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.

Colonization by Phloem-Feeding Herbivore Overrides Effects of Plant Virus on Amino Acid Composition in Phloem of Chili Plants.

The 'adaptive host manipulation' hypothesis predicts that parasites can enhance their transmission rates via manipulation of their host's phenotype. For example, many plant pathogens alter the nutritional quality of their host for herbivores that serve as their vectors. However, herbivores, including non-vectors, might cause additional alterations in the plant phenotype. Here, we studied changes in the amino acid (AA) content in the phloem of chilli (Capsicum annuum) plants infected with Pepper golden mosaic virus (PepGMV) upon subsequent colonization with a non-vector, the phloem-feeding whitefly (Trialeurodes vaporariorum). Virus infection alone caused an almost 30-fold increase in overall phloem AAs, but colonization by T. vaporariorum completely reversed this effect. At the level of individual AAs, contents of proline, tyrosine, and valine increased, and histidine and alanine decreased in PepGMV -infected as compared to control plants, whereas colonization by T. vaporariorum caused decreased contents of proline, tyrosine, and valine, and increased contents of histidine and alanine. Overall, the colonization by the whitefly had much stronger effects on phloem AA composition than virus infection. We conclude that the phloem composition of a virus-infected host plant can rapidly change upon arrival of an herbivore and that these changes need to be monitored to predict the nutritional quality of the plant in the long run.

Cross-kingdom effects of plant-plant signaling via volatile organic compounds emitted by tomato (Solanum lycopersicum) plants infested by the greenhouse whitefly (Trialeurodes vaporariorum).

Volatile organic compounds (VOCs) emitted from plants in response to insect infestation can function as signals for the attraction of predatory/parasitic insects and/or repulsion of herbivores. VOCs also may play a role in intra- and inter-plant communication. In this work, the kinetics and composition of VOC emissions produced by tomato (Solanum lycopersicum) plants infested with the greenhouse whitefly Trialeurodes vaporariorum was determined within a 14 days period. The VOC emission profiles varied concomitantly with the duration of whitefly infestation. A total of 36 different VOCs were detected during the experiment, 26 of which could be identified: 23 terpenoids, plus decanal, decane, and methyl salicylate (MeSA). Many VOCs were emitted exclusively by infested plants, including MeSA and 10 terpenoids. In general, individual VOC emissions increased as the infestation progressed, particularly at 7 days post-infestation (dpi). Additional tunnel experiments showed that a 3 days exposure to VOC emissions from whitefly-infested plants significantly reduced infection by a biotrophic bacterial pathogen. Infection of VOC-exposed plants induced the expression of a likely tomato homolog of a methyl salicylate esterase gene, which preceded the expression of pathogenesis-related protein genes. This expression pattern correlated with reduced susceptibility in VOC-exposed plants. The observed cross-kingdom effect of plant-plant signaling via VOCs probably represents a generalized defensive response that contributes to increased plant fitness, considering that resistance responses to whiteflies and biotrophic bacterial pathogens in tomato share many common elements.