Summary: Global agricultural systems are under increasing pressure to deliver sufficient, healthy food for a growing population. Seasonal inputs, including synthetic pesticides and fertilizers, are applied to crops to reduce losses by pathogens, and enhance crop biomass, although their production and application can also incur several economic and environmental penalties. New solutions are therefore urgently required to enhance crop yield whilst reducing dependence on these seasonal inputs. Volatile Organic Compounds (VOCs) produced by soil microorganisms may provide alternative, sustainable solutions, due to their ability to inhibit plant pathogens, induce plant resistance against pathogens and enhance plant growth promotion. This review will highlight recent advances in our understanding of the biological activities of microbial VOCs (mVOCs), providing perspectives on research required to develop them into viable alternatives to current unsustainable seasonal inputs. This can identify potential new avenues for mVOC research and stimulate discussion across the academic community and agri‐business sector.

Agricultural crop productivity relies on the application of chemical pesticides to reduce pest and pathogen damage. However, chemical pesticides also pose a range of ecological, environmental and economic penalties. This includes the development of pesticide resistance by insect pests and pathogens, rendering pesticides less effective. Alternative sustainable crop protection tools should therefore be considered. Semiochemicals are signalling molecules produced by organisms, including plants, microbes, and animals, which cause behavioural or developmental changes in receiving organisms. Manipulating semiochemicals could provide a more sustainable approach to the management of insect pests and pathogens across crops. Here, we review the role of semiochemicals in the interaction between plants, insects and microbes, including examples of how they have been applied to agricultural systems. We highlight future research priorities to be considered for semiochemicals to be credible alternatives to the application of chemical pesticides.

Entomopathogenic fungi can adopt an endophytic lifestyle and provide protection against insect herbivores and plant pathogens. So far, most studies have focused onBeauveria bassianato increase plant resistance against abiotic and biotic stresses, while only little is known for other entomopathogenic fungi. In this study, we investigated whether root inoculation of sweet pepper (Capsicum annuumL.) by the entomopathogenic fungiAkanthomyces muscariusARSEF 5128 andB.bassianaARSEF 3097 can improve resistance against the tobacco peach aphidMyzus persicaevar.nicotianae. First, dual-choice experiments were performed to test the hypothesis that the fungi deter aphids via modifying plant volatile profiles. Next, we tested the hypothesis that endophytic colonization negatively affects aphid life history traits, such as fecundity, development and mortality rate. Aphids were significantly attracted to the odor of plants inoculated withA.muscariusover non-inoculated plants. Plants inoculated withA.muscariusemitted significantly higher amounts of β-pinene than non-inoculated plants, and significantly higher amounts of indole thanB.bassiana-inoculated and non-inoculated plants. Inoculation with the fungal strains also caused significantly higher emission of terpinolene. Further, both aphid longevity and fecundity were significantly reduced by 18% and 10%, respectively, when feeding on plants inoculated withA.muscarius, although intrinsic rate of population increase did not differ between inoculated and non-inoculated plants. Sweet pepper plants inoculated withB.bassianaARSEF 3097 did not elicit a significant behavioral response nor affected the investigated life history traits. We conclude that endophytic colonization by entomopathogenic fungi has the potential to alter olfactory behavior and performance ofM.persicaevar.nicotianae, but effects are small and depend on the fungal strain used.

The use of beneficial soil fungi or their natural products offers a more sustainable alternative to synthetic fungicides for pathogen management in crops. Volatile organic compounds (VOCs) produced by such fungi act as semiochemicals that inhibit pathogens, with VOC production influenced by physical interactions between competing fungi. This study explores the interaction between the beneficial soil fungus Trichoderma hamatum GD12 strain (GD12), previously shown to antagonise crop pathogens such as Sclerotinia sclerotiorum , to test the hypothesis that its antagonistic effect is mediated by volatile chemical signalling. In dual‐culture confrontation assays, co‐inoculation of GD12 and S. sclerotiorum led to fungistatic interactions after 7 days. VOCs collected from individual and co‐cultures were analysed by gas chromatography–flame ionisation detector (GC‐FID) analysis and coupled GC‐mass spectrometry (GC–MS), revealing significant differences in VOC production between treatments, with VOC production notably upregulated in the GD12 + S. sclerotiorum co‐culture. Peak VOC production occurred 17 days post‐inoculation. Synthetic VOC assays revealed several compounds inhibitory to S. sclerotiorum , including 1‐octen‐3‐one, which also arrested the growth of other fungal crop pathogens ( Botrytis cinerea , Pyrenopeziza brassicae , and Gaeumannomyces tritici ). Structural insights into 1‐octen‐3‐one's antifungal activity against S. sclerotiorum are also presented. These findings support the hypothesis that the antagonistic properties of T. hamatum GD12 against crop fungal pathogens can, in part, be attributed to VOC production. Further research is needed to assess the potential of these semiochemicals as tools for pathogen management in agriculture.