.x
De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology, URL http://sites.google.com/site/miqueldecaceres/
De Cauwer B, Reheul D, D’Hooghe K, Nijs I, Milbau A (2006) Disturbance effects on early succession of field margins along the shaded and unshaded side of a tree lane. Agr Ecosyst Environ 112:78–86. doi:10.1016/j.agee.2005.07.006
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:325–337. doi:10.1038/ismej.2010.48
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381
Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496. doi:10.1890/1051-0761(2000)010[0484:SIAMCA]2.0.CO;2
Eom AH, Hartnett DC, Wilson GWT, Figge DAH (1999) The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. Am Midl Nat 142:55–70. doi:10.1674/0003-0031(1999)142[0055:TEOFMA]2.0.CO;2
Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biol Rev 25:68–72. doi:10.1016/j.fbr.2011.01.002
Fraterrigo JM, Turner MG, Pearson SM, Dixon P (2005) Effects of past land use on spatial heterogeneity of soil nutrients in southern appalachian forests. Ecol Monogr 75:215–230. doi:10.1890/03-0475
Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) (2002) Mycorrhizal technology in agriculture: from genes to bioproducts. Birkhäuser Verlag, Switzerland
Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker R, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530. doi:10.1007/s00572-010-0333-3
Gosling P, Proctor M, Jones J, Bending GD (2014) Distribution and diversity of Paraglomus spp. in tilled agricultural soils. Mycorrhiza 24:1–11. doi:10.1007/s00572-013-0505-z
Grubb PJ (1977) Maintenance of species-richness in plant communities—importance of regeneration niche. Biol Rev Camb Philos 52:107–145. doi:10.1111/j.1469-185X.1977.tb01347.x
Hao XL, Jiang R, Chen T (2011) Clustering 16S rRNA for OTU prediction: a method of unsupervised Bayesian clustering. Bioinformatics 27:611–618. doi:10.1093/bioinformatics/btq725
Harris JK, Sahl JW, Castoe TA, Wagner BD, Pollock DD, Spear JR (2010) Comparison of normalization methods for construction of large, multiplex amplicon pools for next-generation sequencing. Appl Environ Microbiol 76:3863–3868. doi:10.1128/AEM.02585-09
Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429. doi:10.1105/tpc.004861
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344. doi:10.1046/j.0028-646X.2001.00312.x
Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431. doi:10.1038/28764
Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384. doi:10.1046/j.1365-2745.2001.00674.x
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. doi:10.1111/j.1462-2920.2007.01309.x
Hiiesalu I, Partel M, Davison J, Gerhold P, Metsis M, Moora M, Öpik M, Vasar M, Zobel M, Wilson SD (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244. doi:10.1111/nph.12765
Hijri I, Sýkorová Z, Oehl F, Ineichen K, Mäder P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289. doi:10.1111/j.1365-294X.2006.02921.x
Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678. doi:10.1046/j.1365-294X.2002.01647.x
James TY, Kauff F, Schoch CL et al (2006) Reconstructing the early evolution of Fungi using six-gene phylogeny. Nature 443:818–824. doi:10.1038/nature05110
Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234. doi:10.1007/s005572-002-0163-z
Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176. doi:10.1890/1051-0761(2003)13[1164:STATCS]2.0.CO;2
Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276:163–176. doi:10.1007/s11104-005-4274-0
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789. doi:10.1111/j.1469-8137.2007.02294.x
Jansa J, Erb A, Oberholzer HS, Smilauer P, Egli S (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol 23:2118–2135. doi:10.1111/mec.12706
Jasper DA, Abbott LK, Robson AD (1991) The effect of soil disturbance on vesicular-arbuscular mycorrhizal fungi in soils from different vegetation types. New Phytol 118:471–476. doi:10.1111/j.1469-8137.1991.tb00029.x
Jeffries P, Gianinazzi S, Perotto S, Turanu K, Barea M (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16. doi:10.1007/s00374-002-0546-5
Kiers ET, van der Heijden MGA (2006) Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87:1627–1636. doi:10.1890/0012-9658(2006)87[1627:MSITAM]2.0.CO;2
Kim YC, Gao C, Zheng Y, He XH, Chen L, Wan SQ, Guo LD (2014) Arbuscular mycorrhizal fungal community response to warming and nitrogen addition in a semi-arid steppe ecosystem. Mycorrhiza. doi:10.1007/s00572-014-0608-1
Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungal. Proc Natl Acad Sci U S A 101:2369–2371. doi:10.1073/pnas.0306441101
Koch AM, Croll D, Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecol Lett 9:103–110. doi:10.1111/j.1461-0248.2005.00853.x
Kohout P, Sudova R, Janouskova M, Ctvrtlikova M, Hejda M, Pankova H, Slavikova R, Stajerova K, Vosatka M, Sýkorová Z (2014) Comparison of commonly used primer sets for evaluating arbuscular mycorrhizal fungal communities: is there a universal solution? Soil Biol Biochem 68:482–493. doi:10.1016/j.soilbio.2013.08.027
Landis FC, Gargas A, Givnish TJ (2004) Relationships among arbuscular mycorrhizal fungi, vascular plants and environmental conditions in oak savannas. New Phytol 164:493–504. doi:10.1111/j.1469-8137.2004.01202.x
Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045. doi:10.1139/B04-060
Lekberg Y, Schnoor T, Kjoller R, Gibbons SM, Hansen LH, Al-Soud WA, Sorensen SJ, Rosendahl S (2012) 454-sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J Ecol 100:151–160. doi:10.1111/j.1365-2745.2011.01894.x
Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433. doi:10.1038/ismej.2013.41
Lin X, Feng Y, Zhang H, Chen R, Wang J, Zhang J, Chu H (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in north China revealed by 454 pyrosequencing. Environ Sci Technol 46:5764–5771. doi:10.1021/es3001695
Liu YJ, Shi GX, Mao L, Cheng G, Jiang SJ, Ma XJ, An LZ, Du GZ, Johnson NC, Feng HY (2012) Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523–535. doi:10.1111/1574-6941.12361
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005
Ludwig W, Strunk O, Westram R et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. doi:10.1093/nar/gkh293
Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179. doi:10.1111/j.1462-2920.2009.02099.x
Mäder P, Edenhofer S, Boller T, Wiemken A, Niggli U (2000) Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol Fertil Soils 31:150–156. doi:10.1007/s003740050638
Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364. doi:10.1111/j.1469-8137.2004.01169.x
Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824. doi:10.1128/AEM.69.5.2816-2824.2003
Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283. doi:10.1111/j.1469-8137.2004.01235.x
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-9. http://CRAN.R-project.org/package=vegan
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. doi:10.1111/j.1365-2745.2006.01136.x
Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179:867–876. doi:10.1111/j.1469-8137.2008.02515.x
Pinheiro J, Bates D, Debroy S, Sarkar D, R core team (2014) Package nmle. Linear and nonlinear mixed effects models. http://CRAN.R-project.org/package=nlme
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. doi:10.1007/s11104-007-9290-9
R development core team (2013) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, ISBN 3-900051-07-0, URL http://www.R-project.org/
Ranwez V, Harispe S, Delsuc F, Douzery EJP (2011) MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One 6, e22594. doi:10.1371/journal.pone.0022594
Redecker D, Raab P (2006) Phylogeny of the Glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers. Mycologia 98:885–895. doi:10.3852/mycologia.98.6.885
Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531. doi:10.1007/s00572-013-0486-y
Robertson GP, Crum JR, Ellis BG (1993) The spatial variability of soil resources following long-term disturbance. Oecologia 96:451–456. doi:10.1007/BF00320501
Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266. doi:10.1111/j.1469-8137.2008.02378.x
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. doi:10.1111/j.1469-8137.2006.01799.x
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. doi:10.1111/j.1365-2745.2007.01244.x
Schnoor TK, Olsson PA (2010) Effects of soil disturbance on plant diversity of calcareous grasslands. Agr Ecosyst Environ 139:714–719. doi:10.1016/j.agee.2010.10.018
Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21:211–220. doi:10.1007/s00572-010-0325-3
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246. doi:10.1073/pnas.1117018109
Smilauer P (2001) Communities of arbuscular mycorrhizal fungi in grassland: seasonal variability and effects of environment and host plants. Folia Geobot 36:243–263. doi:10.1007/BF02803179
Stockinger H, Walker C, Schüßler A (2009) ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187, http://www.jstor.org/stable/40302144
Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474. doi:10.1111/j.1469-8137.2010.03262.x
Stockinger H, Peyret-Guzzon M, Bouffaud ML, Koegel S, Redecker D (2014) The largest subunit of RNA polymerase II as a new marker gene to study assemblages of arbuscular mycorrhizal fungi in the field. PLoS One 9, e107783. doi:10.1371/journal.pone.0107783
Sýkorová Z, Ineichen K, Wiemken A, Redecker D (2007a) 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. doi:10.1007/s00572-007-0147-0
Sýkorová Z, Wiemken A, Redecker D (2007b) Cooccurring Gentiana verna and Gentiana acaulis and their neighboring plants in two Swiss upper montane meadows harbor distinct arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 73:5426–5434. doi:10.1128/AEM.00987-07
Thian H, Drijber RA, Zhang JL, Li XL (2013) Impact of long-term nitrogen fertilization and rotation with soybean on the diversity and phosphorus metabolism of indigenous arbuscular mycorrhizal fungi within the roots of maize (Zea mays L.). Agric Ecosyst Environ 164:53–61. doi:10.1016/j.agee.2012.09.007
Thonar C, Erb A, Jansa J (2012) Real‐time PCR to quantify composition of arbuscular mycorrhizal fungal communities—marker design, verification, calibration and field validation. Mol Ecol Resour 12:219–232. doi:10.1111/j.1755-0998.2011.03086.x
Toljander JF, Santos-Gonzalez 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. doi:10.1111/j.1574-6941.2008.00512.x
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methodes d’estimation ayant une signification fonctionnelle. Physiological and genetical aspects of mycorrhizae. Proceedings of the 1st European Symposium on Mycorrhizae. INRA, Paris, pp 217–221
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72. doi:10.1038/23932
van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578. doi:10.1046/j.1469-8137.2003.00688.x
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. doi:10.1111/j.1461-0248.2007.01139.x
Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPM (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095. doi:10.1046/j.1365-294X.2003.01967.x
Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560. doi:10.1111/j.1752-4571.2010.00145.x
Verbruggen E, Roling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, van der Heijden MGA (2010) Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol 186:968–979. doi:10.1111/j.1469-8137.2010.03230.x
Vickery JA, Bradbury RB, Henderson IG, Eaton MA, Grice PV (2004) The role of agri-environment schemes and farm management practices in reversing the decline of farmland birds in England. Biol Conserv 119:19–39. doi:10.1016/j.biocon.2003.06.004
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/AEM.00062-07
Wilson SD, Tilman D (1993) Plant competition and resource availability in response to disturbance and fertilization. Ecology 74:599–611. doi:10.2307/1939319
Yu L, Nicolaisen M, Larsen J, Ravnskov S (2012) Succession of root-associated fungi in Pisum sativum during a plant growth cycle as examined by 454 pyrosequencing. Plant Soil 358:216–224. doi:10.1007/s11104-012-1188-5
Acknowledgments
The authors are grateful to Marie-Hélène Bernicaut, Philippe Chamois, Annie Colombet, Odile Chatagnier, Bernard Alixant, Eric Bernaud, Diederik van Tuinen, Romain Barnard, Aymé Spor and Nassybat Binti Said Ismaïl for their helpful participation and comments in this study, which was funded by the gratefully acknowledged Burgundy Region (FABER programme no. 2010-9201AAO047S01404).
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The authors declare that they have no competing interest.
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Online Resource 1
Schematic representation of the experimental set-up used at the experimental domain of Epoisses at Bretenières, Burgundy region, France. a. Overview of the experimental design: unploughed plots are shown in grey, ploughed plots in white. Fertilisation treatments (+N, 100 kg ha−1 of nitrogen; +P, 30 kg ha−1 of phosphorus; +N+P, combined fertilisation; C, no fertilisation) were randomly arranged within each strip of the ploughing treatment. b. Zoom on a plot showing planting pattern of Plantago lanceolata trap plant, pre-grown in a climate chamber during 1 month. (PDF 322 kb)
Online Resource 2
Sequences used for the RPB1 reference tree. Bold characters refer to new sequences. (PDF 508 kb)
Online Resource 3
Maximum likelihood tree of RPB1 sequences used as reference tree to assign operational taxonomic units to molecular taxa (MTs). Branch support values are based on 1000 bootstrap replicates using RAxML software. Mortierella verticillata and Mucor hiemalis were chosen as outgroups to root the tree. (PDF 333 kb)
Online Resource 4
Accumulation curve analysis of observed OTU numbers versus cumulative sequence number by sample (different colours) before (a) and after (b) subsampling to a 1400 sequence threshold (represented by the dotted line). (PDF 569 kb)
Online Resource 5
Number of RPB1 sequence reads retained per sample after sub-sampling to a threshold of 1400 sequence reads at the species-level molecular taxa (MT). Numbers of OTUs found for each MT are in brackets. (PDF 492 kb)
Online Resource 6
Data table of Plantago lanceolata fresh shoot weight, dry root weight and root colonisation parameters (estimation by Trouvelot et al. 1986) and estimation of plant species richness found in each plot (other than P. lanceolata) according to soil treatment (physical soil disturbance and fertilisation treatments). (PDF 169 kb)
Online Resource 7
Statistical significance (P value) of indicator species analysis based on species-level molecular taxa (MT) after sub-sampling to a threshold of 1400 sequences. Only species with more than 100 sequences over the total read number and having both sensitivity and specificity values higher than 0.75 were kept. (PDF 261 kb)
Online Resource 8
Variance of species abundance reads using a nested linear mixed model showing effects of nitrogen and phosphorus fertilisation within the physical soil disturbance treatments randomised by block. Significant results (P < 0.05) are in bold type. Red dollar symbols show indicator species identified by the De Caceres-Jansen index using 2000 permutations. (PDF 297 kb)
Online Resource 9
Restriction fragment length polymorphism patterns (=RFLP types) of the mitochondrial rRNA subunit gene region from root-colonising Rhizophagus irregularis, obtained using primers RNL-29/ RNL-30. Numbers of clones of each RFLP type are listed per treatment. (PDF 455 kb)
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Peyret-Guzzon, M., Stockinger, H., Bouffaud, ML. et al. Arbuscular mycorrhizal fungal communities and Rhizophagus irregularis populations shift in response to short-term ploughing and fertilisation in a buffer strip. Mycorrhiza 26, 33–46 (2016). https://doi.org/10.1007/s00572-015-0644-5
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DOI: https://doi.org/10.1007/s00572-015-0644-5