Insight into the truffle brûlé: tripartite interactions between the black truffle (Tuber melanosporum), holm oak (Quercus ilex) and arbuscular mycorrhizal plants

Abstract

Tuber melanosporum is an ectomycorrhizal (ECM) fungus from Mediterranean transitory ecosystems where ECM trees start to dominate among arbuscular-mycorrhizal (AM) shrubs and herbs (companion plants). Its presence entails the development of 'brûlés', where 2 vegetation is scarce for unknown reasons. Current T. melanosporum production comes from plantations where management often suppresses the understory vegetation, although empirical knowledge advocates a positive role of some companion plants in truffle production. This study aimed at (i) experimentally testing the reciprocal interaction between T. melanosporum and companion plants and (ii) examining T. melanosporum-mediated soil feedback involved in the dynamics of truffle ground vegetation. Methods A three-year experiment was set up with Quercus ilex associated with T. melanosporum (or not, as control), grown in association (or not, as control) with a companion plant. Six companion plant species were chosen based on different empirical criteria including those indicated by local truffle growers' knowledge. A trait-based approach was applied to plants and associated fungi (abundance of T. melanosporum and AM fungi mycelium). Results-Conclusion Companion plants promoted the development of truffle mycelium. In the presence of T. melanosporum, companion plant growth and nutrition and AM fungi abundance decreased, while the nutrition status of its host increased. The truffle inhibited germination of weed seeds. These results highlight the role of T. melanosporum in mediating plant-plant interactions, possible mechanisms underlying brûlé formation and a potential successional role for T. melanosporum.

Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum, endophytically colonise roots of non‐ectomycorrhizal plants in natural environments

“…The interactions demonstrated on the co‐culture of ECM trees, non‐ECM plants and T. melanosporum mycelium, reported by Taschen et al . (), support the physiological relevance of the resulting network. This broader view revisits the classical view of ectomycorrhizal networks, and opens these to other ecosystem compartments, if not to other mycorrhizal networks when ECM fungi endophytically colonise orchid, ericoid or arbuscular mycorrhizal plants.…”

“…Reciprocally, Taschen et al . () also document that T. melanosporum develops more efficiently (higher mycelial abundance) in rhizotrons with non‐ECM plants. This questions whether endophytic colonisation provides some resources to the mycelium, ranging from sugar to vitamins.…”

“…Several observations suggest that T. aestivum and T. melanosporum affect plant physiology and development: first, the brûlé phenomenon supports a difficult settlement and/or growth where T. aestivum and T. melanosporum mycelium occurs in natura ; second, rhizotron experiments with or without T. melanosporum (Taschen et al ., ) have documented how non‐ECM plants: (1) germinate less efficiently: and (2) when surviving, have lower leaf N and P in rhizotrons inoculated with T. melanosporum compared with uninoculated ones (Taschen et al ., ). Moreover, the expression of a secreted protein gene (ProtID2632) at a similar level as in ECM root tips supports the possibility to influence host tissue (although its high expression in ascocarps may also point to another role).…”

“…On the one hand, an allelopathic role of inhibitory volatile organic compounds produced by Tuber mycelia could be involved (Pacioni, ; Angelini et al ., ), and T. melanosporum produces ethylene and auxin, which may affect root development (Splivallo et al ., ). Impacts on soil microbiota are also described that can mediate the brûlé effect (Mello et al ., ; Taschen et al ., ). On the other hand, a more direct endophytic interaction in the roots of non‐ECM plants could shape the brûlé.…”

“…Recently, a 3‐yr long rhizotron experiment involving young Quercus ilex trees inoculated (or not) with T. melanosporum and with (or without) non‐ECM plants from six species further supported direct interactions (Taschen et al ., ): T. melanosporum reduced the growth and nutrition of non‐ECM plants, and strongly inhibited germination of weed seeds in the rhizotrons. Interestingly, the presence of non‐ECM plants promoted the development of truffle mycelium in the soil (Taschen et al ., ). Although this work did not investigate the actual colonisation of non‐ECM plants, it suggests that interactions with T. melanosporum may contribute to brûlé formation.…”