Kaori Shiojiri

Changing green leaf volatile biosynthesis in plants: An approach for improving plant resistance against both herbivores and pathogens

Green leaf volatiles (GLVs) are commonly emitted by green plants, and their production is drastically enhanced when they are under biotic stress. To clarify the ecological function of naturally emitted GLVs, we studied the response of Arabidopsis, whose GLV biosynthesis had been modified, when subjected to herbivory or a pathogenic infection. There was a significant increase in GLV production after herbivory by cabbage white butterfly larvae and pathogen (gray mold) infection in hydroperoxide lyase (HPL) sense Arabidopsis compared with WT controls. The HPL sense modification resulted in the plant being more attractive to the parasitic wasp Cotesia glomerata, leading to higher mortality of the herbivores. The HPL sense modification also resulted in greater inhibition of growth of the fungus. By contrast, HPL antisense Arabidopsis produced fewer GLVs, attracted fewer parasitoids, and was more susceptible to the pathogens than the WT control. These data show that (i) one of the ecological functions of GLV biosynthesis related to resistance against both herbivores and pathogens, and (ii) the genetic modification of GLV biosynthesis could be a unique approach for improving plant resistance against such biotic stresses.

Infochemically mediated tritrophic interaction webs on cabbage plants

Abstract In response to damage by herbivores, plants are known to emit infochemicals that enhance the effectiveness of insect parasitoids. Studies on plant–parasitoid interactions mediated by such infochemicals have focused on the tritrophic systems in which plants are infested by a single herbivore species. In natural ecosystems, however, plants are often simultaneously infested by several herbivorous species. The present study focuses on two herbivorous species that simultaneously attack crucifer plants and their respective parasitic wasps. We first show the specific responses of the two specialist parasitic wasps [Cotesia plutellae and C. glomerata (Hymenoptera: Braconidae)] to infochemicals originating from cabbage plants (Brassica oleracea cv. Sikidori) infested by each of their respective host larvae [Plutella xylostella (Lepidoptera: Yponomeutidae) and Pieris rapae (Lepidoptera: Pieridae)]. We then coupled the two tritrophic systems on the same cabbage plants. These experiments demonstrated the presence of indirect interactions between the two species of herbivores. Overall, the results indicate the presence of infochemically mediated tritrophic interaction webs on a single plant.

Self-recognition affects plant communication and defense.

Animals have the ability to distinguish self from non-self, which has allowed them to evolve immune systems and, in some instances, to act preferentially towards individuals that are genetically identical or related. Self-recognition is less well known for plants, although recent work indicates that physically connected roots recognize self and reduce competitive interactions. Sagebrush uses volatile cues emitted by clipped branches of self or different neighbours to increase resistance to herbivory. Here, we show that plants that received volatile cues from genetically identical cuttings accumulated less natural damage than plants that received cues from non-self cuttings. Volatile communication is required to coordinate systemic processes such as induced resistance and plants respond more effectively to self than non-self cues. This self/non-self discrimination did not require physical contact and is a necessary first step towards possible kin recognition and kin selection.

Kin recognition affects plant communication and defence

The ability of many animals to recognize kin has allowed them to evolve diverse cooperative behaviours; such ability is less well studied for plants. Many plants, including Artemisia tridentata, have been found to respond to volatile cues emitted by experimentally wounded neighbours to increase levels of resistance to herbivory. We report that this communication was more effective among A. tridentata plants that were more closely related based on microsatellite markers. Plants in the field that received cues from experimentally clipped close relatives experienced less leaf herbivory over the growing season than those that received cues from clipped neighbours that were more distantly related. These results indicate that plants can respond differently to cues from kin, making it less likely that emitters will aid strangers and making it more likely that receivers will respond to cues from relatives. More effective defence adds to a growing list of favourable consequences of kin recognition for plants.

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.

Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks

In response to feeding by phytophagous arthropods, plants emit volatile chemicals. This is shown to be an active physiological response of the plant and the released chemicals are therefore called herbivore-induced plant volatiles (HIPV). One of the supposed functions of HIPV for the plant is to attract carnivorous natural enemies of herbivores. Depending on which plant and herbivore species interact, blends of HIPV show qualitative and quantitative variation. Hence, one may ask whether this allows the natural enemies to discriminate between volatiles from plants infested by herbivore species that are either suitable or unsuitable as a food source for the natural enemy. Another question is whether natural enemies can also recognise HIPV when two or more herbivore species that differ in suitability as a food source simultaneously attack the same plant species. By reviewing the literature we show that arthropod predators and parasitoids can tell different HIPV blends apart in several cases of single plant–single herbivore systems and even in single plant–multiple herbivore systems. Yet, there are also cases where predators and parasitoids do not discriminate or discriminate only after having learned the association between HIPV and herbivores that are either suitable or non-suitable as a source of food. In this case, suitable herbivores may profit from colonising plants that are already infested by another non-suitable herbivore. The resulting temporal or partial refuge may have important population dynamical consequences, as such refuges have been shown to stabilise otherwise unstable predator–prey models of the Lotka-Volterra or Nicholson-Bailey type.

Role of the Lipoxygenase/lyase Pathway of Host-food Plants in the Host Searching Behavior of Two Parasitoid Species, Cotesia glomerata and Cotesia plutellae

To elucidate the role of the plant lipoxygenase (LOX)/lyase pathway for host search behavior of two parasitic wasps attacking herbivorous larvae, an Arabidopsis mutant (all84) was isolated with a mutation somewhere in the LOX/lyase pathway. Detached leaves of the mutant were shown to release less (Z)-3-hexenal, a first green leaf volatile (GLV) product of the LOX/lyase pathway. The braconid larval parasitoids studied, Cotesia glomerata and Cotesia plutella, differ in their ability to discriminate among plant volatiles induced by feeding of lepidopteran hosts and nonhosts: C. plutella only responds to plant volatiles induced by hosts (Plutella larvae), whereas the response by the more generalist C. glomerata is not host specific. The Arabidopsis mutant all84 infested by Pieris larvae was less attractive to C. glomerata than Arabidopsis wild type (wt) infested by the host larvae. C. glomerata was attracted by two of the GLV biosynthesized through the LOX/lyase pathway, (E)-2-hexenal and (Z)-3-hexenyl acetate. However, attraction of C. plutellae to volatiles from Plutella-infested all84 plants did not differ from attraction to host-infested wt Arabidopsis. Both wasp species were arrested to the respective host-infested edge of the wt leaf by showing characteristic antennal searching behavior on the edge. In C. glomerata, the duration of this searching behavior at the infested leaf edge was significantly shorter on all84 plants than on wt plants. By contrast, the duration of the searching behavior of C. plutellae on the host-infested leaf edge of all84 was not significantly different from that on the wt leaf. These data suggest that the LOX/lyase pathway is directly involved in the production of attractants and arrestants important for host search behavior of the more generalist C. glomerata, but not for the specialist C. plutellae.

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.

Deciphering the language of plant communication: volatile chemotypes of sagebrush

Volatile communication between sagebrush (Artemisia tridentata) individuals has been found previously to reduce herbivory and to be more effective between individuals that are genetically identical or related relative to between strangers. The chemical nature of the cues involved in volatile communication remains unknown for this and other systems. We collected headspace volatiles from sagebrush plants in the field and analyzed these using GC-MS. Volatile profiles were highly variable among individuals, but most individuals could be characterized as belonging to one of two chemotypes, dominated by either thujone or camphor. Analyses of parents and offspring revealed that chemotypes were highly heritable. The ecological significance of chemotypes and the genetic mechanisms that control them remain poorly understood. However, we found that individuals of the same chemotype communicated more effectively and experienced less herbivory than individuals of differing chemotypes. Plants may use chemotypes to distinguish relatives from strangers.

Effects of specialist parasitoids on oviposition preference of phytophagous insects : encounter-dilution effects in a tritrophic interaction

Abstract.  1. Host plant preferences of the female diamondback moth Plutella xylostella were studied.