Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Abstract

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.

Root volatiles in plant–plant interactions I: High root sesquiterpene release is associated with increased germination and growth of plant neighbours

“…Thus, the positive effect of C. stoebe root VOCs on the receiver plants could either be a direct effect mediated through the impact of the VOCs on the physiology of the seeds and growing plants, or an indirect effect mediated through soil microbial communities (Hu, Robert, et al, ). Of note, C. stoebe VOCs do not only modulate plant performance but can also change root physiology and herbivore resistance, as shown in the companion paper to this study (Huang et al, ). Thus, the effects of C. stoebe VOCs on neighbouring plants are likely multifaceted and may change the interactions of neighbouring plants with other organisms.…”

“…The Geotex fleece of the mesh cages was sufficient to stop roots from growing out of the mesh cages, thus eliminating direct root contact between the plants. Diffusion of C. stoebe VOCs into the airgap was confirmed by SPME (Huang et al, ). Plants for this experiment were grown in a greenhouse (light: 14 hr; temperature: day 16–24°C, night 16–22°C, mean temperature over growth period 20°C; humidity: 30–60°C) in potting soil consisting of five parts “Landerde” (RICOTER, Aarberg, Switzerland), four parts “Floratorf” (Floragard, Oldenburg, Germany), and one part sand (“Capito” 1–4 mm, LANDI Schweiz AG, Dotzigen, Switzerland).…”

“…This work thus sheds light on the genetic basis and ecological consequences of VOC‐mediated plant‐plant interactions below ground. The results of this study also provide a mechanistic basis to determine the impact of C. stoebe root sesquiterpenes on T. officinale and its interaction with M. melolontha larvae (Huang et al, ).…”

Overexpression of the caryophyllene synthase gene GhTPS1 in cotton negatively affects multiple pests while attracting parasitoids

“…In another recent study, it was shown that the volatiles emitted by the roots of spotted knapweed ( Centaurea stoebe ) can promote the growth of Melolontha melolontha (Coleoptera: Melolonthidae) larvae on neighboring Taraxacum officinale plants. In both studies, ( E )‐β‐caryophyllene was among the volatiles that modified the neighbor plant‐herbivore interaction . Another interesting phenomenon is that volatiles emitted from C. stoebe roots, including ( E )‐β‐caryophyllene, also can affect the composition of the sympatric plant community by promoting germination and growth of neighboring plants .…”

“…In both studies, (E)--caryophyllene was among the volatiles that modified the neighbor plant-herbivore interaction. 52,53 Another interesting phenomenon is that volatiles emitted from C. stoebe roots, including (E)--caryophyllene, also can affect the composition of the sympatric plant community by promoting germination and growth of neighboring plants. 54 Hence, volatiles emitted from plants play multiple roles in the interactions among organisms belonging to the same or different trophic levels.…”