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

Danner H, Brown P, Cator EA, Harren FJ, van Dam NM, Cristescu SM - J. Chem. Ecol. (2015)

Bottom Line: There is growing evidence that interactive effects of simultaneous herbivory also occur across the root-shoot interface.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Interaction Ecology, Institute for Water and Wetland Research (IWWR), Radboud University, PO Box 9010, 6500 GL, Nijmegen, The Netherlands.

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.

No MeSH data available.


Related in: MedlinePlus

Time-resolved emission of sulfur-containing compounds from Brassica rapa shoots aboveground (AG, left) and roots belowground (BG, right) infested only with root feeding Delia radicum larvae (green lines plus circles), leaf feeding Pieris brassicae larvae (blue line plus squares) or both (red line plus crosses). Grey lines are undamaged plants. Emission of methanethiol (m/z 49; panel a and d), dimethylsulfide (DMS; m/z 63; panel b and e), and dimethyldisulfide (DMDS; m/z 93; panel c and f) are represented in gas mixing ratios (parts per billion volume) normalized over the dry weight (in gram) of the respective plant organ. Colored bands represent the standard errors (+/− 1 SE, N = 8). Night periods are indicated by grey shading. Different letters indicate the results of the autoregressive time series model (see supplementary Table S1)
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Fig2: Time-resolved emission of sulfur-containing compounds from Brassica rapa shoots aboveground (AG, left) and roots belowground (BG, right) infested only with root feeding Delia radicum larvae (green lines plus circles), leaf feeding Pieris brassicae larvae (blue line plus squares) or both (red line plus crosses). Grey lines are undamaged plants. Emission of methanethiol (m/z 49; panel a and d), dimethylsulfide (DMS; m/z 63; panel b and e), and dimethyldisulfide (DMDS; m/z 93; panel c and f) are represented in gas mixing ratios (parts per billion volume) normalized over the dry weight (in gram) of the respective plant organ. Colored bands represent the standard errors (+/− 1 SE, N = 8). Night periods are indicated by grey shading. Different letters indicate the results of the autoregressive time series model (see supplementary Table S1)

Mentions: Plants infested with both herbivores emitted methanethiol from their shoots in higher quantities than in any other treatment (Fig. 2a, P < 0.01). Methanethiol emissions of shoot-infested plants were induced only slightly and were not statistically different from control plants (P = 0.063). When both herbivores were feeding simultaneously, DMS emissions from the shoots were increased compared to controls and root-infested plants (Fig. 2b, P < 0.05), whereas they were not significantly different from shoot-infested plants. Plants infested only on their shoots still emitted more DMS than controls (Fig. 2b, P < 0.05). The DMDS emissions from double-infested plants were enhanced overall, but did not differ statistically from shoot-induced or root-induced plants (Fig. 2c, P = 0.066 and P = 0.068, respectively). DMDS emissions of control plants were significantly different over the course of the experiment from those of shoot and root-infested plants; at several time points, the emissions of DMDS from controls exceeded that of root or shoot infested plants (Fig. 2c, P < 0.05). Emission of methanol from AG tissues showed a diurnal rhythm in all treatments (Fig. 3a) with maxima during the night. Emissions were highest in double-infested plants, which emitted more methanol than controls and root-infested plants (Fig. 3a, P < 0.01). Additionally, P. brassicae infested plants emitted more methanol than root-infested plants (P < 0.01), but not significantly more than control plants (Fig. 3a, P = 0.074).Fig. 2


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

Danner H, Brown P, Cator EA, Harren FJ, van Dam NM, Cristescu SM - J. Chem. Ecol. (2015)

Time-resolved emission of sulfur-containing compounds from Brassica rapa shoots aboveground (AG, left) and roots belowground (BG, right) infested only with root feeding Delia radicum larvae (green lines plus circles), leaf feeding Pieris brassicae larvae (blue line plus squares) or both (red line plus crosses). Grey lines are undamaged plants. Emission of methanethiol (m/z 49; panel a and d), dimethylsulfide (DMS; m/z 63; panel b and e), and dimethyldisulfide (DMDS; m/z 93; panel c and f) are represented in gas mixing ratios (parts per billion volume) normalized over the dry weight (in gram) of the respective plant organ. Colored bands represent the standard errors (+/− 1 SE, N = 8). Night periods are indicated by grey shading. Different letters indicate the results of the autoregressive time series model (see supplementary Table S1)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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Fig2: Time-resolved emission of sulfur-containing compounds from Brassica rapa shoots aboveground (AG, left) and roots belowground (BG, right) infested only with root feeding Delia radicum larvae (green lines plus circles), leaf feeding Pieris brassicae larvae (blue line plus squares) or both (red line plus crosses). Grey lines are undamaged plants. Emission of methanethiol (m/z 49; panel a and d), dimethylsulfide (DMS; m/z 63; panel b and e), and dimethyldisulfide (DMDS; m/z 93; panel c and f) are represented in gas mixing ratios (parts per billion volume) normalized over the dry weight (in gram) of the respective plant organ. Colored bands represent the standard errors (+/− 1 SE, N = 8). Night periods are indicated by grey shading. Different letters indicate the results of the autoregressive time series model (see supplementary Table S1)
Mentions: Plants infested with both herbivores emitted methanethiol from their shoots in higher quantities than in any other treatment (Fig. 2a, P < 0.01). Methanethiol emissions of shoot-infested plants were induced only slightly and were not statistically different from control plants (P = 0.063). When both herbivores were feeding simultaneously, DMS emissions from the shoots were increased compared to controls and root-infested plants (Fig. 2b, P < 0.05), whereas they were not significantly different from shoot-infested plants. Plants infested only on their shoots still emitted more DMS than controls (Fig. 2b, P < 0.05). The DMDS emissions from double-infested plants were enhanced overall, but did not differ statistically from shoot-induced or root-induced plants (Fig. 2c, P = 0.066 and P = 0.068, respectively). DMDS emissions of control plants were significantly different over the course of the experiment from those of shoot and root-infested plants; at several time points, the emissions of DMDS from controls exceeded that of root or shoot infested plants (Fig. 2c, P < 0.05). Emission of methanol from AG tissues showed a diurnal rhythm in all treatments (Fig. 3a) with maxima during the night. Emissions were highest in double-infested plants, which emitted more methanol than controls and root-infested plants (Fig. 3a, P < 0.01). Additionally, P. brassicae infested plants emitted more methanol than root-infested plants (P < 0.01), but not significantly more than control plants (Fig. 3a, P = 0.074).Fig. 2

Bottom Line: There is growing evidence that interactive effects of simultaneous herbivory also occur across the root-shoot interface.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Interaction Ecology, Institute for Water and Wetland Research (IWWR), Radboud University, PO Box 9010, 6500 GL, Nijmegen, The Netherlands.

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.

No MeSH data available.


Related in: MedlinePlus