Effective distance of volatile cues for plant–plant communication in beech

In response to volatiles emitted from a plant infested by herbivorous arthropods, neighboring undamaged conspecific plants become better defended against herbivores; this is referred to as plant‒plant communication. Although plant‒plant communication occurs in a wide range of plant species, most studies have focused on herbaceous plants. Here, we investigated plant‒plant communication in beech trees in two experimental plantations in 2018 and one plantation in 2019. Approximately 20% of the leaves of a beech tree were clipped in half in the spring seasons of 2018 and 2019 (clipped tree). The damage levels to leaves in the surrounding undamaged beech trees were evaluated 90 days after the clipping (assay trees). In both years, the damage levels decreased with a reduction in the distance from the clipped tree. In 2019, we also recorded the damage levels of trees that were not exposed to volatiles (nonexposed trees) as control trees and found that those that were located <5 m away from clipped trees had significantly less leaf damage than nonexposed trees. By using a gas chromatograph–mass spectrometer, ten and eight volatile compounds were detected in the headspaces of clipped and unclipped leaves, respectively. Among them, the amount of (Z)-3-hexenyl acetate in clipped leaves was significantly higher than that in nonclipped leaves. Our result suggests that green leaf volatiles such as (Z)-3-hexenol and (Z)-3-hexenyl acetate and other volatile organic compounds emitted from clipped trees induced defenses in the neighboring trees within the 5 m radius. The effective distances of plant‒plant communication in trees were discussed from the viewpoint of the arthropod community structure in forest ecosystems

Targeting diamondback moths in greenhouses by attracting specific native parasitoids with herbivory-induced plant volatiles

植物の香りで特定の天敵を誘引し、標的とした害虫の発生抑制に成功 --植物の香りを用いた新しい害虫防除法--. 京都大学プレスリリース. 2020-12-02.We investigated the recruitment of specific parasitoids using a specific blend of synthetic herbivory-induced plant volatiles (HIPVs) as a novel method of pest control in greenhouses. In the Miyama rural area in Kyoto, Japan, diamondback moth (DBM) (Plutella xylostella, Lepidoptera: Plutellidae) larvae are an important pest of cruciferous crops in greenhouses, and Cotesia vestalis (Hymenoptera: Braconidae), a larval parasitoid of DBM, is found in the surrounding areas. Dispensers of HIPVs that attracted C. vestalis and honey feeders were set inside greenhouses (treated greenhouses). The monthly incidence of DBMs in the treated greenhouses was significantly lower than that in the untreated greenhouses over a 2-year period. The monthly incidences of C. vestalis and DBMs were not significantly different in the untreated greenhouses, whereas monthly C. vestalis incidence was significantly higher than monthly DBM incidence in the treated greenhouses. Poisson regression analyses showed that, in both years, a significantly higher number of C. vestalis was recorded in the treated greenhouses than in the untreated greenhouses when the number of DBM adults increased. We concluded that DBMs were suppressed more effectively by C. vestalis in the treated greenhouses than in the untreated greenhouses

Plant Volatiles, Rather than Light, Determine the Nocturnal Behavior of a Caterpillar

Although many organisms show daily rhythms in their activity patterns, the mechanistic causes of these patterns are poorly understood. Here we show that host plant volatiles affect the nocturnal behavior of the caterpillar Mythimna separata. Irrespective of light status, the caterpillars behaved as if they were in the dark when exposed to volatiles emitted from host plants (either uninfested or infested by conspecific larvae) in the dark. Likewise, irrespective of light status, the caterpillars behaved as if they were in the light when exposed to volatiles emitted from plants in the light. Caterpillars apparently utilize plant volatile information to sense their environment and modulate their daily activity patterns, thereby potentially avoiding the threat of parasitism

Host Plant Volatiles and the Sexual Reproduction of the Potato Aphid, Macrosiphum euphorbiae

Abstract: In late summer, heteroecious aphids, such as the potato aphid, Macrosiphum euphorbiae, move from their secondary summer host plants to primary host plants, where the sexual oviparae mate and lay diapausing eggs. We tested the hypothesis that volatiles of the primary host, Rosa rugosa, would attract the gynoparae, the parthenogenetic alate morph that produce oviparae, as well as the alate males foraging for suitable mates. In wind tunnel assays, both gynoparae and males oriented towards and reached rose cuttings significantly more often than other odour sources, including potato, a major secondary host. The response of males was as high to rose cuttings alone as to potato with a calling virgin oviparous female. These findings are discussed within the seasonal ecology of host alternating aphids

The exposure of field-grown maize seedlings to weed volatiles affects their growth and seed quality

Plants exposed to volatiles emitted from artificially damaged conspecific or heterospecific plants exhibit increased resistance to herbivorous insects. Here, we examined whether volatiles from artificially damaged weeds affect maize growth and reproduction. Seven days after germination, maize seedlings were exposed to volatiles emitted by artificially damaged mugwort (Artemisia indica var. maximowiczii) or tall goldenrod (Solidago altissima) plants either separately, or as a mixture of the two, for seven days. Unexposed seedlings were used as controls. Treated and control seedlings were cultivated in an experimental field without any insecticides applied. Plants exposed to either of the three volatile treatments sustained significantly less damage than controls. Additionally, seedlings exposed to either goldenrod or mixed volatiles produced more leaves and tillers than control plants. Furthermore, a significant increase in the number of ears was observed in plants exposed to the volatile mixture. In all treated plants, ear sugar content was significantly higher than that in the controls. Further, we cultivated seedlings that were either exposed to the volatile mixture or unexposed, under the conventional farming method using pesticides. Similar significant differences were observed for sugar content, number of tillers, leaves, damaged leaves, and ears. Laboratory experiments were conducted to further evaluate the mechanisms involved in the improved performance of volatile-treated plants. A significant reduction in the growth of common armyworm (Mythimna separata) larvae was observed when maize plants were exposed to the volatile mixture. This treatment did not affect the amount of jasmonic acid in the seedlings, whereas salicylic acid content increased upon exposure. The characteristic differences in chemical composition of mugwort and goldenrod volatiles were confirmed and, in turn, the volatile mixture differed significantly from the volatiles of either species

Oviposition Experience of Parasitoid Wasps with Nonhost Larvae Affects their Olfactory and Contact-Behavioral Responses toward Host- and Nonhost-Infested Plants

In nature, parasitoid wasps encounter and sometimes show oviposition behavior to nonhost species. However, little is known about the effect of such negative incidences on their subsequent host-searching behavior. We tested this effect in a tritrophic system of maize plants (Zea mays), common armyworms (hosts), tobacco cutworms (nonhosts), and parasitoid wasps, Cotesia kariyai. We used oviposition inexperienced C. kariyai and negative-experienced individuals that had expressed oviposition behavior toward nonhosts on nonhost-infested maize leaves. We first observed the olfactory behavior of C. kariyai to volatiles from host-infested plants or nonhost-infested plants in a wind tunnel. Negative-experienced wasps showed significantly lower rates of taking-off behavior (Step-1), significantly longer duration until landing (Step-2), and lower rates of landing behavior (Step-3) toward nonhost-infested plants than inexperienced wasps. However, the negative-experience did not affect these three steps toward host-infested plants. A negative experience appears to have negatively affected the olfactory responses to nonhost-infested plants. The chemical analyses suggested that the wasps associated (Z)-3-hexenyl acetate, a compound that was emitted more in nonhost-infested plants, with the negative experience, and reduced their response to nonhost-infested plants. Furthermore, we observed that the searching duration of wasps on either nonhost- or host-infested plants (Step-4) was reduced on both plant types after the negative experiences. Therefore, the negative experience in Step-4 would be nonadaptive for wasps on host-infested plants. Our study indicated that the density (i.e., possible encounters) of nonhost species as well as that of host species in the field should be considered when assessing the host-searching behavior of parasitoid wasps

Identification of a tomato UDP-arabinosyltransferase for airborne volatile reception

植物間コミュニケーションの仕組みを解明 --受容した香りを防御物質に変える遺伝子発見--. 京都大学プレスリリース. 2023-02-28.Volatiles from herbivore-infested plants function as a chemical warning of future herbivory for neighboring plants. (Z)-3-Hexenol emitted from tomato plants infested by common cutworms is taken up by uninfested plants and converted to (Z)-3-hexenyl β-vicianoside (HexVic). Here we show that a wild tomato species (Solanum pennellii) shows limited HexVic accumulation compared to a domesticated tomato species (Solanum lycopersicum) after (Z)-3-hexenol exposure. Common cutworms grow better on an introgression line containing an S. pennellii chromosome 11 segment that impairs HexVic accumulation, suggesting that (Z)-3-hexenol diglycosylation is involved in the defense of tomato against herbivory. We finally reveal that HexVic accumulation is genetically associated with a uridine diphosphate-glycosyltransferase (UGT) gene cluster that harbors UGT91R1 on chromosome 11. Biochemical and transgenic analyses of UGT91R1 show that it preferentially catalyzes (Z)-3-hexenyl β-D-glucopyranoside arabinosylation to produce HexVic in planta

The Composite Effect of Transgenic Plant Volatiles for Acquired Immunity to Herbivory Caused by Inter-Plant Communications

A blend of volatile organic compounds (VOCs) emitted from plants induced by herbivory enables the priming of defensive responses in neighboring plants. These effects may provide insights useful for pest control achieved with transgenic-plant-emitted volatiles. We therefore investigated, under both laboratory and greenhouse conditions, the priming of defense responses in plants (lima bean and corn) by exposing them to transgenic-plant-volatiles (VOCos) including (E)-β-ocimene, emitted from transgenic tobacco plants (NtOS2) that were constitutively overexpressing (E)-β-ocimene synthase. When lima bean plants that had previously been placed downwind of NtOS2 in an open-flow tunnel were infested by spider mites, they were more defensive to spider mites and more attractive to predatory mites, in comparison to the infested plants that had been placed downwind of wild-type tobacco plants. This was similarly observed when the NtOS2-downwind maize plants were infested with Mythimna separata larvae, resulting in reduced larval growth and greater attraction of parasitic wasps (Cotesia kariyai). In a greenhouse experiment, we also found that lima bean plants (VOCos-receiver plants) placed near NtOS2 were more attractive when damaged by spider mites, in comparison to the infested plants that had been placed near the wild-type plants. More intriguingly, VOCs emitted from infested VOCos-receiver plants affected their conspecific neighboring plants to prime indirect defenses in response to herbivory. Altogether, these data suggest that transgenic-plant-emitted volatiles can enhance the ability to prime indirect defenses via both plant-plant and plant-plant-plant communications

Differential Metabolisms of Green Leaf Volatiles in Injured and Intact Parts of a Wounded Leaf Meet Distinct Ecophysiological Requirements

Almost all terrestrial plants produce green leaf volatiles (GLVs), consisting of six-carbon (C6) aldehydes, alcohols and their esters, after mechanical wounding. C6 aldehydes deter enemies, but C6 alcohols and esters are rather inert. In this study, we address why the ability to produce various GLVs in wounded plant tissues has been conserved in the plant kingdom. The major product in completely disrupted Arabidopsis leaf tissues was (Z)-3-hexenal, while (Z)-3-hexenol and (Z)-3-hexenyl acetate were the main products formed in the intact parts of partially wounded leaves. 13C-labeled C6 aldehydes placed on the disrupted part of a wounded leaf diffused into neighboring intact tissues and were reduced to C6 alcohols. The reduction of the aldehydes to alcohols was catalyzed by an NADPH-dependent reductase. When NADPH was supplemented to disrupted tissues, C6 aldehydes were reduced to C6 alcohols, indicating that C6 aldehydes accumulated because of insufficient NADPH. When the leaves were exposed to higher doses of C6 aldehydes, however, a substantial fraction of C6 aldehydes persisted in the leaves and damaged them, indicating potential toxicity of C6 aldehydes to the leaf cells. Thus, the production of C6 aldehydes and their differential metabolisms in wounded leaves has dual benefits. In disrupted tissues, C6 aldehydes and their α,β-unsaturated aldehyde derivatives accumulate to deter invaders. In intact cells, the aldehydes are reduced to minimize self-toxicity and allow healthy cells to survive. The metabolism of GLVs is thus efficiently designed to meet ecophysiological requirements of the microenvironments within a wounded leaf

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 herbivore's 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