Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores

Abstract

Considerable research has examined plant responses to concurrent attack by herbivores and pathogens, but the effects of attack by parasitic plants, another important class of plant-feeding organisms, on plant defenses against other enemies has not been explored. We investigated how attack by the parasitic plant Cuscuta pentagona impacted tomato (Solanum lycopersicum) defenses against the chewing insect beet armyworm (Spodoptera exigua; BAW). In response to insect feeding, C. pentagona-infested (parasitized) tomato plants produced only one-third of the antiherbivore phytohormone jasmonic acid (JA) produced by unparasitized plants. Similarly, parasitized tomato, in contrast to unparasitized plants, failed to emit herbivore-induced volatiles after 3 d of BAW feeding. Although parasitism impaired antiherbivore defenses, BAW growth was slower on parasitized tomato leaves. Vines of C. pentagona did not translocate JA from BAW-infested plants: amounts of JA in parasite vines grown on caterpillar-fed and control plants were similar. Parasitized plants generally contained more salicylic acid (SA), which can inhibit JA in some systems. Parasitized mutant (NahG) tomato plants deficient in SA produced more JA in response to insect feeding than parasitized wild-type plants, further suggesting cross talk between the SA and JA defense signaling pathways. However, JA induction by BAW was still reduced in parasitized compared to unparasitized NahG, implying that other factors must be involved. We found that parasitized plants were capable of producing induced volatiles when experimentally treated with JA, indicating that resource depletion by the parasite does not fully explain the observed attenuation of volatile response to herbivore feeding. Collectively, these findings show that parasitic plants can have important consequences for host plant defense against herbivores.

Figure 1.

Schematic showing a 25-d-old tomato plant with attached C. pentagona as used in this study. Tomato plants were first parasitized by C. pentagona seedlings when 10 d old (attachment point below cotyledons). The parasite vine was allowed to grow for 10 d and to attach again to the petiole of the second expanded leaf of the now-20-d-old tomato. Five days later, the leaf of the parasitized petiole (indicated with arrow) of the 25-d-old plant received caterpillar feeding for volatile collection or phytohormone analysis.

Figure 2.

Time course of changes in JA (A) and SA (B) in unparasitized tomato plants and plants parasitized by C. pentagona in response to BAW feeding. Parasitized and unparasitized plants that did not receive insect feeding served as controls. Note breaks in the x axis (A and B) and the y axis (A). Data show the mean and se of untransformed values from six replicates. Different letters indicate significance differences within each time point (P < 0.05); n.s., no significance between treatments.

Figure 3.

Total volatile production (mean ± se) by unparasitized tomato plants and plants parasitized by C. pentagona on days 1 to 3 of BAW feeding. Parasitized and unparasitized plants that did not receive insect feeding served as controls. Data show untransformed values from six replicates. Different letters indicate significance differences within each day (P < 0.05).

Figure 4.

Amounts (mean ± se) of α-pinene, 2-carene, β-phellandrene, limonene, and one unidentified monoterpene produced by unparasitized tomato plants and plants parasitized by C. pentagona on day 3 of BAW feeding. Parasitized and unparasitized plants that did not receive insect feeding served as controls. These five volatile compounds are induced by BAW feeding on unparasitized plants. Data show untransformed values from six replicates. Different letters indicate significance differences between treatments (P < 0.05).

Figure 5.

Relative growth rate of BAW on unparasitized tomato and tomato parasitized by C. pentagona. Data show means and se of untransformed values from 15 replicates. Different letters indicate significance differences between treatments (P < 0.05).

Figure 6.

Comparison of SA (A) and JA (B) in unparasitized NahG and wild-type tomato plants and plants parasitized by C. pentagona after 24 h of BAW feeding. Data represent means and se of untransformed values from six replicates. *, Significant differences in SA or JA between NahG and wild-type plants within treatments (P < 0.05).

Figure 7.

Total volatile production (means ± se) by unparasitized tomato plants and plants parasitized by C. pentagona on days 1 to 3 after treatment with JA. Data show untransformed values from six replicates. Different uppercase letters indicate significance differences among days for unparasitized plants; lowercase letters indicate significance differences among days for parasitized plants (P < 0.05); P values indicate differences between unparasitized and parasitized plants within days.