Aboveground and Belowground Herbivores Synergistically Induce Volatile Organic Sulfur Compound Emissions from Shoots but Not from Roots

Abstract

Studies on aboveground (AG) plant organs have shown that volatile organic compound (VOC) emissions differ between simultaneous attack by herbivores and single herbivore attack. There is growing evidence that interactive effects of simultaneous herbivory also occur across the root-shoot interface. In our study, Brassica rapa roots were infested with root fly larvae (Delia radicum) and the shoots infested with Pieris brassicae, either singly or simultaneously, to study these root-shoot interactions. As an analytical platform, we used Proton Transfer Reaction Mass Spectrometry (PTR-MS) to investigate VOCs over a 3 day time period. Our set-up allowed us to monitor root and shoot emissions concurrently on the same plant. Focus was placed on the sulfur-containing compounds; methanethiol, dimethylsulfide (DMS), and dimethyldisulfide (DMDS), because these compounds previously have been shown to be biologically active in the interactions of Brassica plants, herbivores, parasitoids, and predators, yet have received relatively little attention. The shoots of plants simultaneously infested with AG and belowground (BG) herbivores emitted higher levels of sulfur-containing compounds than plants with a single herbivore species present. In contrast, the emission of sulfur VOCs from the plant roots increased as a consequence of root herbivory, independent of the presence of an AG herbivore. The onset of root emissions was more rapid after damage than the onset of shoot emissions. The shoots of double infested plants also emitted higher levels of methanol. Thus, interactive effects of root and shoot herbivores exhibit more strongly in the VOC emissions from the shoots than from the roots, implying the involvement of specific signaling interactions.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-015-0601-y) contains supplementary material, which is available to authorized users.

The role of volatiles in plant communication

“…Semiochemicals that function in these interactions can be produced constitutively or in response to outside interactions and stimuli, and this occurs above as well as below ground (Massalha et al ., ). Although there are indications that above‐ and below‐ground semiochemical responses are integrated (Danner et al ., ; Van Dam et al ., ), details on what drives this remain to be elucidated. Although semiochemicals can travel long distances, plant−plant and plant−microbe communication usually take place at relatively short distances, while plant volatiles with a role in plant−insect interaction are perceived at distances of several hundred metres.…”

Root-emitted volatile organic compounds: can they mediate belowground plant-plant interactions?

“…Depending on the plant species studied, volatile blends released belowground by plant roots can be characterized by compounds belonging to various chemical families, particularly terpenoids (Rasmann et al 2005;Lin et al 2007;Ali et al 2010), fatty acid derivatives (Gfeller et al 2013) or sulphur-containing compounds (Ferry et al 2007;Crespo et al 2012;Danner et al 2015). Important ecological roles have been associated with root-emitted VOCs (Fig.…”

“…GC-MS and proton transfer reaction-mass spectrometry (PTR-MS) analyses have shown that insect-damaged Brassica roots release mainly highly volatile sulphur compounds (methanethiol, dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide) and glucosinolate breakdown products (thiocyanates and isothiocyanates) in the soil, with a VOC emission pattern depending on the plant species studied Danner et al 2012;Crespo et al 2012;Danner et al 2015). To date, PTR-MS analyses of root-emitted VOCs have been performed only on potted Brassica spp.…”

“…PTR-MS has been shown to be an efficient tool for the real-time analysis of root-emitted VOCs in situ Danner et al 2012;Crespo et al 2012;Danner et al 2015). The identity of the molecules entering the ionization chamber, however, cannot be determined using the mass spectral data acquired with this technique because only the mass of a small number of product ions (particularly cluster ions) can be obtained .…”

Herbivore‐induced plant volatiles accurately predict history of coexistence, diet breadth, and feeding mode of herbivores

“…On the one hand, there is experimental evidence that the concurrent feeding by aboveground feeding nonhosts does not affect parasitization levels of suitable herbivores in long-term experiments (Chabaane et al, 2015;de Rijk et al, 2016). Root herbivore feeding, however, causes shifts in Brassica HIPV profiles which reduce parasitization rates both in the field and in spatially explicit experiments (Soler et al, 2007a,b;Pierre et al, 2011;Danner et al, 2015). It was postulated that these parasitoids avoid plants with root herbivores because their offspring's performance will be reduced as a result of changes in the plant's metabolome that are trickling up via their herbivorous hosts (Soler et al, 2005;Qiu et al, 2009).…”