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“Ectomycorrhizal exploration type” could be a functional trait explaining the spatial distribution of tree symbiotic fungi as a function of forest humus forms

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Summary

In European forests, most tree species form symbioses with ectomycorrhizal (EM) and arbuscular mycorrhizal (AM) fungi. The EM fungi are classified into different morphological types based on the development and structure of their extraradical mycelium. These structures could be root extensions that help trees to acquire nutrients. However, the relationship between these morphological traits and functions involved in soil nutrient foraging is still under debate.

We described the composition of mycorrhizal fungal communities under 23 tree species in a wide range of climates and humus forms in Europe and investigated the exploratory types of EM fungi. We assessed the response of this tree extended phenotype to humus forms, as an indicator of the functioning and quality of forest soils. We found a significant relationship between the relative proportion of the two broad categories of EM exploration types (short- or long-distance) and the humus form, showing a greater proportion of long-distance types in the least dynamic soils. As past land-use and host tree species are significant factors structuring fungal communities, we showed this relationship was modulated by host trait (gymnosperms versus angiosperms), soil depth and past land use (farmland or forest).

We propose that this potential functional trait of EM fungi be used in future studies to improve predictive models of forest soil functioning and tree adaptation to environmental nutrient conditions.

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Acknowledgements

This study was made possible by a large, continent-scale, field campaign. Therefore, we gratefully acknowledge all the persons involved in fieldwork, samples handling, and laboratory analyses: Rémi Borelle, Coralie Chesseron, Jean-Luc Denou, Céline Gire, Catherine Lambrot, Julien Langrand, Tania Maxwell, Sylvie Milin, Alain Mollier, Arnaud Reichard, and Samir Moutama (France); Yasmin Jaber, Stamatis Rafail Tziaferidis, Giorgos Xanthopoulos, Fani Lyrou (Greece); Kris Ceunen (Belgium); Frank Ashwood, Sue Benham, Chris Reynolds, Liz Richardson, Mark Oram, Tom Pettingale and Andrew Ross (England); Ming Yu and Haifeng Zheng (Denmark); Dorothea Zannantonio (Sweden); Raino Lievonen (Finland). We particularly thank Lucie Bon and Mohamed El-Mazlouzi, who help us at organizing and leading the field missions. We also thank Bruno Ringeval and Lucas Auer for their help at collecting global climate data and at performing statistical analyses. F.K. held a PhD fellowship awarded by the Grand Est Region and the “Agence Nationale de la Recherche” (ANR) as part of the ANR project “CARbon functional Traits and their OptimisatioN” - CARTON - (AAPG2019 CES32). This project was supported by funds obtained from the CARTON project and the ANR as part of the ‘Investissements d’Avenir’ program (ANR-11-LABX-0002-01, Lab of Excellence ARBRE).

Author information

Authors and Affiliations

  1. Université de Lorraine, INRAE, IAM, Nancy, F-54000, France

    Khalfallah F. & Buée M.

  2. INRAE, BEF, Nancy, F-54000, France

    Khalfallah F., Legout A., Zeller B. & Derrien D.

  3. INRAE, ISPA, Bordeaux Sciences Agro, Villenave d’Ornon, F-33140, France

    Bon L., El Mazlouzi M., Bakker M.R., Fanin N. & Augusto L.

  4. INRAE, Site de la Villa Thuret, Antibes, 1353 UEVT, 06600, France

    Bellanger R., Ducatillon C. & Gateble G.

  5. INRAE, Domaine de l’Hermitage, Cestas Pierroton, 0570 UEFP, 33610, France

    Bernier F.

  6. Departement Biowetenschappen en Industriële Technologie, AgroFoodNature HOGENT, Melle, 9090, Belgium

    De Schrijver A.

  7. Forest Research Institute Hellenic Agricultural Organization Dimitra, Vassilika, Thessaloniki, 57006, Greece

    Fotelli M.N. & Spyroglou G.

  8. Department of Forest Ecology and Management, Swedish Univ. of Agricultural Sciences, Umeå, 901-83, Sweden

    Gundale M.J. & Larsson M.

  9. Forest Research, Northern Research Station, Roslin, Midlothian, EH25 9SY, Scotland, UK

    Mason W.L.

  10. Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre (UPSC), Swedish University of Agricultural Sciences, Umeå, 901-83, Sweden

    Nordin A.

  11. Natural Resources Institute Finland (Luke), Latokartanonkaari 9, Helsinki, 00790, Finland

    Smolander A.

  12. Forest Research, Alice Holt, Alice Holt Lodge, Farnham, GU10 4LH, UK

    Vanguelova E.I.

  13. Forest & Nature Lab, Ghent University, Gontrode, Melle, 9090, Belgium

    Verheyen K.

  14. Department of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg C, 1958, Denmark

    Vesterdal L.

  15. IEES, Université Paris Est Créteil, CNRS, INRAE, IRD, Créteil, 94010, 94010, France

    El Mazlouzi M.

Authors
  1. Khalfallah F.
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  2. Bon L.
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  3. El Mazlouzi M.
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  4. Bakker M.R.
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  5. Fanin N.
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  6. Bellanger R.
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  7. Bernier F.
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  8. De Schrijver A.
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  9. Ducatillon C.
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  10. Fotelli M.N.
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  11. Gateble G.
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  12. Gundale M.J.
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  13. Larsson M.
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  14. Legout A.
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  15. Mason W.L.
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  16. Nordin A.
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  17. Smolander A.
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  18. Spyroglou G.
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  19. Vanguelova E.I.
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  20. Verheyen K.
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  21. Vesterdal L.
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  22. Zeller B.
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  23. Augusto L.
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  24. Derrien D.
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  25. Buée M.
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Contributions

L.A. initiated and coordinated the ANR “CARTON” project. He selected the studied common gardens and interacted with the scientists in charge of those sites (M.N.F., G.S., C.D., R.B., G.G., A.L., B.Z., A.D.S., K.V., E.V., B.M., L.V., A.N., M.J.G., M.L., A.S.), who provided data, ensured monitoring, and supported the field campaign (hosting, field work, tools, shipments, etc.). M.B., D.D. and F.K. designed this study, embedded in the CARTON project. F.K. carried out the molecular biology experiments, handled data, and performed data analyses (bioinformatics and statistics). M.B. and F.K. analysed and interpreted the results. M.B. wrote the manuscript with the help of L.A., D.D., N.F., F.K., M.R.B., and all other authors.

Corresponding authors

Correspondence to Augusto L. or Buée M..

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F., K., L., B., M., E.M. et al. “Ectomycorrhizal exploration type” could be a functional trait explaining the spatial distribution of tree symbiotic fungi as a function of forest humus forms. Mycorrhiza (2024). https://doi.org/10.1007/s00572-024-01146-8

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  • DOI: https://doi.org/10.1007/s00572-024-01146-8

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