Masayoshi Uefune

Herbivore-specific, density-dependent induction of plant volatiles: Honest or "cry wolf" signals?

Plants release volatile chemicals upon attack by herbivorous arthropods. They do so commonly in a dose-dependent manner: the more herbivores, the more volatiles released. The volatiles attract predatory arthropods and the amount determines the probability of predator response. We show that seedlings of a cabbage variety (Brassica oleracea var. capitata, cv Shikidori) also show such a response to the density of cabbage white (Pieris rapae) larvae and attract more (naive) parasitoids (Cotesia glomerata) when there are more herbivores on the plant. However, when attacked by diamondback moth (Plutella xylostella) larvae, seedlings of the same variety (cv Shikidori) release volatiles, the total amount of which is high and constant and thus independent of caterpillar density, and naive parasitoids (Cotesia vestalis) of diamondback moth larvae fail to discriminate herbivore-rich from herbivore-poor plants. In contrast, seedlings of another cabbage variety of B. oleracea (var. acephala: kale) respond in a dose-dependent manner to the density of diamondback moth larvae and attract more parasitoids when there are more herbivores. Assuming these responses of the cabbage cultivars reflect behaviour of at least some genotypes of wild plants, we provide arguments why the behaviour of kale (B. oleracea var acephala) is best interpreted as an honest signaling strategy and that of cabbage cv Shikidori (B. oleracea var capitata) as a “cry wolf” signaling strategy, implying a conflict of interest between the plant and the enemies of its herbivores: the plant profits from being visited by the herbivores enemies, but the latter would be better off by visiting other plants with more herbivores. If so, evolutionary theory on alarm signaling predicts consequences of major interest to students of plant protection, tritrophic systems and communication alike.

Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense

Significance Plants receive volatile compounds emitted by neighboring plants that are infested by herbivores, and consequently the receiver plants begin to defend against forthcoming herbivory. To date, how plants receive volatiles and, consequently, how they fortify their defenses, is largely unknown. We found that tomato plants absorbed the airborne green leaf alcohol (Z)-3-hexenol emitted by neighboring conspecific plants under attack by herbivores and subsequently converted the alcohol to a glycoside. The glycoside suppressed growth and survival rates of cutworms. The accumulation of glycoside in the receiver plants explained the defense acquired via “smelling” their neighbors. This study showed that the processing of a volatile compound is a mechanism of volatile reception in tomato plants. Plants receive volatile compounds emitted by neighboring plants that are infested by herbivores, and consequently the receiver plants begin to defend against forthcoming herbivory. However, to date, how plants receive volatiles and, consequently, how they fortify their defenses, is largely unknown. In this study, we found that undamaged tomato plants exposed to volatiles emitted by conspecifics infested with common cutworms (exposed plants) became more defensive against the larvae than those exposed to volatiles from uninfested conspecifics (control plants) in a constant airflow system under laboratory conditions. Comprehensive metabolite analyses showed that only the amount of (Z)-3-hexenylvicianoside (HexVic) was higher in exposed than control plants. This compound negatively affected the performance of common cutworms when added to an artificial diet. The aglycon of HexVic, (Z)-3-hexenol, was obtained from neighboring infested plants via the air. The amount of jasmonates (JAs) was not higher in exposed plants, and HexVic biosynthesis was independent of JA signaling. The use of (Z)-3-hexenol from neighboring damaged conspecifics for HexVic biosynthesis in exposed plants was also observed in an experimental field, indicating that (Z)-3-hexenol intake occurred even under fluctuating environmental conditions. Specific use of airborne (Z)-3-hexenol to form HexVic in undamaged tomato plants reveals a previously unidentified mechanism of plant defense.

Intraspecies Variation in the Kanzawa Spider Mite Differentially Affects Induced Defensive Response in Lima Bean Plants

The Kanzawa spider mite, Tetranychus kanzawai, is a polyphagous herbivore that feeds on various plant families, including the Leguminacae. Scars made by the mite on lima bean leaves (Phaseolus lunatus) were classified into two types: white and red. We obtained two strains of mites—“White” and “Red”—by selecting individual mites based on the color of the scars. Damage made by the Red strain induced the expression of genes for both basic chitinase, which was downstream of the jasmonic acid (JA) signaling pathway, and acidic chitinase, which was downstream of the salicylic acid (SA) signaling pathway. White strain mites also induced the expression of the basic chitinase gene in infested leaves but they only slightly induced the acidic chitinase gene. The Red genotype was dominant over the White for the induction of the acidic chitinase gene. The amount of endogenous salicylates in leaves increased significantly when infested by Red strain mites but did not increase when infested by White strain mites. JA and SA are known to be involved in the production of lima bean leaf volatiles induced by T. urticae. The blend of volatiles emitted from leaves infested by the Red strain were qualitatively different from those infested by the White strain, suggesting that the SA and JA signaling pathways are differently involved in the production of lima bean leaf volatiles induced by T. kanzawai of different strains.

Application of synthetic herbivore‐induced plant volatiles causes increased parasitism of herbivores in the field

We previously reported that Cotesia vestalis (Hymenoptera, Braconidae), a parasitoid of diamondback moth (DBM) (Plutella xylostella; Lepidoptera, Plutellidae) larvae, was attracted to volatiles from crucifer plants infested by moth larvae kept in a desktop acrylic box, and that a blend of four DBM‐induced plant volatiles was responsible for this attraction. In this study, using a specially designed dispenser to release the four compounds, we demonstrated that the wasp was attracted to intact komatsuna plants (Brassica rapa var. perviridis). The experiments were performed in a climate‐controlled room, which was approximately 1000 times larger than the acrylic box used previously. Similarly, using the dispenser in the field, C. vestalis females were attracted to intact komatsuna plants with the dispenser from a distance of three metres. We also examined the effect of the volatile blend on the incidence of parasitism of DBM larvae in the field. Three small containers containing DBM‐infested komatsuna plants with dispensers, and three control containers containing only infested plants (control) were arranged in two lines running perpendicular to a komatsuna field in which both DBM larvae and C. vestalis populations were maintained, at distances of 12, 30 and 70u2003m. The results showed that the incidence of DBM parasitism was significantly higher in containers containing dispensers than in the control containers, suggesting that the blend could potentially be applied to DBM control in agroecosystems.

Diamondback moth females oviposit more on plants infested by non-parasitised than by parasitised conspecifics

Abstract 1.u2002When offered a choice, female diamondback moths (Plutella xylostella) oviposited more eggs on plants with non‐parasitised conspecific larvae than on plants with parasitised larvae.

Host-searching responses to herbivory-associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores.

Previous infestation of pea aphids Acyrthosiphon pisum on broad bean plants resulted in the increased performance of conspecific nymphs on the plants

Abstract We studied the effects of previous infestation of broad bean plants by pea aphids Acyrthosiphon pisum on the performance of conspecific nymphs on the plants and the involvement of jasmonic acid (JA)-related defenses. The time needed for newly emerged nymphs to become reproductive adults on broad bean plants previously infested by conspecifics (pre-infested plants) was significantly shorter than on uninfested (control) broad bean plants. The total numbers of nymphs produced by aphids on preinfested and control plants were not significantly different. Preinfested plants produced significantly less endogenous JA than that control plants did. To test the effect of JA decreases, we conducted experiments on the developmental duration of nymphs on broad bean plants treated with JA (JA-treated plants) before infestation. The time needed for nymphs to become reproductive adults on JA treated preinfested broad bean plants was not significantly different from that on JA-treated control plants. The results suggested a possible parental care by pea aphids: the adult aphids manipulated JA-related defenses in broad bean plants that had positive effects for their offspring.

Herbivore-induced plant volatiles enhance the ability of parasitic wasps to find hosts on a plant

We previously reported that cabbage plants emitted volatiles in response to herbivory by diamondback moth (DBM) larvae and that a cocktail of four induced volatile compounds (n‐heptanal, sabinene, α‐pinene and (Z)‐3‐hexenyl acetate) attracted Cotesia vestalis, a wasp parasitoid of DBM larvae (Shiojiri et al., PLOS ONE, 2010). Here, we describe the behaviour of the wasp in response to exposure to the cocktail and a solvent (control) on crucifer plants (Brassica rapa) with DBM larvae. Wasps showed longer residence and search times on plants with the cocktail than they did on control plants. Further, both wasp–host encounters and oviposition frequencies were significantly higher on plants associated with the cocktail and the rates of parasitism on plants with the cocktail increased due to longer residence and increased searching activity by the parasitoid on the plant. These results indicate that the host‐searching activity of the parasitoid C. vestalis is enhanced on host‐infested plants by the DBM‐induced plant volatiles.

Starvation and herbivore-induced plant volatiles affect the color preferences of parasitic wasps

Using light-emitting diode spotlights, we examined the responses of Cotesia vestalis, a parasitoid of diamondback moth (DBM), Plutella xylostella larvae, with different hunger level to different chromatic cues. Naïve satiated female wasps showed no significant preference for either green, yellow, orange, or red spotlighted areas over a control area with background fluorescent light. When starved for 2xa0h, female wasps preferred yellow and green light over the control area, but not orange or red light. We also tested the effects of DBM-larvae-induced cabbage-plant volatiles, which attract female wasps, on wasp responses to green versus yellow light. In control experiments with no plant volatiles, starved wasps showed no color preference. However, when synthetic volatiles were present, the wasps preferred green over yellow light. We concluded that both hunger level and herbivore-induced plant volatiles were important factors affecting the response of parasitic wasps to light of different color.

Predation-related odours reduce oviposition in a herbivorous mite.

When adult females of the herbivorous mite, Tetranychus urticae, were exposed to the predatory mite, Phytoseiulus persimilis, they laid fewer eggs than females that had not been exposed to P. persimilis when transferred onto a new leaf patch. However, when T. urticae females were exposed to either products of P. persimilis or artificially damaged conspecific eggs on a leaf patch, the number of T. urticae eggs on a new leaf patch did not differ significantly from the control. The reduced oviposition was neither due to the feeding activity on the leaf patch with P. persimilis nor to that on the new leaf patch. There was also no significant difference between the number of T. urticae eggs produced on a new leaf patch following exposure to the odours of a neighbouring leaf patch where there had previously been either P. persimilis or T. urticae adults. However, female T. urticae that had been exposed to odours from neighbouring leaf patches on which both T. urticae and P. persimilis had been placed produced significantly fewer eggs on a new leaf patch than those that had not been exposed to such odours. Neither odours from neighbouring intact leaf patches on which T. urticae eggs were preyed on by P. persimilis, nor odours from a neighbouring Parafilm patch on which T. urticae was preyed on by P. persimilis affected the oviposition of T. urticae. These data suggest that the presence of T. urticae, P. persimilis and a leaf patch are needed for the emission of odours to reduce oviposition in T. urticae.