Jasmonate-dependent plant defense restricts thrips performance and preference

Abstract

Background: The western flower thrips (Frankliniella occidentalis [Pergande]) is one of the most important insect herbivores of cultivated plants. However, no pesticide provides complete control of this species, and insecticide resistance has emerged around the world. We previously reported the important role of jasmonate (JA) in the plant's immediate response to thrips feeding by using an Arabidopsis leaf disc system. In this study, as the first step toward practical use of JA in thrips control, we analyzed the effect of JA-regulated Arabidopsis defense at the whole plant level on thrips behavior and life cycle at the population level over an extended period. We also studied the effectiveness of JA-regulated plant defense on thrips damage in Chinese cabbage (Brassica rapa subsp. pekinensis).

Results: Thrips oviposited more on Arabidopsis JA-insensitive coi1-1 mutants than on WT plants, and the population density of the following thrips generation increased on coi1-1 mutants. Moreover, thrips preferred coi1-1 mutants more than WT plants. Application of JA to WT plants before thrips attack decreased the thrips population. To analyze these important functions of JA in a brassica crop plant, we analyzed the expression of marker genes for JA response in B. rapa. Thrips feeding induced expression of these marker genes and significantly increased the JA content in B. rapa. Application of JA to B. rapa enhanced plant resistance to thrips, restricted oviposition, and reduced the population density of the following generation.

Conclusion: Our results indicate that the JA-regulated plant defense restricts thrips performance and preference, and plays an important role in the resistance of Arabidopsis and B. rapa to thrips damage.

Figure 1

Function of JA in plant resistance to thrips feeding. Twenty adult females fed on 3-week-old WT plants (left) or coi1-1 mutants (right). Typical plants after 4 weeks of feeding are shown.

Figure 2

Effect of JA-dependent plant resistance on thrips oviposition on leaf discs. One adult female fed per leaf disc of 3-week-old WT plants (A) or coi1-1 mutants (B) for 4 days. Eggs oviposited on leaf discs were stained with trypan blue. Photos show typical leaf discs after staining; some eggs are shown by red arrowheads. (C) Number of eggs per leaf disc (mean ± SD) based on more than 10 independent determinations. Asterisks indicate significant difference (Student's t-test), ***p < 0.001.

Figure 3

Effect of the JA-dependent plant defense on thrips population. (A, B) Twenty adult females fed on 3-week-old WT plants (A) or coi1-1 mutants (B) for 2 weeks. (C-E) Number of adults (C), larvae (D), and pupae (E) after 2 weeks; mean ± SD based on five independent determinations. Asterisks indicate significant differences (Student's t-test), **p < 0.005, ***p < 0.001.

Figure 4

Effect of the JA-dependent plant defense on host plant preference of thrips. (A) Three-week-old WT plants (left) and coi1-1 mutants (right) were grown at each end of a pot. One hundred adult females were collected in a 1-mL tube and laid between the plants. Photo shows plants after 2 days. (B) Number of adult thrips on each plant after 2 days. Mean ± SD based on five independent determinations. Asterisk indicates a significant difference between the two plants, χ² test, ***p < 0.001. The remaining thrips roamed the surroundings were excluded from the statistical analysis.

Figure 5

Effect of JA-induced Arabidopsis defense response on thrips population. Twenty adult females fed on 3-week-old WT plants. Either 50 μM JA or water (control) was applied 2 days before thrips were introduced. After 2 weeks, eggs (A), adults (B), and larvae (C) were counted. Mean ± SD based on five independent determinations. Asterisks indicate significant differences (Student's t-test), *p < 0.05, ***p < 0.001.

Figure 6

Involvement of JA signaling in B. rapa response to thrips feeding. (A-D) Expression of marker genes for JA response in B. rapa was induced by thrips feeding. BrVSP2 (A), BrLOX2 (B), BrAOS (C), and BrAOC2 (D) are brassica counterparts of Arabidopsis marker genes of the JA pathway and JA biosynthesis. Twenty-five adult females fed on five 2-week-old plants per pot. After 0, 1, 2, and 5 days, total RNA was prepared from the plants with (+Feeding) or without (-Feeding) thrips, and first-strand cDNA was synthesized for PCR analysis. The expression level of each gene was normalized to the expression of BrACT2 (control). Mean ± SD based on three replications. (E) Proposed model of the biosynthesis of JA in Arabidopsis. (F) Effect of thrips feeding on the biosynthesis of JA in B. rapa. Ten adult females fed on a 2-week-old plant (+Feeding). A control plant was kept without thrips (-Feeding). At the beginning of the experiment (0 h) and after 1 day from the start of feeding, 1 g of plant tissue was sampled for measurement of endogenous JA (JA + methyl JA). Means ± SD of three independent measurements. Different letters indicate statistically significant differences between treatments (Tukey-Kramer HSD test; p < 0.05).

Figure 7

Effect of JA application on plant resistance to thrips. Twenty adult females fed on 2-week-old B. rapa plants for 10 days. Water (control; A, C) or 50 μM JA (B, D) was applied 1 day before thrips were introduced. (E) Mean ± SD of area of feeding scars based on more than 10 independent determinations. Asterisk indicates significant difference (Student's t-test), **p < 0.005.

Figure 8

Effect of JA-induced B. rapa defense response on thrips population. (A) Water (control) or 10, 100, or 1000 μM JA was applied to 2-week-old B. rapa plants 1 day before thrips were introduced. One adult female fed on each leaf disc for 4 days. Eggs were stained with trypan blue. Mean ± SD of eggs per leaf disc based on 10 independent determinations. Different letters indicate statistically significant differences between treatments (Tukey-Kramer HSD test; p < 0.05). (B, C) Twenty adult females fed on 2-week-old WT plants for 2 weeks. Water (control) or 50 μM JA was applied 1 day before thrips were introduced. After 2 weeks, adults (B) and larvae (C) were counted. Mean ± SD based on five independent determinations. Asterisks indicate significant differences (Student's t-test), *p < 0.05, ***p < 0.001.