Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions

Abstract

Systemic acquired resistance (SAR) is a plant self-defense mechanism against a broad-range of pathogens and insect pests. Among chemical SAR triggers, plant and bacterial volatiles are promising candidates for use in pest management, as these volatiles are highly effective, inexpensive, and can be employed at relatively low concentrations compared with agrochemicals. However, such volatiles have some drawbacks, including the high evaporation rate of these compounds after application in the open field, their negative effects on plant growth, and their inconsistent levels of effectiveness. Here, we demonstrate the effectiveness of volatile organic compound (VOC)-mediated induced resistance against both the bacterial angular leaf spot pathogen, Pseudononas syringae pv. lachrymans, and the sucking insect aphid, Myzus persicae, in the open field. Using the VOCs 3-pentanol and 2-butanone where fruit yields increased gave unexpectedly, a significant increase in the number of ladybird beetles, Coccinella septempunctata, a natural enemy of aphids. The defense-related gene CsLOX was induced by VOC treatment, indicating that triggering the oxylipin pathway in response to the emission of green leaf volatiles can recruit the natural enemy of aphids. These results demonstrate that VOCs may help prevent plant disease and insect damage by eliciting induced resistance, even in open fields.

Figure 1

Induction of systemic resistance by 3-pentanol and 2-butanone against Pseudomonas syringae pv. lachrymans. The severity of symptoms was scored from 0 to 5 as follows: 0, no symptoms; 1, yellowish color; 2, chlorosis only; 3, partial necrosis and chlorosis; 4, necrosis of the inoculated area and expanded chlorosis; and 5, complete necrosis of the inoculated area. Disease severity of cucumber treated with 3-pentanol and 2-butanone was assessed 7 days after infection with P. syringae pv. lachrymans. Water and 0.5 mM benzothiadizole (BTH) were used as negative and positive controls, respectively. Means in columns followed by different letters are significantly different at P = 0.05 according to the LSD test. Error bars indicate the standard error (n = 16).

Figure 2

3-Pentanol and 2-butanone confer induced resistance against aphids in cucumber: a, Nymph number; b, Adult number. Bars represent the mean ± SE (sample size, n = 12 replications per treatment). Means in columns followed by different letters are significantly different at P = 0.05 according to the LSD test.

Figure 3

3-Pentanol and 2-butanone treatments increase the number of ladybird beetles. Bars represent the mean ± SE (sample size, n = 8 replications per treatment). Means in columns followed by different letters are significantly different at P = 0.05 according to the LSD test. The experiment was repeated three times with similar results.

Figure 4

3-Pentanol and 2-butanone do not alter cucumber growth: (a) Shoot length; (b) Internode number; (c) Shoot fresh weight. The growth of 3-pentanol and 2-butanone-treated cucumber plants was assessed at 24 (a), 34 (b), and 52 (c) dps. Water and 1 mM BTH were used as the negative and positive controls, respectively. Bars represent the mean ± SE (sample size, n = 8 replications per treatment). Means in columns followed by different letters are significantly different at P = 0.05 according to the LSD test. Error bars indicate the standard error (n = 8).

Figure 5

Increase in cucumber yield by 3-pentanol and 2-butanone. Fruit weight of 3-pentanol and 2-butanone-treated cucumber plants was assessed at 52 dps. Bars represent the mean ± SE (sample size, n = 8 replications per treatment). Means in columns followed by different letters are significantly different at P = 0.05 according to the LSD test. Error bars indicate the standard error.

Figure 6

Expression of defense-related genes in response to 3-pentanol and 2-butanone. The expression levels of the cucumber resistance genes Peroxidase, LOX1, and ETR1 were assessed by qRT-PCR at 0 and 6 h after Pseudomoans syringae pv. lachrymans challenge in plants pretreated with 3-pentanol or 2-butanone. Bars represent the mean value ± SE (n = 3). The housekeeping gene Actin was used as a control. The experiment was repeated twice with similar results.