Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms.

Abstract

We reviewed the impact of fungal volatile organic compounds (VOCs) on soil-inhabiting organisms and their physiological and molecular consequences for their targets. Because fungi can only move by growth to distinct directions, a main mechanism to protect themselves from enemies or to manipulate their surroundings is the secretion of exudates or VOCs. The importance of VOCs in this regard has been significantly underestimated. VOCs not only can be means of communication, but also signals that are able to specifically manipulate the recipient. VOCs can reprogram root architecture of symbiotic partner plants or increase plant growth leading to enlarged colonization surfaces. VOCs are also able to enhance plant resistance against pathogens by activating phytohormone-dependent signaling pathways. In some cases, they were phytotoxic. Because the response was specific to distinct species, fungal VOCs may contribute to regulate the competition of plant communities. Additionally, VOCs are used by the producing fungus to attack rivaling fungi or bacteria, thereby protecting the emitter or its nutrient sources. In addition, animals, like springtails, nematodes, and earthworms, which are important components of the soil food web, respond to fungal VOCs. Some VOCs are effective repellents for nematodes and, therefore, have applications as biocontrol agents. In conclusion, this review shows that fungal VOCs have a huge impact on soil fauna and flora, but the underlying mechanisms, how VOCs are perceived by the recipients, how they manipulate their targets and the resulting ecological consequences of VOCs in inter-kingdom signaling is only partly understood. These knowledge gaps are left to be filled by future studies.