Junji Takabayashi

PLANT STRATEGIES OF MANIPULATING PREDATOR- PREY INTERACTIONS THROUGH ALLELOCHEMICALS: PROSPECTS FOR APPLICATION IN PEST CONTROL

To understand the role of allelochemicals in predator-prey interactions it is not sufficient to study the behavioral responses of predator and prey. One should elucidate the origin of the allelochemicals and be aware that it may be located at another trophic level. These aspects are reviewed for predator-prey interactions in general and illustrated in detail for interactions between predatory mites and herbivorous mites. In the latter system there is behavioral and chemical evidence for the involvement of the host plant in production of volatile allelochemicals upon damage by the herbivores with the consequence of attracting predators. These volatiles not only influence predator behavior, but also prey behavior and even the attractiveness of nearby plants to predators. Herbivorous mites disperse away from places with high concentrations of the volatiles, and undamaged plants attract more predators when previously exposed to volatiles from infested conspecific plants rather than from uninfested plants. The latter phenomenon may well be an example of plant-to-plant communication. The involvement of the host plant is probably not unique to the predator-herbivore-plant system under study. It may well be widespread since it makes sense from an evolutionary point of view. If so, prospects for application in pest control are wide open. These are discussed, and it is concluded that crop protection in the future should include tactics whereby man becomes an ally to plants in their strategies to manipulate predator-prey interactions through allelochemicals.

Herbivory-induced volatiles elicit defence genes in lima bean leaves

In response to herbivore damage, several plant species emit volatiles that attract natural predators of the attacking herbivores. Using spider mites (Tetranychus urticae) and predatory mites (Phytoseiulus persimilis), it has been shown that not only the attacked plant but also neighbouring plants are affected, becoming more attractive to predatory mites and less susceptible to spider mites. The mechanism involved in such interactions, however, remains elusive. Here we show that uninfested lima bean leaves activate five separate defence genes when exposed to volatiles from conspecific leaves infested with T. urticae, but not when exposed to volatiles from artificially wounded leaves. The expression pattern of these genes is similar to that produced by exposure to jasmonic acid. At least three terpenoids in the volatiles are responsible for this gene activation; they are released in response to herbivory but not artificial wounding. Expression of these genes requires calcium influx and protein phosphorylation/dephosphorylation.

Plant—carnivore mutualism through herbivore-induced carnivore attractants

Plants and carnivorous arthropods can interact mutualistically. A recent discovery is that such mutualisms can be mediated by volatile compounds — produced by plants in response to herbivore damage — that attract carnivores. However, after emission of these attractants, the plant has no control over their use. Thus, exploitation of the information may occur, to the detriment of the plant, leading to costs in addition to benefits. Although all plants studied to date become attractive to carnivorous arthropods after damage by herbivores, they do so in different ways and it is important to understand why this is so.

Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions.

In response to herbivory, plants emit specific blends of herbivore-induced plant volatiles (HIPVs). HIPVs mediate sizable arrays of interactions between plants and arthropods, microorganisms, undamaged neighboring plants or undamaged sites within the plant in various ecosystems. HIPV profiles vary according to the plant and herbivore species, and the developmental stages and conditions of the live plants and herbivores. To understand the regulatory mechanisms underling HIPV biosynthesis, the following issues are reviewed here: (i) herbivore-induced formation of plant volatile terpenoids and green leaf volatiles; (ii) initial activation of plant responses by feeding herbivores; and (iii) the downstream network of the signal transduction. To understand the ecological significance of HIPVs, we also review case studies of insect-plant and inter-/intraplant interactions mediated by HIPVs that have been documented in the field and laboratory in recent years.

Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors

Plants may defend themselves against herbivores by enhancing the effectiveness of natural enemies of herbivores. This is termed “indirect defense,” which may be induced by herbivore damage. An important aspect of induced indirect defense is the attraction of the herbivores natural enemies to infested plants by the plant emitting so-called “herbivore-induced synomone” (HIS) in response to herbivore damage. In this paper, we review the role of terpenoids in the induced indirect defense of plants against herbivorous mites. HIS are emitted from both damaged and undamaged areas of infested plants, and the composition of HIS varies among different plant species. The emission of HIS may also vary within a plant species, depending upon: (1) plant cultivar, (2) leaf growth stage, (3) the herbivore species that is attacking, and (4) abiotic conditions (light intensity, time of year, and water stress). Predatory mites cope with this variation of HIS by innate recognition as well as temporary specialization to a certain HIS via learning.

SCREAM/ICE1 and SCREAM2 Specify Three Cell-State Transitional Steps Leading to Arabidopsis Stomatal Differentiation

Differentiation of specialized cell types in multicellular organisms requires orchestrated actions of cell fate determinants. Stomata, valves on the plant epidermis, are formed through a series of differentiation events mediated by three closely related basic-helix-loop-helix proteins: SPEECHLESS (SPCH), MUTE, and FAMA. However, it is not known what mechanism coordinates their actions. Here, we identify two paralogous proteins, SCREAM (SCRM) and SCRM2, which directly interact with and specify the sequential actions of SPCH, MUTE, and FAMA. The gain-of-function mutation in SCRM exhibited constitutive stomatal differentiation in the epidermis. Conversely, successive loss of SCRM and SCRM2 recapitulated the phenotypes of fama, mute, and spch, indicating that SCRM and SCRM2 together determined successive initiation, proliferation, and terminal differentiation of stomatal cell lineages. Our findings identify the core regulatory units of stomatal differentiation and suggest a model strikingly similar to cell-type differentiation in animals. Surprisingly, map-based cloning revealed that SCRM is INDUCER OF CBF EXPRESSION1, a master regulator of freezing tolerance, thus implicating a potential link between the transcriptional regulation of environmental adaptation and development in plants.

Developmental stage of herbivorePseudaletia separata affects production of herbivore-induced synomone by corn plants.

The female parasitic waspCotesia kariyai discriminated between the volatiles of corn leaves infested by younger host larvaePseudaletia separata (first to fourth instar) and uninfested leaves in a Y-tube olfactometer; the wasps were attracted to the infested leaves. In contrast, when corn plants were infested by the later stages (fifth and sixth instar) of the armyworm, the wasps did not distinguish between infested corn leaves and uninfested corn leaves in the olfactometer. Mechanically damaged leaves were no more attractive than undamaged leaves, and host larvae or their feces were not attractive to the parasitoid. Through chemical analysis, the herbivore-induced plant volatiles were identified in the headspace of infested corn leaves. The herbivore-induced volatiles (HIVs) constituted a larger proportion of the headspace of corn leaves infested by early instar armyworms than of corn leaves infested by late instar armyworms. Application of third-instar larval regurgitant onto artificially damaged sites of leaves resulted in emission of parasitoid attractants from the leaf, whereas leaves treated with sixth-instar regurgitant did not. The function of this herbivore-stage related specificity of herbivore-induced synomones is discussed in a tritrophic context.

Variation in composition of predator-attracting allelochemicals emitted by herbivore-infested plants: Relative influence of plant and herbivore

SummaryDuring foraging, natural enemies of herbivores may employ volatile allelochemicals that originate from an interaction of the herbivore and its host plant. The composition of allelochemical blends emitted by herbivore-infested plants is known to be affected by both the herbivore and the plant. Our chemical data add new evidence to the recent notion that the plants are more important than the herbivore in affecting the composition of the volatile blends. Blends emitted by apple leaves infested with spider mites of 2 different species,T. urticae andP. ulmi, differed less in composition (principally quantitative differences for some compounds) than blends emitted by leaves of two apple cultivars infested by the same spider-mite species,T. urticae (many quantitative and a few qualitative differences). Comparison between three plant species — apple, cucumber and Lima bean — reveals even larger differences between volatile blends emitted upon spider-mite damage (many quantitative differences and several qualitative differences).

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.

Plant—Phytoseiid Interactions Mediated by Herbivore-Induced Plant Volatiles: Variation in Production of Cues and in Responses of Predatory Mites

Phytoseiid mites use herbivore-induced plant volatiles in long-range prey-habitat location and are arrested by these volatiles in a prey patch. The responses of predatory mites to these volatiles are considered to be an important factor in the local extermination of prey populations by phytoseiids such as Phytoseiulus persimilis. Prey-induced plant volatiles are highly detectable and can be reliable indicators of prey presence and prey identity. The composition of herbivore-induced plant volatiles depends on plant species and plant cultivar. Moreover, the composition may also vary with the herbivore species that infests a plant. The responses of phytoseiids to prey-induced plant volatiles from a specific plant-herbivore combination are highly variable. Causal factors include starvation, specific hunger, experience, pathogen infestation and the presence of competitors. Investigating variation in the phytoseiids behavioural response in relation to these factors is important for understanding how and why behavioural strategies maximize phytoseiid fitness.