Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper
- State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, China
- College of Life Sciences, Xinyang Normal University, China
- Laboratory of Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, Switzerland
Figures
Figure 1
The study organisms on a rice plant, the brown planthopper Nilaparvata lugens, the rice-striped stem borer Chilo suppressalis, and the egg parasitoid Anagrus nilaparvatae.
Figure 2
Planthoppers prefer to settle and lay eggs on caterpillar-infested rice plants.
Preferences of BPH when given a choice between uninfested or SSB caterpillar-infested cultivated rice (A) and wild rice (B) plants were evaluated. Wild or cultivated rice plants were individually infested with two 3rd instar SSB caterpillars, and plants without caterpillar damage (uninfested plants) served as control. One day after the caterpillars had been placed on the plants, fifteen mated BPH females were released in the center of the cylindrical tube at equal distance from the two plants, and the number of BPH per plant was recorded for two consecutive days at different time points (1 hr, 2 hr, 4 hr, 8 hr, 12 hr, 24 hr and 48 hr) and the number of BPH eggs on the infested and healthy plants were counted at the end of the experiment. A Wilcoxon’s signed-rank test for mean number of planthoppers and a likelihood ratio test (LR test) applied to a Generalized Linea Model (GLM, Poisson distribution error) for the mean number eggs. Asterisks indicate a significant difference within a choice test (*p<0.05, **p<0.01; N = 18–21).
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Figure 2—source data 1
Number of BPH on caterpillar-infested or uninfested rice plants.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig2-data1-v1.xlsx
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Figure 2—source data 2
Number of BPH eggs laid on caterpillar-infested or uninfested rice plants.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig2-data2-v1.xlsx
Figure 3
Choices of female A. nilaparvatae wasps in a Y-tube olfactometer.
(A) Proportion of females choosing for the odor of BPH-infested plants without or with (one or two) SSB larvae, when offered next to the odor of control (insect-free) plants. (B) Percentage of females choosing for rice plants infested by 10 BPH without or with SSB caterpillars when offered next to the odor of rice plants only infested by 5 BPH. A LR test applied to a GLM (binomial distribution error) was used for the data, and the asterisks with the data points (A) or columns (B) indicate significant deviation from a 50:50 ratio (*p<0.05; **p<0.01; N = 89–102).
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Figure 3—source data 1
Number of female A. nilaparvatae wasps choosing for the odors of differently treated plants.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig3-data1-v1.xlsx
Figure 4
Partial least squares discriminant analysis (PLS-DA) of rice plant volatile compounds.
The rice plants were either uninfested (Control), infested with 10 gravid BPH females for 12 hr (10 BPH), with two 3rd-instar SSB larvae for 12 hr then with 10 gravod BPH females for another 12 hr (2 SSB+10 BPH), with two SSB for 12 hr then with 5 BPH for another 12 hr (2 SSB+5 BPH), or with two SSB for 24 hr (2 SSB). The score plot display the grouping pattern according to the first two components and the ellipse defines the Hotelling’s T2 confidence interval (95%) for the observations.
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Figure 4—source data 1
Volatile compounds released by differently infested rice plants.
Volatile compounds collected from the headspace of control rice plants (Uninfested), plants infested with 10 gravid BPH females for 12 hr (Infested by BPH (10)), plants infested with two 3rd-instar SSB larvae for 12 hr and then 10 gravid BPH females for another 12 hr (Infested by SSB plus BPH (2:10)), plants infested with two SSB larvae for 12 hr and then five gravid BPH females for another 12 hr (Infested by SSB plus BPH (2:5)), and plants infested with two SSB larvae for 24 hr (Infested by SSB (2)). The values represent the mean percentages ± SE of the peak area relative to the peak area of the internal standard (nonyl acetate). Letters following each value in the same row indicate significant differences between rice plant treatments based on one-way ANOVA followed Tukey HSD test (p<0.05) (N = 7–8). Data were fourth-root transformed before analysis.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig4-data1-v1.docx
Figure 5 with 1 supplement
Parasitoid responses to individual herbivore-induced volatile compounds at low (3–180 ng) or high (50 µg) doses.
Response of A. nilaparvatae (Y-tube assay) to selected key rice volatile compounds that were induced by damage of SSB, BPH or both herbivores. The compounds A-G exhibited were repellent at either a low or high dose or both doses, compound H was attractive at a low dose, but repellent at a high dose, whereas compounds I-M were attractive at both dosages. The remaining compounds (N-T) had no effect on the behavior of the parasitoid females at either dose. Columns with asterisks indicated the test volatiles significantly attract or repel the parasitoid (LR test applied to a GLM, binomial distribution error; *p<0.05, **p<0.01) (N = 50–122).
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Figure 5—source data 1
Responses of A. nilaparvatae wasps to individual synthetic volatile compounds.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig5-data1-v1.xlsx
Figure 5—figure supplement 1
The emission pattern of 13 volatile compounds that affect parasitoid behavior.
The amounts of volatile compounds (mean ± SE) released by rice plants that were either uninfested (control), infested with 10 gravid BPH females (10 BPH), with two 3rd-instar SSB larvae plus 10 gravid BPH females (2 SSB+10 BPH), with two SSB larvae plus five gravid BPH females (2 SSB+5 BPH), or only with 2 SSB larvae (2 SSB). The absolute amount for each compound was calculated based on its response factor relative to the internal standard. Data columns marked with different letters in the same group indicate significant differences between rice plant treatments based on one-way ANOVA followed by Tukey HSD test (p<0.05) (N = 7–8).
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Figure 5—figure supplement 1—source data 1
Absolute concentrations of the 13 volatile compounds released by differently infested rice plants.
Based on the above results, the 13 volatile compounds that either attracted or repelled the parasitoid were selected for further experiments. For this, we calculated the absolute quantities of the 13 compounds, using the response factors of synthetic versions of these compounds (Kalambet and Kozmin, 2018). Compared to uninfested plants, rice plants that were infested with BPH only, infested with BPH plus SSB, and plants infested with SSB only, showed a consist increase in the release of most of the 13 compounds, but with considerable ratio differences among the treatments (Figure 5—figure supplement 1).
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig5-figsupp1-data1-v1.xlsx
Figure 6
Response of A. nilaparvatae wasps to synthetic volatile blends.
The synthetic blends contained volatile compounds at ratios equal to those detected in volatile blends emitted by rice plants that had been infested with 10 BPH only, 10 BPH plus 2 SSB larvae, 5 BPH plus 2 BPH larvae, or 2 SSB larvae only. Pure hexane was used as a control. Columns marked with asterisks indicate significant differences (LR test applied to a GLM, binomial distribution error; **p<0.01), and n.s. indicated a non-significant difference (p>0.05) (N = 60).
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Figure 6—source data 1
Concentrations of 13 volatile compounds contained in each synthetic blend.
Volatile compounds were mixed in pure hexane in ratios that correspond to the ratios of compounds detected in the collection of volatiles from insect infested rice plants. The obtained hexane solutions were used to test the responses of female Anagrus nilaparvatae wasps to each synthetic blend.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig6-data1-v1.docx
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Figure 6—source data 2
Choice of A. nilaparvatae wasps between pure hexane (control) and synthetic volatile blends.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig6-data2-v1.xlsx
Figure 7
Parasitization rates of planthopper eggs by A. nilaparvatae in the greenhouse experiments.
(A) Mean numbers of eggs deposited by BPH females on rice plants infested with BPH only or with both BPH and SSB, and (B) rates of parasitization of BPH eggs by A. nilaparvatae on the differently infested plants. LR tests applied to a GLM were conducted for the number of eggs (Poisson distribution error) and for the percentage of parasitized eggs (binomial distribution error). Columns marked with asterisks indicate significant differences (**p<0.01) and n.s. indicated a non-significant difference (p>0.05) (N = 14–15).
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Figure 7—source data 1
Numbers of eggs deposited by BPH females and rates of parasitism of BPH eggs by A. nilaparvatae on the differently infested plants.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig7-data1-v1.xlsx
Figure 8
Parasitism rates of planthopper eggs by A. nilaparvatae in the field cage experiments.
(A) Mean numbers of eggs deposited by BPH on rice plants that were infested with BPH only or with both BPH and SSB, and (B) rates of parasitism of BPH eggs by A. nilaparvatae on the differently infested plants. LR tests applied to a GLM were conducted for the number of eggs (Poisson distribution error) and for the percentage of parasitized eggs (binomial distribution error). Data columns marked with asterisks indicate significant differences (**p<0.01) (N = 5).
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Figure 8—source data 1
Numbers of eggs deposited by BPH females and rates of parasitization of BPH eggs by A. nilaparvatae on the differently infested plants.
- https://cdn.elifesciences.org/articles/55421/elife-55421-fig8-data1-v1.xlsx
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Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper
eLife 9:e55421.
https://doi.org/10.7554/eLife.55421
