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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.

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Acknowledgments

AP is grateful to the Deutsche Forschungsgemeinschaft for financial support for research in this area (Po362/20-2).

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Correspondence to Stephanie Werner or Nicole Brinkmann.

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This article does not contain any studies with human participants or animals performed by any of the authors (Dr. S. Werner, Prof. Dr. A. Polle, Dr. N. Brinkmann). This mini review has been read and approved by all authors and informed consent was obtained from all individual participants included in the study.

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The authors declare that they have no conflict of interest.

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Werner, S., Polle, A. & Brinkmann, N. Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Appl Microbiol Biotechnol 100, 8651–8665 (2016). https://doi.org/10.1007/s00253-016-7792-1

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  • DOI: https://doi.org/10.1007/s00253-016-7792-1

Keywords

  • Volatile organic compounds (VOCs)
  • Soil fungi
  • Interactions
  • Plant growth
  • Phytopathogenic fungi and bacteria
  • Soil fauna