Fungal volatile organic compounds: mechanisms involved in their sensing and dynamic communication with plants.

Microbial volatile organic compounds (MVOCs) are mixtures of gas-phase hydrophobic carbon-based molecules produced by microorganisms such as bacteria and fungi. They can act as airborne signals sensed by plants being crucial players in triggering signaling cascades influencing their secondary metabolism, development, and growth. The role of fungal volatile organic compounds (FVOCs) from beneficial or detrimental species to influence the physiology and priming effect of plants has been well studied. However, the plants mechanisms to discern between FVOCs from friend or foe remains significantly understudied. Under this outlook, we present an overview of the VOCs produced by plant-associate fungal species, with a particular focus on the challenges faced in VOCs research: i) understanding how plants could perceive FVOCs, ii) investigating the differential responses of plants to VOCs from beneficial or detrimental fungal strains, and finally, iii) exploring practical aspects related to the collection of VOCs and their eco-friendly application in agriculture.

Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism.

Plants in more than 100 families secrete extrafloral nectar (EFN) to establish food-for-protection mutualisms with ants. Facultative ant-plants secrete EFN as a jasmonic acid (JA)-dependent response to attract generalist ants. In contrast, obligate ant-plants like the Central American "Swollen-Thorn Acacias" are colonized by specialized ants, although an individual host can carry ant colonies from different species that differ in the degree of protection they provide. We hypothesized that hosts that associate simultaneously with various partners should produce rewards in a modular manner to preferentially reward high quality partners. To test this hypothesis, we applied JA to distinct leaves and quantified cell wall invertase activity (CWIN; a regulator of nectar secretion) and EFN secretion by these "local" (i.e., treated) and the "systemic" (i.e., non-treated) leaves of the same branch. Both CWIN activity and EFN secretion increased in local and systemic leaves of the facultative ant-plant Acacia cochliacantha, but only in the local leaves of the obligate ant-plant, A. cornigera. The systemic EFN secretion in A. cochliacantha was associated with an enhanced emission of volatile organic compounds (VOCs). Such VOCs function as "external signals" that control systemic defense responses in diverse plant species. Indeed, the headspace of JA-treated branches of A. cochliacantha induced EFN secretion in both plant species, whereas the headspace of A. cornigera caused no detectable induction effect. Analyses of the headspace using GC-MS identified six VOCs in the headspace of A. cochliacantha that were not emitted by A. cornigera. Among these VOCs, ß-caryophyllene and (cis)-hexenyl isovalerate have already been reported in other plant species to induce defense traits, including EFN secretion. Our observations underline the importance of VOCs as systemic within-plant signals and show that the modular rewarding in A. cornigera is likely to result from a reduced emission of the systemic signal, rather than from a reduced responsiveness to the signal. We suggest that modular rewarding allows hosts to restrict the metabolic investment to specific partners and to efficiently sanction potential exploiters.