Volatile organic compounds are secondary metabolites emitted by all organisms, especially by plants and microbes. Their role as aboveground signals has been established for decades. Recent evidence suggests that they might have a non-negligible role belowground and might be involved in root–root and root–microbial/pest interactions. Our aim here was to make a comprehensive review of belowground volatile diversity using a meta-analysis approach. At first we synthesized current literature knowledge on plant root volatiles and classified them in terms of chemical diversity. In a second step, relying on the mVOC database of microbial volatiles, we classified volatiles based on their emitters (bacteria vs. fungi) and their specific ecological niche (i.e., rhizosphere, soil). Our results highlight similarities and differences among root and microbial volatiles and also suggest that some might be niche specific. We further explored the possibility that volatiles might be involved in intra- and inter-specific root–root communication and discuss the ecological implications of such scenario. Overall this work synthesizes current knowledge on the belowground volatilome and the potential signaling role of its constituents. It also highlights that the total diversity of belowground volatiles might be orders of magnitude larger that the few hundreds of compounds described to date.

The plant-growth modulating effect of microbial volatile organic compounds (VOCs) has been demonstrated repeatedly. This has most often been performed by exposing plants to VOC released by microbes grown on nutrient rich media. Here, we used soil instead to grow fungi of the Fusarium genus and investigate how VOCs emitted by this system influenced the development of Arabidopsis plants. The volatile profiles of Fusarium strains grown in soil and malt extract were also compared. Our results demonstrate that distinct volatile signatures can be attributed to different Fusarium genetic clades but also highlight a major influence of the growth medium on volatile emission. Furthermore, all soil-grown Fusarium isolates increased primary root length in Arabidopsis by decreasing VOC concentrations in soil. This result represents a major paradigm shift in plant-microbe interactions since growth modulating effects have been attributed so far to the emission and not the consumption of volatile signals.

Summary Plants and microbes release a plethora of volatiles that act as signals in plant–microbe interactions. Characterizing soil's volatilome and microbiome might shed light on the nature of relevant volatile signals and on their emitters. This hypothesis was tested by characterizing plant cover, soil's volatilome, nutrient content and microbiomes in three grasslands of the Swiss Jura Mountains. The fingerprints of soil's volatiles were generated by solid‐phase micro‐extraction gas chromatography/mass spectrometry, whereas high‐throughput sequencing was used to create a snapshot of soil's microbial communities. A high similarity was observed in plant communities of two out of three sites, which was mirrored by the soil's volatilome. Multiple factor analysis evidenced a strong association among soil's volatilome, plant and microbial communities. The proportion of volatiles correlated to single bacterial and fungal taxa was higher than for plants. This suggests that those organisms might be major contributors to the volatilome of grassland soils. These findings illustrate that key volatiles in grassland soils might be emitted by a handful of organisms that include specific plants and microbes. Further work will be needed to unravel the structure of belowground volatiles and understand their implications for plant health and development.