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Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts

Nature Ecology & Evolution volume 6, pages 1145–1154 (2022)Cite this article

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Abstract

Phosphorus (P) acquisition is key for plant growth. Arbuscular mycorrhizal fungi (AMF) help plants acquire P from soil. Understanding which factors drive AMF-supported nutrient uptake is essential to develop more sustainable agroecosystems. Here we collected soils from 150 cereal fields and 60 non-cropped grassland sites across a 3,000 km trans-European gradient. In a greenhouse experiment, we tested the ability of AMF in these soils to forage for the radioisotope 33P from a hyphal compartment. AMF communities in grassland soils were much more efficient in acquiring 33P and transferred 64% more 33P to plants compared with AMF in cropland soils. Fungicide application best explained hyphal 33P transfer in cropland soils. The use of fungicides and subsequent decline in AMF richness in croplands reduced 33P uptake by 43%. Our results suggest that land-use intensity and fungicide use are major deterrents to the functioning and natural nutrient uptake capacity of AMF in agroecosystems.

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Fig. 1: Experimental set-up using Plantago lanceolata as model plant.
Fig. 2: Comparison of grassland and cropland soils.
Fig. 3: Relative importance of predictors.
Fig. 4: Recovery of 33P in grassland sites.
Fig. 5: Recovery of 33P in cropland sites.

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Data availability

The data that support the findings of this study are available here: https://doi.org/10.6084/m9.figshare.15134328.

Code availability

The code used to analyse the data is available here: https://doi.org/10.6084/m9.figshare.15134670.

References

  1. Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).

    Article  CAS  PubMed  Google Scholar 

  2. Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452 (2016).

    Article  PubMed  Google Scholar 

  4. Tamburini, G. et al. Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv. 6, eaba1715 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Smith, S. & Read, D. Mycorrhizal Symbiosis (Elsevier, 2008).

  6. Soudzilovskaia, N. A. et al. Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob. Ecol. Biogeogr. 24, 371–382 (2015).

    Article  Google Scholar 

  7. 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. Ecol. Lett. 11, 296–310 (2008).

    Article  PubMed  Google Scholar 

  8. Bennett, E. M., Carpenter, S. R. & Caraco, N. F. Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51, 227–234 (2001).

    Article  Google Scholar 

  9. Smith, V. H. & Schindler, D. W. Eutrophication science: where do we go from here? Trends Ecol. Evol. 24, 201–207 (2009).

    Article  PubMed  Google Scholar 

  10. Rillig, M. C. & Mummey, D. L. Mycorrhizas and soil structure. New Phytol. 171, 41–53 (2006).

    Article  CAS  PubMed  Google Scholar 

  11. 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. J. Appl. Ecol. 52, 228–239 (2015).

    Article  CAS  Google Scholar 

  12. Rodriguez, A. & Sanders, I. R. The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J. 9, 1053–1061 (2015).

    Article  PubMed  Google Scholar 

  13. Oviatt, P. & Rillig, M. C. Mycorrhizal technologies for an agriculture of the middle. Plants, People, Planet. https://doi.org/10.1002/ppp3.10177 (2020).

  14. Ryan, M. H. & Graham, J. H. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol. 220, 1092–1107 (2018).

    Article  PubMed  Google Scholar 

  15. Rillig, M. C. et al. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol. 222, 1171–1175 (2019).

    Article  PubMed  Google Scholar 

  16. Zhang, S., Lehmann, A., Zheng, W., You, Z. & Rillig, M. C. Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol. 222, 543–555 (2019).

    Article  CAS  PubMed  Google Scholar 

  17. Thirkell, T. J., Charters, M. D., Elliott, A. J., Sait, S. M. & Field, K. J. Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J. Ecol. 105, 921–929 (2017).

    Article  CAS  Google Scholar 

  18. Davison, J. et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349, 970–973 (2015).

    Article  CAS  PubMed  Google Scholar 

  19. Pringle, A. & Bever, J. D. Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol. 180, 162–175 (2008).

    Article  PubMed  Google Scholar 

  20. Francis, R. & Read, D. J. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can. J. Bot. 73, 1301–1309 (1995).

    Article  Google Scholar 

  21. Thirkell, T. J., Pastok, D. & Field, K. J. Carbon for nutrient exchange between arbuscular mycorrhizal fungi and wheat varies according to cultivar and changes in atmospheric carbon dioxide concentration. Glob. Change Biol. 26, 1725–1738 (2020).

    Article  Google Scholar 

  22. Lehmann, A., Barto, E. K., Powell, J. R. & Rillig, M. C. Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—a meta-analysis on studies from 1981 to 2010. Plant Soil 355, 231–250 (2012).

    Article  CAS  Google Scholar 

  23. Martín-Robles, N. et al. Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species. New Phytol. 218, 322–334 (2018).

    Article  PubMed  Google Scholar 

  24. Leake, J. et al. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82, 1016–1045 (2004).

    Article  Google Scholar 

  25. Oehl, F. et al. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of central Europe. Appl. Environ. Microbiol. 69, 2816–2824 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Xiang, D. et al. Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol. 204, 968–978 (2014).

    Article  CAS  PubMed  Google Scholar 

  27. Bainard, L. D. et al. Plant communities and soil properties mediate agricultural land use impacts on arbuscular mycorrhizal fungi in the Mixed Prairie ecoregion of the North American Great Plains. Agric. Ecosyst. Environ. 249, 187–195 (2017).

    Article  Google Scholar 

  28. Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H. & Young, J. P. W. Ploughing up the wood-wide web? Nature 394, 431–431 (1998).

    Article  CAS  PubMed  Google Scholar 

  29. van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998).

    Article  CAS  Google Scholar 

  30. Vogelsang, K. M., Reynolds, H. L. & Bever, J. D. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol. 172, 554–562 (2006).

    Article  PubMed  Google Scholar 

  31. Scheublin, T. R., Ridgway, K. P., Young, J. P. W. & van der Heijden, M. G. A. Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl. Environ. Microbiol. 70, 6240–6246 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Oehl, F. et al. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol. Biochem. 42, 724–738 (2010).

    Article  CAS  Google Scholar 

  33. De Vries, F. T. et al. Soil food web properties explain ecosystem services across European land use systems. Proc. Natl Acad. Sci. USA 110, 14296–14301 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Verbruggen, E., Xiang, D., Chen, B., Xu, T. & Rillig, M. C. Mycorrhizal fungi associated with high soil N:P ratios are more likely to be lost upon conversion from grasslands to arable agriculture. Soil Biol. Biochem. 86, 1–4 (2015).

    Article  CAS  Google Scholar 

  35. Balami, S., Vašutová, M., Godbold, D., Kotas, P. & Cudlín, P. Soil fungal communities across land use types. iForest 13, 548–558 (2020).

    Article  Google Scholar 

  36. Öpik, M., Mari, M., Liira, J. & Zobel, M. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J. Ecol. 94, 778–790 (2006).

    Article  Google Scholar 

  37. Jansa, J. et al. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12, 225–234 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. van Groenigen, K. J. et al. Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol. Biochem. 42, 48–55 (2010).

    Article  CAS  Google Scholar 

  39. Sallach, J. B., Thirkell, T. J., Field, K. J. & Carter, L. J. The emerging threat of human‐use antifungals in sustainable and circular agriculture schemes. Plants People Planet 3, 685–693 (2021).

    Article  Google Scholar 

  40. Meyer, A. et al. Different land use intensities in grassland ecosystems drive ecology of microbial communities involved in nitrogen turnover in soil. PLoS ONE 8, e73536 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Change Biol. 21, 973–985 (2015).

    Article  Google Scholar 

  42. Tardy, V. et al. Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol. Biochem. 90, 204–213 (2015).

    Article  CAS  Google Scholar 

  43. Sawers, R. J. H. et al. Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol. 214, 632–643 (2017).

    Article  CAS  PubMed  Google Scholar 

  44. Svenningsen, N. B. et al. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 12, 1296–1307 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Schweiger, P. F., Thingstrup, I. & Jakobsen, I. Comparison of two test systems for measuring plant phosphorus uptake via arbuscular mycorrhizal fungi. Mycorrhiza 8, 207–213 (1999).

    Article  CAS  Google Scholar 

  46. Emmett, B. D., Lévesque-Tremblay, V. & Harrison, M. J. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J. 15, 2276–2288 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Jiang, F., Zhang, L., Zhou, J., George, T. S. & Feng, G. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol. 230, 304–315 (2021).

    Article  CAS  PubMed  Google Scholar 

  48. Thonar, C., Schnepf, A., Frossard, E., Roose, T. & Jansa, J. Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339, 231–245 (2011).

    Article  CAS  Google Scholar 

  49. Cavagnaro, T. R., Smith, F. A., Smith, S. E. & Jakobsen, I. Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant Cell Environ. 28, 642–650 (2005).

    Article  CAS  Google Scholar 

  50. Jakobsen, I., Gazey, C. & Abbott, L. K. Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol. 149, 95–103 (2001).

    Article  CAS  PubMed  Google Scholar 

  51. Pearson, J. N. & Jakobsen, I. The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P. New Phytol. 124, 489–494 (1993).

    Article  CAS  Google Scholar 

  52. Nagy, R., Drissner, D., Amrhein, N., Jakobsen, I. & Bucher, M. Erratum: mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol. 184, 1029 (2009).

    Google Scholar 

  53. Smith, S. E., Jakobsen, I., Grønlund, M. & Smith, F. A. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050–1057 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Williams, A., Manoharan, L., Rosenstock, N. P., Olsson, P. A. & Hedlund, K. Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange. New Phytol. 213, 874–885 (2017).

    Article  CAS  PubMed  Google Scholar 

  55. Koerselman, W. & Meuleman, A. F. M. The Vegetation N:P Ratio: a new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 33, 1441 (1996).

    Article  Google Scholar 

  56. Van Aarle, I. M., Olsson, P. A. & Söderström, B. Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol. 155, 173–182 (2002).

    Article  PubMed  Google Scholar 

  57. Staddon, P. L. et al. Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob. Change Biol. 9, 186–194 (2003).

    Article  Google Scholar 

  58. Weber, S. E. et al. Responses of arbuscular mycorrhizal fungi to multiple coinciding global change drivers. Fungal Ecol. 40, 62–71 (2019).

    Article  Google Scholar 

  59. Peat, H. J. & Fitter, A. H. The distribution of arbuscular mycorrhizas in the British flora. New Phytol. 125, 845–854 (1993).

    Article  CAS  PubMed  Google Scholar 

  60. Cruz-Paredes, C. et al. Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils. FEMS Microbiol. Ecol. 95, fiz020 (2019).

    Article  CAS  PubMed  Google Scholar 

  61. Jansa, J., Erb, A., Oberholzer, H.-R., Šmilauer, P. & Egli, S. Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol. Ecol. 23, 2118–2135 (2014).

    Article  CAS  PubMed  Google Scholar 

  62. Davison, J. et al. Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi. New Phytol. 231, 763–776 (2021).

    Article  CAS  PubMed  Google Scholar 

  63. Yang, H. et al. Changes in soil organic carbon, total nitrogen, and abundance of arbuscular mycorrhizal fungi along a large-scale aridity gradient. Catena 87, 70–77 (2011).

    Article  CAS  Google Scholar 

  64. Riedo, J. et al. Widespread occurrence of pesticides in organically managed agricultural soils—the ghost of a conventional agricultural past? Environ. Sci. Technol. https://doi.org/10.1021/acs.est.0c06405 (2021).

  65. Pánková, H., Dostálek, T., Vazačová, K. & Münzbergová, Z. Slow recovery of arbuscular mycorrhizal fungi and plant community after fungicide application: an eight-year experiment. J. Veg. Sci. 29, 695–703 (2018).

    Article  Google Scholar 

  66. Ipsilantis, I., Samourelis, C. & Karpouzas, D. G. The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol. Biochem. https://doi.org/10.1016/j.soilbio.2011.08.007 (2012).

  67. Buysens, C., Dupré de Boulois, H. & Declerck, S. Do fungicides used to control Rhizoctonia solani impact the non-target arbuscular mycorrhizal fungus Rhizophagus irregularis? Mycorrhiza. https://doi.org/10.1007/s00572-014-0610-7 (2015).

  68. Lekberg, Y., Wagner, V., Rummel, A., McLeod, M. & Ramsey, P. W. Strong indirect herbicide effects on mycorrhizal associations through plant community shifts and secondary invasions. Ecol. Appl. 27, 2359–2368 (2017).

    Article  PubMed  Google Scholar 

  69. Hage-Ahmed, K., Rosner, K. & Steinkellner, S. Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manag. Sci. 75, 583–590 (2019).

    Article  CAS  PubMed  Google Scholar 

  70. Kjøller, R. & Rosendahl, S. Effects of fungicides on arbuscular mycorrhizal fungi: differential responses in alkaline phosphatase activity of external and internal hyphae. Biol. Fertil. Soils 31, 361–365 (2000).

    Article  Google Scholar 

  71. Gange, A. C., Brown, V. K. & Sinclair, G. S. Vesicular-arbuscular mycorrhizal fungi: a determinant of plant community structure in early succession. Funct. Ecol. 7, 616 (1993).

    Article  Google Scholar 

  72. Hartnett, D. C. & Wilson, G. W. T. The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244, 319–331 (2002).

    Article  CAS  Google Scholar 

  73. Guzman, A. et al. Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytol. https://doi.org/10.1111/nph.17306 (2021).

  74. LUCAS 2018 Technical Reference Document C3 Classification (Land Cover and Land Use) (Eurostat, 2018).

  75. Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).

    Article  Google Scholar 

  76. Trabucco, A. & Zomer, R. Global Aridity Index and Potential Evapotranspiration (ET0) Climate Database v.2. figshare https://doi.org/10.6084/m9.figshare.7504448.v3 (2019).

  77. García-Palacios, P., Gross, N., Gaitán, J. & Maestre, F. T. Climate mediates the biodiversity-ecosystem stability relationship globally. Proc. Natl Acad. Sci. USA 115, 8400–8405 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Berdugo, M. et al. Global ecosystem thresholds driven by aridity. Science 367, 787–790 (2020).

    Article  CAS  PubMed  Google Scholar 

  79. Sinnott, R. W. Virtues of the Haversine. Sky Telescope 68, 158–159 (1984).

    Google Scholar 

  80. Garland, G. et al. Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems. Nat. Food 2, 28–37 (2021).

    Article  Google Scholar 

  81. Boden‐und Substratuntersuchungen zur Düngeberatung (Schweizerische Referenzmethoden der Eidgenössischen Forschungsanstalten, 1996).

  82. Berry, D., Mahfoudh, K., Ben, Wagner, M. & Loy, A. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol. 77, 7846–7849 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Gardes, M., White, T. J., Fortin, J. A., Bruns, T. D. & Taylor, J. W. Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA. Can. J. Bot. 69, 180–190 (1991).

    Article  CAS  Google Scholar 

  84. Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993).

    Article  CAS  PubMed  Google Scholar 

  85. Fiore-Donno, A. M. et al. New barcoded primers for efficient retrieval of cercozoan sequences in high-throughput environmental diversity surveys, with emphasis on worldwide biological soil crusts. Mol. Ecol. Resour. 18, 229–239 (2018).

    Article  CAS  PubMed  Google Scholar 

  86. Helfenstein, J., Jegminat, J., McLaren, T. I. & Frossard, E. Soil solution phosphorus turnover: derivation, interpretation, and insights from a global compilation of isotope exchange kinetic studies. Biogeosciences 15, 105–114 (2018).

    Article  CAS  Google Scholar 

  87. Thirkell, T. J. et al. Cultivar‐dependent increases in mycorrhizal nutrient acquisition by barley in response to elevated CO2. Plants People Planet 3, 553–566 (2021).

    Article  Google Scholar 

  88. Rodushkin, I., Ruth, T. & Huhtasaari, Å. Comparison of two digestion methods for elemental determinations in plant material by ICP techniques. Anal. Chim. Acta 378, 191–200 (1999).

    Article  CAS  Google Scholar 

  89. Ohno, T. & Zibilske, L. M. Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55, 892–895 (1991).

    Article  CAS  Google Scholar 

  90. Frossard, E. et al. in Phosphorus in Action (eds Bünemann, E. et al.) 59–91 (Springer, 2011).

  91. Sato, K., Suyama, Y., Saito, M. & Sugawara, K. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl. Sci. 51, 179–181 (2005).

    Article  CAS  Google Scholar 

  92. Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Öpik, M. et al. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol. 188, 223–241 (2010).

    Article  PubMed  CAS  Google Scholar 

  95. Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. R Core team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  99. Calcagno, V. glmulti: Model Selection and Multimodel Inference Made Easy. R version 1.0.8 https://CRAN.R-project.org/package=glmulti (2020).

  100. Cade, B. S. Model averaging and muddled multimodel inferences. Ecology. https://doi.org/10.1890/14-1639.1 (2015).

  101. Barton, K. MuMIn: Multi-Model Inference. R version 1.43.17 https://CRAN.R-project.org/package=MuMIn (2020).

  102. Burnham, K. P. & Anderson, D. R. (eds) Model Selection and Multimodel Inference (Springer, 2002).

  103. Rosseel, Y. Lavaan: an R package for structural equation modeling. J. Stat. Softw. https://doi.org/10.18637/jss.v048.i02 (2012).

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Acknowledgements

We thank all the farmers and farm managers for allowing us to sample their fields and for completing our detailed questionnaires. We also thank A. Bonvicini, L. Schönholzer, M. Macsai, F. Tamburini, H. Gamper, S. Müller, D. Bürge, M. Zuber, S. Zhao, V. Somerville, A. Brugger, O. Scholz, D. Bugmann, R. Heiz, B. Seitz and M. Roser for help with field work, the design and execution of the greenhouse experiment and lab analyses. We also thank J. Helfenstein and the anonymous reviewers for valuable feedback on the manuscript. The Digging Deeper project was funded through the 2015–2016 BiodivERsA COFUND call for research proposals, with the national funders Swiss National Science Foundation (grant 31BD30-172466), Deutsche Forschungsgemeinschaft (317895346), Swedish Research Council Formas (contract 2016-0194), Ministerio de Economía y Competitividad (Digging_Deeper, Ref. PCIN-2016-028) and Agence Nationale de la Recherche (ANR, France; grant ANR-16-EBI3-0004-01).

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Authors and Affiliations

  1. Agroscope, Division of Agroecology and Environment, Plant-Soil Interactions Group, Zürich, Switzerland

    Anna Edlinger, Gina Garland, Kyle Hartman, Alain Valzano-Held, Chantal Herzog, Elena Kost & Marcel G. A. van der Heijden

  2. Department of Plant and Microbial Biology, University of Zürich, Zürich, Switzerland

    Anna Edlinger, Chantal Herzog & Marcel G. A. van der Heijden

  3. Department of Microbiological Sciences, North Dakota State University, Fargo, ND, USA

    Samiran Banerjee

  4. Freie Universität Berlin, Institute of Biology, Berlin, Germany

    Florine Degrune & Matthias C. Rillig

  5. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Berlin, Germany

    Florine Degrune & Matthias C. Rillig

  6. Soil Science and Environment Group, Changins, University of Applied Sciences and Arts Western Switzerland, Nyon, Switzerland

    Florine Degrune

  7. Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, Madrid, Spain

    Pablo García-Palacios

  8. Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden

    Sara Hallin & Aurélien Saghaï

  9. Institute of Microbiology, Czech Academy of Sciences, Prague, Czech Republic

    Jan Jansa

  10. Instituto Multidisciplinar para el Estudio del Medio ‘Ramón Margalef’, Universidad de Alicante, Alicante, Spain

    Fernando T. Maestre

  11. Departamento de Ecología, Universidad de Alicante, Alicante, Spain

    Fernando T. Maestre

  12. Departamento de Farmacología, Farmacognosia y Botánica, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid, Spain

    David Sánchez Pescador

  13. Departamento de Biología y Geología, Física y Química Inorgánica, Universidad Rey Juan Carlos, Móstoles, Madrid, Spain

    David Sánchez Pescador

  14. Department of Agroecology, University Bourgogne Franche Comte, INRAE, AgroSup Dijon, Dijon, France

    Laurent Philippot, Sana Romdhane & Ayme Spor

  15. ETH Zürich, Institute of Agricultural Sciences, Group of Plant Nutrition, Lindau, Switzerland

    Emmanuel Frossard

Authors
  1. Anna Edlinger
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  2. Gina Garland
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  3. Kyle Hartman
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  4. Samiran Banerjee
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  5. Florine Degrune
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  6. Pablo García-Palacios
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  7. Sara Hallin
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  8. Alain Valzano-Held
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  9. Chantal Herzog
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  10. Jan Jansa
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  11. Elena Kost
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  12. Fernando T. Maestre
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  13. David Sánchez Pescador
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  14. Laurent Philippot
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  15. Matthias C. Rillig
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  16. Sana Romdhane
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  17. Aurélien Saghaï
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  18. Ayme Spor
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  19. Emmanuel Frossard
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  20. Marcel G. A. van der Heijden
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Contributions

M.G.A.v.d.H., S.H., F.T.M., L.P. and M.C.R. designed the study and obtained research funding. A.E., G.G., K.H., S.B., A.V.-H., C.H., E.K., D.S.P., S.R., A. Saghaï, F.D., P.G.-P. and A. Spor contributed to data collection and analysis. J.J. and E.F. supported the design and execution of the greenhouse experiment. A.E. conducted data analysis. A.E., G.G., M.G.A.v.d.H. and J.J. were involved in the interpretation of results. A.E., G.G. and M.G.A.v.d.H. drafted the manuscript with significant contributions to the writing from all co-authors. All authors commented on and approved the final manuscript.

Corresponding author

Correspondence to Marcel G. A. van der Heijden.

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Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Minxia Liang, Katie Field and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Sampling locations of the grassland and cropland soils in Europe.

Grassland sites comprised both extensively used grasslands in the vicinity of sampled croplands, as well as marginal land (field strips next to the croplands).

Extended Data Fig. 2 Relationship between the soil microbial biomass carbon (a), AMF richness associated with plant roots (b), and soil available P (c) with the 33P recovery in grassland (green) and cropland soils (orange).

Asterisks indicate a significant relationship at p < 0.001 (***). The grey polygon marks a confidence level of 0.95. Since eight sites had to be excluded in the estimation of AMF richness, the no. of observation is smaller in B (n = 142).

Extended Data Fig. 3 The relationship between hyphal 33P transfer activity (measured as 33P recovery in the shoots) and the shoot N:P ratio (scale log-transformed) in grassland (a) and cropland soils (b).

The polygons frame the upper and lower confidence level (0.95). Asterisks indicate the significances of the relationships at p < 0.001 (***) and p < 0.05 (*).

Extended Data Fig. 4 Site-specific variation of AMF communities.

Relative abundances of different families of AMF per site in cropland soils (n = 146) and grassland soils (n = 58).

Extended Data Fig. 5 Structural Equation Models demonstrating the drivers of root AMF richness and 33P recovery in grassland (a and b) and cropland (c and d) soils.

Models a and c assume no direct relationship between AMF richness and 33P recovery. In b and d, a unidirectional relationship between AMF richness and 33P recovery was defined. Solid and dashed lines represent positive and negative associations, respectively. Curved lines indicate co-variances. The line width corresponds to the regression coefficient shown next to the respective line. Numbers next to the response variables represent the coefficients of variance. Significances are indicated by ***. **, * (p < 0.001, p < 0.01, p < 0.05) and non-significant relationships are coloured in grey. P-values of the Chi-square parameter for model a, b, c and d were 0.772, 0.772, 0.799 and 0.829 (p-values higher 0.05 indicate significant models).

Supplementary information

Supplementary Information

Supplementary Tables 1–5, Figs. 1–5 and Methods.

Reporting Summary

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Supplementary Tables 6 and 7

Supplementary Tables 6 and 7: correlation matrix showing Spearman’s correlation coefficient between predictors in grassland (Supplementary Table 6) and cropland (Supplementary Table 7) sites. The selected predictors used for the model-selection procedure are marked with an x. Correlation coefficients >0.80 are highlighted in bold. Significant correlations are indicated as *** P < 0.001, ** P < 0.01, * P < 0.05. ‘Location’ refers to the geographic distance from the southwest-most sampling site.

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Edlinger, A., Garland, G., Hartman, K. et al. Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. Nat Ecol Evol 6, 1145–1154 (2022). https://doi.org/10.1038/s41559-022-01799-8

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