Published February 27, 2023 | Version v1
Journal article Open

A soil fungus confers plant resistance against a phytophagous insect by disrupting the symbiotic role of its gut microbiota

  • 1. Department of Agricultural Sciences, University of Naples Federico II, Naples, Italy.
  • 2. Department of Agricultural and Environmental Sciences, University of Milan, 20133 Milano, Italy
  • 3. Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy
  • 4. Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy
  • 5. Department of Biosciences, University of Milan, 20133 Milano, Italy
  • 6. Italian National Agency for New Technologies, Energy, and Sustainable Development, 00196 Roma, Italy
  • 7. Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples Federico II, 80055 Portici, Italy
  • 8. Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples Federico II, 80055 Portici, Italy Department of Pharmacy, University of Naples Federico II, 80131 Napoli, Italy
  • 9. Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples Federico II, 80055 Portici, Italy
  • 10. Department of Biosciences, University of Milan, 20133 Milano, Italy Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples Federico II, 80055 Portici, Italy
  • 11. Department of Agricultural Sciences, University of Naples Federico II, Naples, Italy. ; Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples Federico II, 80055 Portici, Italy

Description

Plants generate energy flows through natural food webs, driven by competition for resources among organisms, which are part of a complex network of multitrophic interactions. Here, we demonstrate that the interaction between tomato plants and a phytophagous insect is driven by a hidden interplay between their respective microbiotas. Tomato plants colonized by the soil fungus Trichoderma afroharzianum, a beneficial microorganism widely used in agriculture as a biocontrol agent, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the larval gut microbiota and its nutritional support to the host. Indeed, experiments aimed to restore the functional microbial community in the gut allow a complete rescue. Our results shed light on a novel role played by a soil microorganism in the modulation of plant–insect interaction, setting the stage for a more comprehensive analysis of the impact that biocontrol agents may have on ecological sustainability of agricultural systems.

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Funding

European Commission
EcoStack – Stacking of ecosystem services: mechanisms and interactions for optimal crop protection, pollination enhancement, and productivity 773554