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.

Keywords: associational effects; belowground herbivory; neighbourhood effects; plant-herbivore interactions; plant-plant interactions; volatile priming.

Figure 1

Sesquiterpene VOCs from Centaurea stoebe diffuse through the rhizosphere. (a) Experimental setup: Taraxacum officinale plants were grown in the vicinity of empty soil compartments (soil), T. officinale plants (TO), or C. stoebe plants (CS), and volatiles were collected in the gap between the plants. (b) The results of a principal component analysis of the volatile organic compound profiles in the gap are shown: The first two axes explained 19.03% and 11.73% of the total variation, respectively. Differences between treatments were visualized by principal component analysis (PCA). Data points represent biological replicates (n = 4). Circles, http://www.baidu.com/link?url=VsyTNqpQEzvCHtnzvlozV5VEDn_x09pEoTLtC-8ztmOJgBf7gzPQ_0GupRIKHUCFqVrM43nFIeQPfrZuok2O8l9-ek_vrQyHdPxTvg5DDpl9kUaCvrmAnUnhdnKGSFnfs, and squares indicate neighbour identities. Typical total‐ion count gas chromatography mass spectrometry chromatograms of volatiles collected from gap between focal and neighbouring plants from 0 to 39 min (c–e) and from 15 to 18 mins (f–h) are shown

Figure 2

Root volatile organic compounds emitted by Centaurea stoebe increase Melolontha melolontha performance on neighbouring plants. (a) Experimental setup: Individual M. melolontha larvae were allowed to feed on Taraxacum officinale plants growing in the vicinity of empty soil compartments (soil), T. officinale (TO), or C. stoebe (CS) for 18 days. (b) Larval performance: Average larval weight gain was calculated as percentage increase in larval weight per day and is shown as mean ± 1 SE (n = 16). Differences between treatments were determined by one‐way ANOVAs followed by post hoc multiple comparisons (different letters indicate P < 0.05, least square mean) [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Root volatile organic compounds emitted by neighbouring plant influence growth and chemistry of Taraxacum officinale. (a) Root biomass, (b) soluble protein, (c) glucose, (d) fructose, (e) sucrose, and (f) taraxinic acid β‐D glucopyranosyl ester (TA‐G) of T. officinale growing in the vicinity of empty soil compartment (soil), T. officinale (TO), or Centaurea stoebe (CS) are shown on the left. The T. officinale plants were not attacked (light grey bars, n = 8) or attacked by Melolontha melolontha larvae (dark grey bars, n = 16). Values are means ± 1 SE. Differences between treatments were determined by two‐way ANOVAs followed by post hoc multiple comparisons (different letters indicate P < 0.05, least square mean). The relationships between larval weight gain and (g) root biomass, (h) soluble protein, (i) glucose, (j) fructose, (k) sucrose, and (l) TA‐G of T. officinale are shown on the right. Circles, http://www.baidu.com/link?url=VsyTNqpQEzvCHtnzvlozV5VEDn_x09pEoTLtC-8ztmOJgBf7gzPQ_0GupRIKHUCFqVrM43nFIeQPfrZuok2O8l9-ek_vrQyHdPxTvg5DDpl9kUaCvrmAnUnhdnKGSFnfs, and squares indicate T. officinale growing in the vicinity of soil, TO, or CS, respectively. Pearson coefficients, and R ² values are shown in the top of the figures. Regression lines and equations are shown for significant correlations

Figure 4

(E)‐β‐caryophyllene contributes to increased Melolontha melolontha growth on neighboring plants. (a) Experimental setup: Taraxacum officinale plants were growing in the vicinity of empty soil compartment (soil) or Centaurea stoebe (CS) and supplemented with or without synthetic (E)‐β‐caryophyllene in the gap. Physiological concentration of (E)‐β‐caryophyllene in gap (b): Control and (E)‐β‐caryophyllene dispensers were put in the gap for 2 days before measurements. Values were mean ± 1 SE (n = 8). Differences between treatments were determined by independent sample t tests. Impact of (E)‐β‐caryophyllene on M. melolontha larval growth (c): The M. melolontha larva was allowed to feed on T. officinale for 18 days. Values were mean ± 1 SE (n = 12). Differences between treatments were determined by one‐way ANOVA followed by post hoc multiple comparisons (different letters indicate P < 0.05, least square mean) [Colour figure can be viewed at http://wileyonlinelibrary.com]