Volatile signaling in plant-<i>Metarhizium</i>-insect interactions: Implications for nitrogen cycling.

Abstract

Nitrogen exchange between plants and insects is a major component of ecosystem nitrogen cycling. Endophytic insect pathogenic fungi transfer insect-derived nitrogen to plants through symbiotic associations mediated by fungal mycelia, enabling plants to thrive even after losing nitrogen to insects. However, the mechanisms underlying this process remain unexplored. Here, we show that the widespread endophytic entomopathogen <i>Metarhizium robertsii</i> degrades the common root-derived antifungal compound caulilexin C to produce the volatile 1-methoxyindole. This compound is recognized by the Or74a olfactory receptor in <i><i>Drosophila melanogaster</i></i> larvae and attracts multiple Dipteran species to the plant-<i>Metarhizium</i> consortium. The recruited insects are subsequently infected and consumed, resulting in enhanced insect-derived nitrogen transfer to the plants. This self-reinforcing mechanism strengthens the plant-fungus symbiosis and reveals a pathway contributing to ecosystem nitrogen flux.