Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts

Abstract

Previous studies have shown that vector-borne pathogens can alter the phenotypes of their hosts and vectors in ways that influence the frequency and nature of interactions between them, with significant implications for the transmission and spread of disease. For insect-borne pathogens, host odors are particularly likely targets for manipulation, because both plant- and animal-feeding insects use volatile compounds derived from their hosts as key foraging cues. Here, we document the effects of a widespread plant pathogen, Cucumber mosaic virus (CMV), on the quality and attractiveness of one of its host plants (Cucurbita pepo cv. Dixie) for two aphid vectors, Myzus persicae and Aphis gossypii. Our results indicate that CMV greatly reduces host-plant quality-aphids performed poorly on infected plants and rapidly emigrated from them-but increases the attractiveness of infected plants to aphids by inducing elevated emissions of a plant volatile blend otherwise similar to that emitted by healthy plants. Thus, CMV appears to attract vectors deceptively to infected plants from which they then disperse rapidly, a pattern highly conducive to the nonpersistent transmission mechanism employed by CMV and very different from the pattern previously reported for persistently transmitted viruses that require sustained aphid feeding for transmission. In addition to providing a documented example of a pathogen inducing a deceptive signal of host-plant quality to vectors, our results suggest that the transmission mechanism is a major factor shaping pathogen-induced changes in host-plant phenotypes. Furthermore, our findings yield a general hypothesis that, when vector-borne plant or animal pathogens reduce host quality for vectors, pathogen-induced changes in host phenotypes that enhance vector attraction frequently will involve the exaggeration of existing host-location cues.

Fig. 1.

Study system. (A) Healthy 2-week-old C. pepo cv. Dixie. (B) CMV-infected 2-week-old C. pepo. (C) Winged morph of M. persicae. (D) Winged morphs of A. gossypii. (E) Wingless morph of M. persicae. (F) Wingless morph of A. gossypii. Insets are approximately 3x magnified.

Fig. 2.

Colonization of CMV-infected C. pepo plants in the field by A. gossypii. Means and standard errors are displayed for visual reference only and pertain to populations of A. gossypii that established naturally on plants in field plots. Analysis with the Kruskal-Wallis test indicates that samples from the two treatments differ in mean ranks for census two (H = 14.62, df = 1, P = 0.000) and census three (H = 4.04, df = 1, P = 0.044) (indicated by asterisks on graph). Inset shows the percent of plants that had been colonized by aphids by treatment and census date.

Fig. 3.

Growth of A. gossypii and M. persicae populations on CMV-infected plants. (A) For A. gossypii, data were log transformed to normalize residuals and analyzed by GLM. Letters show significant differences as indicated by Tukey's test. At 7 days, infected vs. mock:, P = 0.000; infected vs. untouched: P = 0.004. At 14 days, infected vs. mock: P = 0.001; infected vs. untouched: P = 0.02. Mock and untouched treatments did not differ at either time point. (B) For M. persicae means and standard errors are displayed for visual reference only (nonparametric statistics were used). Samples from the infected treatment differ in mean ranks relative to both the untouched and mock treatments at 7 days (infected vs. mock: H = 11.94, df = 1, P = 0.001; infected vs. untouched, H = 8.54, df = 1, P = 0.003) and at 14 days (infected vs. mock, H = 7.35, df = 1, P = 0.007; infected vs. untouched: H = 4.92, df = 1, P = 0.027). The mock and untouched treatments did not differ in mean ranks for either time point.

Fig. 4.

Aphid behavioral responses to contact cues of healthy and CMV-infected plants. Fifty aphids were allowed to disperse onto leaves of a healthy (i.e., mock-inoculated) or a CMV-infected release plant and then given the option to emigrate to a neighboring choice plant of the opposite disease status. (A) Fewer aphids were retained on infected release plants than on healthy plants both after 30 min (GLM, data log transformed, df = 1, F = 6.73, P = 0.041) and after 24 h (GLM, df = 1, F = 54.96, P = 0.000). (B) Infected choice plants arrested fewer aphids at 24 h relative to healthy choice plants (GLM, df = 1, F = 32.00, P = 0.001). Four tests were performed for each type of release plant. Asterisks indicate significant differences.

Fig. 5.

Aphid behavioral responses to volatile cues from healthy and CMV-infected plants. In pair-wise choice tests performed separately for wingless and winged morphs of both species, aphids preferred the space below leaves infected with CMV over space below untouched or mock-inoculated leaves. Data were analyzed by GLM and are presented as the mean ± SE and are arranged horizontally by the pairs involved in each choice test. *, P < 0.05 for pair-wise comparisons. (A) For wingless A. gossypii, untouched vs. infected: F = 26.5, P = 0.001; mock vs. infected: F = 9.22, P = 0.009. For winged A. gossypii, untouched vs. infected: F = 6.33, P = 0.025; mock vs. infected: F = 7.36, P = 0.019. (B) For winged M. persicae, untouched vs. infected: F = 5.31, P = 0.043; mock vs. infected: F = 11.467, P = 0.0069. For wingless M. persicae, untouched vs. infected: F = 5.91, P = 0.027; mock vs. infected: F = 3.46, P = 0.08. Untouched and mock-inoculated plants did not differ in attractiveness in any treatment.

Fig. 6.

(A) Total volatile release from healthy and CMV-infected plants in the greenhouse and field. Total volatiles are shown as mean ± SE. For whole-plant collections, treatment n = 8, df = 2, F = 8.13, P = 0.003. Infected plants released significantly more volatiles than controls (infected vs. mock, P = 0.004; infected vs. untouched, P = 0.012; mock vs. untouched, P = 0.89). For individual leaves of plants growing in the field, treatment n = 19. Infected plants released significantly more volatiles than healthy plants (*, P < 0.05, df = 1, F = 5.87, P = 0.012). (B) Individual volatile compounds released by CMV-infected C. pepo. Mean ± SE error for the 20 most abundant compounds consistently released during a 12-h daylight period. The same compounds are present in each treatment, and the relative proportions of compounds released by healthy and infected plants are similar. A, (E)-2-hexenal; B, 6-methyl-5-hepten-2-one; C, (E)-β-ocimene; D, methyl benzoate; E, linalool; F, 4-ethyl-benzaldehyde; G, ethyl-benzaldehyde; H, (Z)-3-hexen-1-yl butyrate; I, (Z)-3-hexen-1-yl 3-methylbutyrate; J, (E)-2-decenal; K, ethyl acetophenone; L, ethyl acetophenone; M, (Z)-3-hexenyl butyrate; N, 3,5-dimethyl-1,2,4-trithiolane; O, tetradecane; P, citronellyl propionate; Q, beta-selinene; R, (Z)-jasmone; S, α-humulene; T, unknown.