Inoculation with arbuscular mycorrhizal fungi (AMF) may improve plant performance at disturbed sites, but inoculation may also suppress root colonization by native AMF and decrease the diversity of the root-colonizing AMF community. This has been shown for the roots of directly inoculated plants, but little is known about the stability of inoculation effects, and to which degree the inoculant and the inoculation-induced changes in AMF community composition spread into newly emerging seedlings that were not in direct contact with the introduced propagules. We addressed this topic in a greenhouse experiment based on the soil and native AMF community of a post-mining site. Plants were cultivated in compartmented pots with substrate containing the native AMF community, where AMF extraradical mycelium radiating from directly inoculated plants was allowed to inoculate neighboring plants. The abundances of the inoculated isolate and of native AMF taxa were monitored in the roots of the directly inoculated plants and the neighboring plants by quantitative real-time PCR. As expected, inoculation suppressed root colonization of the directly inoculated plants by other AMF taxa of the native AMF community and also by native genotypes of the same species as used for inoculation. In the neighboring plants, high abundance of the inoculant and the suppression of native AMF were maintained. Thus, we demonstrate that inoculation effects on native AMF propagate into plants that were not in direct contact with the introduced inoculum, and are therefore likely to persist at the site of inoculation.

Institute of Botany The Czech Academy of Sciences Průhonice Czech Republic

Institute of Experimental Botany The Czech Academy of Sciences Praha Czech Republic

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Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters. 2010;13(3):394–407. doi: 10.1111/j.1461-0248.2009.01430.x PubMed DOI

Maherali H, Klironomos JN. Influence of Phylogeny on fungal community assembly and ecosystem functioning. Science. 2007;316(5832):1746–8. doi: 10.1126/science.1143082 PubMed DOI

Middleton EL, Richardson S, Koziol L, Palmer CE, Yermakov Z, Henning JA, et al. Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere. 2015;6(12). 276 doi: 10.1890/es15-00152.1 DOI

Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(5):2093–8. doi: 10.1073/pnas.0906710107 PubMed DOI PMC

Ji BM, Gehring CA, Wilson GWT, Miller RM, Flores-Renteria L, Johnson NC. Patterns of diversity and adaptation in Glomeromycota from three prairie grasslands. Molecular Ecology. 2013;22(9):2573–87. doi: 10.1111/mec.12268 PubMed DOI

Johnson NC. Responses of Salsola kali and Panicum virgatum to mycorrhizal fungi, phosphorus and soil organic matter: implications for reclamation. J Appl Ecol. 1998;35(1):86–94. doi: 10.1046/j.1365-2664.1998.00277.x DOI

Püschel D, Rydlová J, Vosátka M. Does the sequence of plant dominants affect mycorrhiza development in simulated succession on spoil banks? Plant Soil. 2008;302(1–2):273–82. doi: 10.1007/s11104-007-9480-5 DOI

Kabir Z, Ohalloran IP, Fyles JW, Hamel C. Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization: Hyphal density and mycorrhizal root colonization. Plant Soil. 1997;192(2):285–93. doi: 10.1023/a:1004205828485 DOI

Gavito ME, Miller MH. Changes in mycorrhiza development in maize induced by crop management practices. Plant Soil. 1998;198(2):185–92. doi: 10.1023/a:1004314406653 DOI

Pellegrino E, Turrini A, Gamper HA, Cafa G, Bonari E, Young JPW, et al. Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytologist. 2012;194(3):810–22. doi: 10.1111/j.1469-8137.2012.04090.x PubMed DOI

Ceballos I, Ruiz M, Fernandez C, Pena R, Rodriguez A, Sanders IR. The In Vitro Mass-Produced Model Mycorrhizal Fungus, Rhizophagus irregularis, Significantly Increases Yields of the Globally Important Food Security Crop Cassava. Plos One. 2013;8(8). e70633 doi: 10.1371/journal.pone.0070633 PubMed DOI PMC

Maltz MR, Treseder KK. Sources of inocula influence mycorrhizal colonization of plants in restoration projects: a meta-analysis. Restoration Ecology. 2015;23(5):625–34. doi: 10.1111/rec.12231 DOI

Berruti A, Lumini E, Balestrini R, Bianciotto V. Arbuscular Mycorrhizal Fungi as Natural Biofertilizers: Let's Benefit from Past Successes. Frontiers in Microbiology. 2016;6 1559 doi: 10.3389/fmicb.2015.01559 PubMed DOI PMC

Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, et al. Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions. 1999;1(1):3–19. doi: 10.1023/a:1010034312781 DOI

Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, et al. The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecology Letters. 2006;9(5):501–15. doi: 10.1111/j.1461-0248.2006.00910.x PubMed DOI

Symanczik S, Courty PE, Boller T, Wiemken A, Al-Yahya'ei MN. Impact of water regimes on an experimental community of four desert arbuscular mycorrhizal fungal (AMF) species, as affected by the introduction of a non-native AMF species. Mycorrhiza. 2015;25(8):639–47. doi: 10.1007/s00572-015-0638-3 PubMed DOI

Mummey DL, Antunes PM, Rillig MC. Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol Biochem. 2009;41(6):1173–9. doi: 10.1016/j.soilbio.2009.02.027 DOI

Koch AM, Antunes PM, Barto EK, Cipollini D, Mummey DL, Klironomos JN. The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biological Invasions. 2011;13(7):1627–39. doi: 10.1007/s10530-010-9920-7 DOI

Jin HY, Germida JJ, Walley FL. Impact of arbuscular mycorrhizal fungal inoculants on subsequent arbuscular mycorrhizal fungi colonization in pot-cultured field pea (Pisum sativum L.). Mycorrhiza. 2013;23(1):45–59. doi: 10.1007/s00572-012-0448-9 PubMed DOI

Sýkorová Z, Börstler B, Zvolenská S, Fehrer J, Gryndler M, Vosátka M, et al. Long-term tracing of Rhizophagus irregularis isolate BEG140 inoculated on Phalaris arundinacea in a coal mine spoil bank, using mitochondrial large subunit rDNA markers Mycorrhiza. 2011;22(1):69–80. doi: 10.1007/s00572-011-0375-1 PubMed DOI

Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M. Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil. 2010;335(1–2):311–23. doi: 10.1007/s11104-010-0417-z DOI

Janoušková M, Krak K, Wagg C, Štorchová H, Caklová P, Vosátka M. Effects of Inoculum Additions in the Presence of a Preestablished Arbuscular Mycorrhizal Fungal Community. Applied and Environmental Microbiology. 2013;79(20):6507–15. doi: 10.1128/AEM.02135-13 PubMed DOI PMC

Thonar C, Frossard E, Šmilauer P, Jansa J. Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi. Molecular Ecology. 2014;23(3):733–46. doi: 10.1111/mec.12625 PubMed DOI

Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytologist. 2004;164(2):357–64. doi: 10.1111/j.1469-8137.2004.01169.x PubMed DOI

Clapp JP, Rodriguez A, Dodd JC. Inter- and intra-isolate rRNA large subunit variation in Glomus coronatum spores. New Phytologist. 2001;149(3):539–54. doi: 10.1046/j.1469-8137.2001.00060.x PubMed DOI

Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR. High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(8):2369–74. doi: 10.1073/pnas.0306441101 PubMed DOI PMC

Avio L, Cristani C, Strani P, Giovannetti M. Genetic and phenotypic diversity of geographically different isolates of Glomus mosseae. Canadian Journal of Microbiology. 2009;55(3):242–53. doi: 10.1139/w08-129 PubMed DOI

Farmer MJ, Li X, Feng G, Zhao B, Chatagnier O, Gianinazzi S, et al. Molecular monitoring of field-inoculated AMF to evaluate persistence in sweet potato crops in China. Appl Soil Ecol. 2007;35(3):599–609. doi: 10.1016/j.apsoil.2006.09.012 DOI

Vierheilig H, Garcia-Garrido JM, Wyss U, Piche Y. Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem. 2000;32(5):589–95. doi: 10.1016/s0038-0717(99)00155-8 DOI

Werner GDA, Kiers ET. Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytologist. 2015;205(4):1515–24. doi: 10.1111/nph.13092 PubMed DOI

Gryndler M, Sudová R, Püschel D, Rydlová J, Janoušková M, Vosátka M. Cultivation of high-biomass crops on coal mine spoil banks: Can microbial inoculation compensate for high doses of organic matter? Bioresource Technology. 2008;99(14):6391–9. doi: 10.1016/j.biortech.2007.11.059 PubMed DOI

Krüger M, Stockinger H, Krüger C, Schüssler A. DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytologist. 2009;183(1):212–23. doi: 10.1111/j.1469-8137.2009.02835.x PubMed DOI

Robinson-Boyer L, Grzyb I, Jeffries P. Shifting the balance from qualitative to quantitative analysis of arbuscular mycorrhizal communities in field soils. Fungal Ecology. 2009;2:1–9. doi: 10.1016/j.funeco.2008.11.001 DOI

Börstler B, Thiery O, Sykorova Z, Berner A, Redecker D. Diversity of mitochondrial large subunit rDNA haplotypes of Glomus intraradices in two agricultural field experiments and two semi-natural grasslands. Molecular Ecology. 2010;19(7):1497–511. doi: 10.1111/j.1365-294X.2010.04590.x PubMed DOI

Krak K, Janoušková M, Caklová P, Vosátka M, Štorchová H. Intraradical Dynamics of Two Coexisting Isolates of the Arbuscular Mycorrhizal Fungus Glomus intraradices Sensu Lato as Estimated by Real-Time PCR of Mitochondrial DNA. Applied and Environmental Microbiology. 2012;78(10):3630–7. doi: 10.1128/AEM.00035-12 PubMed DOI PMC

Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research. 2007;35:W71–W4. doi: 10.1093/nar/gkm306 PubMed DOI PMC

Gryndler M, Vejsadová H, Vančura V. The effect of magnesium ions on the vesicular arbuscular mycorrhizal infection of maize roots. New Phytologist. 1992;122(3):455–60. doi: 10.1111/j.1469-8137.1992.tb00073.x PubMed DOI

Koske RE, Gemma JN. A modified procedure for staining roots to detect VA mycorrhizas. Mycological Research. 1989;92:486–505. doi: 10.1016/S0953-7562(89)80195-9 DOI

Ter Braak CJF, Šmilauer P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5.0. Ithaca, USA: Microcomputer Power; 2012.

Wilson JM. Competition for infection between vesicular arbuscular mycorrhizal fungi. New Phytologist. 1984;97(3):427–35. doi: 10.1111/j.1469-8137.1984.tb03608.x DOI

Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis. Science. 2011;333(6044):880–2. doi: 10.1126/science.1208473 PubMed DOI

Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN. Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytologist. 2011;189(2):507–14. doi: 10.1111/j.1469-8137.2010.03480.x PubMed DOI

Koch AM, Croll D, Sanders IR. Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecology Letters. 2006;9(2):103–10. doi: 10.1111/j.1461-0248.2005.00853.x PubMed DOI

Giovannetti M, Sbrana C, Strani P, Agnolucci M, Rinaudo V, Avio L. Genetic diversity of isolates of Glomus mosseae from different geographic areas detected by vegetative compatibility testing and biochemical and molecular analysis. Applied and Environmental Microbiology. 2003;69(1):616–24. doi: 10.1128/AEM.69.1.616-624.2003 PubMed DOI PMC

Croll D, Giovannetti M, Koch AM, Sbrana C, Ehinger M, Lammers PJ, et al. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist. 2009;181(4):924–37. doi: 10.1111/j.1469-8137.2008.02726.x PubMed DOI

Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, et al. A proposed unified framework for biological invasions. Trends in Ecology & Evolution. 2011;26(7):333–9. doi: 10.1016/j.tree.2011.03.023 PubMed DOI

Oehl F, Schneider D, Sieverding E, Burga CA. Succession of arbuscular mycorrhizal communities in the foreland of the retreating Morteratsch glacier in the Central Alps. Pedobiologia. 2011;54(5–6):321–31. doi: 10.1016/j.pedobi.2011.07.006 DOI

Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytologist. 2009;184(2):424–37. doi: 10.1111/j.1469-8137.2009.02920.x PubMed DOI

Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH. Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic processes? Journal of Ecology. 2010;98(2):419–28. doi: 10.1111/j.1365-2745.2009.01622.x DOI

Lekberg Y, Schnoor T, Kjoller R, Gibbons SM, Hansen LH, Al-Soud WA, et al. 454-sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. Journal of Ecology. 2012;100(1):151–60. doi: 10.1111/j.1365-2745.2011.01894.x DOI

Griffiths BS, Philippot L. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiology Reviews. 2013;37:112–29. doi: 10.1111/j.1574-6976.2012.00343.x PubMed DOI

Roger A, Colard A, Angelard C, Sanders IR. Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. Isme Journal. 2013;7(11):2137–46. doi: 10.1038/ismej.2013.112 PubMed DOI PMC

Raab PA, Brennwald A, Redecker D. Mitochondrial large ribosomal subunit sequences are homogeneous within isolates of Glomus (arbuscular mycorrhizal fungi, Glomeromycota). Mycological Research. 2005;109:1315–22. doi: 10.1017/s0953756205003977 PubMed DOI

Börstler B, Raab PA, Thiery O, Morton JB, Redecker D. 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 Phytologist. 2008;180(2):452–65. doi: 10.1111/j.1469-8137.2008.02574.x PubMed DOI

Peyret-Guzzon M, Stockinger H, Bouffaud ML, Farcy P, Wipf D, Redecker D. Arbuscular mycorrhizal fungal communities and Rhizophagus irregularis populations shift in response to short-term ploughing and fertilisation in a buffer strip. Mycorrhiza. 2016;26(1):33–46. doi: 10.1007/s00572-015-0644-5 PubMed DOI

Croll D, Corradi N, Gamper HA, Sanders IR. Multilocus genotyping of arbuscular mycorrhizal fungi and marker suitability for population genetics. New Phytologist. 2008;180(3):564–8. doi: 10.1111/j.1469-8137.2008.02602.x PubMed DOI

Pearson JN, Abbott LK, Jasper DA. Mediation of competition between 2 colonizing VA mycorrhizal fungi by the host plant. New Phytologist. 1993;123(1):93–8. doi: 10.1111/j.1469-8137.1993.tb04534.x PubMed DOI

Chagnon P-L, Bradley RL, Maherali H, Klironomos JN. A trait-based framework to understand life history of mycorrhizal fungi. Trends in Plant Science. 2013;18(9):484–491. doi: 10.1016/j.tplants.2013.05.001 PubMed DOI

Maherali H, Klironomos JN. Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. Plos One. 2012;7(5):e36695 doi: 10.1371/journal.pone.0036695 PubMed DOI PMC

Chen BD, Xiao X, Zhu Y-G, Smith FA, Xie ZM, Smith SE. The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquision by Medicago sativa Linn. Science of The Total Environment. 2007;379(2–3):226–234. doi: 10.1016/j.scitotenv.2006.07.038 PubMed DOI

Mensah JA, Koch AM, Antunes PM, Kiers ET, Hart M, Bücking H. High functional diversity within species of arbuscular mycorrhizal fungi is associated with differences in phosphate and nitrogen uptake and fungal phosphate metabolism. Mycorrhiza. 2015;25(7):533–546. doi: 10.1007/s00572-015-0631-x PubMed DOI

Lekberg Y, Koide RT. Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytologist. 2005;168(1):189–204. doi: 10.1111/j.1469-8137.2005.01490.x PubMed DOI

Pinior A, Wyss U, Piche Y, Vierheilig H. Plants colonized by AM fungi regulate further root colonization by AM fungi through altered root exudation. Canadian Journal of Botany-Revue Canadienne De Botanique. 1999;77(6):891–7. doi: 10.1139/b99-052 DOI

Jakobsen I. Transport of phosphorus and carbon in VA mycorrhizas In: Varma A HB, editor. Mycorrhiza, structure, function, molecular biology and biotechnology. Berlin / Heidelberg: Springer Verlag; 1995. p. 297–324.

Li HY, Zhu YG, Marschner P, Smith FA, Smith SE. 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 Soil. 2005;277(1–2):221–32. doi: 10.1007/s11104-005-7082-7 DOI

Kohl L, Lukasiewicz CE, van der Heijden MGA. Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant Cell and Environment. 2016;39(1):136–46. doi: 10.1111/pce.12600 PubMed DOI

Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET. Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytologist. 2013;197(4):1104–9. doi: 10.1111/j.1469-8137.2012.04348.x PubMed DOI

Abiotic contexts consistently influence mycorrhiza functioning independently of the composition of synthetic arbuscular mycorrhizal fungal communities