Plant-mediated interactions between pathogenic microorganisms and arthropod herbivores occur when arthropod infestation or pathogen infection changes the shared host plant in ways that affect a subsequent attacker of the opposite type. Interest in such "tripartite" interactions has increased as the ecological and plant physiological framework for understanding and contextualizing them has developed. The outcomes of plant-mediated interactions are variable, and only a few provisional patterns can be identified at present. However, these interactions can have important consequences not only for individual pathogens and herbivores, but also for the population dynamics of both types of organisms in managed and natural ecosystems. Research has focused on the role of two plant response pathways in mediating tripartite interactions, one involving jasmonic acid and the other salicylic acid. Further studies of plant-mediated interactions will facilitate an understanding of how plants coordinate and integrate their defenses against multiple biotic threats.
In many plants, defence systems against herbivores are induced through the octadecanoid pathway 1,2 , which may also be involved in recruiting natural enemies of herbivores 3 . This pathway can be induced by treating plants with jasmonic acid 4 or by natural herbivory, and increases resistance against herbivorous insects in tomato plants 5 , in part by causing production of toxic and antinutritive proteinase inhibitors and oxidative enzymes 6-8 . Herbivore-infested tomato plants release increased amounts of volatiles 9 and attract natural enemies of the herbivores 10 , as do other plants [11][12][13][14][15] . The octadecanoid pathway may regulate production of these volatiles, which attract host-seeking parasitic wasps 16,17 . However, plant resistance compounds can adversely affect parasitoids as well as herbivores 18 . It is unclear whether the combination of increased retention and/or attractiveness of parasitic wasps to induced plants and the adverse effects of plant defence compounds on both caterpillars and parasitoids results in a net increase in parasitization of herbivores feeding on induced plants. Here I show that inducing plants with jasmonic acid increases parasitism of caterpillar pests in an agricultural field twofold. Thus, elicitors of plant resistance may become useful in agriculture.In the tomato growing region of the Central Valley of California, I stimulated the octadecanoid pathway by spraying eight-week-old tomato plants (Lycopersicon esculentum var. Ace) with 0.5 mM (circa 1.5 mol per plant) jasmonic acid. One-hundred-and-three plots containing 4-6 plants each were randomly divided into plants treated with jasmonic acid (induced plants) and plants sprayed with water and acetone carrier (control). The number of naturally occurring herbivores on induced plants and control plants was not manipulated.I confirmed that the octadecanoid pathway was induced by measuring polyphenol oxidase activity (a putative defence) in the induced and control plants four days after the plants were sprayed (mean change in optical density per gram per minute Ϯ s:e:; control: 6:739 Ϯ 0:884; induced: 19:839 Ϯ 2:389; analysis of variance: F 1;38 ¼ 26:454, P Ͻ 0:001) (methods in ref. 5). Next I examined the effects of induction on the plant-herbivore-natural enemy interaction in a field with natural infestations of Hyposoter exiguae and Spodoptera exigua. H. exiguae is an endoparasitic wasp and an important killer of the agronomic lepidopteran pest, S. exigua 19 . Three weeks after the field was sprayed, the number of naturally occurring H. exiguae pupae, which had developed in native, naturally occurring S. exigua caterpillars, were counted on one plant in each plot. There were twice as many H. exiguae pupae on induced plants as on controls (Kruskall-Wallis: n ¼ 103, x 2 ¼ 5:12, d:f: ¼ 1, P ¼ 0:024; Fig. 1a).To confirm that plant traits per se were responsible for this increased parasitism, I placed sentinel caterpillars underneath the canopy of jasmonate-induced and control plants in the field. The sentinel S. exig...
Wounding increases the levels and activities of several defense-related proteins in the foliage of the tomato plant,Lycopersicon esculentum Mill. Evidence indicates that two of these responses, the systemic increases in polyphenol oxidase and proteinase inhibitors, are regulated by an octadecanoid-based signalling pathway which includes the wound hormone, jasmonic acid. It is not known whether other responses to wounding are also regulated by this same signalling pathway. In this paper, we show that application of jasmonates (jasmonic acid or its volatile derivative, methyl jasmonate) in low concentrations to foliage of young tomato plants induced, in a dose-dependent manner, the same protein responses-polyphenol oxidase, proteinase inhibitors, lipoxygenase, and peroxidase-as doesHelicoverpa zea Boddie feeding. Application of jasmonic acid to a single leaflet of four-leaf tomato plants induced these four proteins in a spatial pattern nearly identical to that produced by localized feeding ofH. zea. Exogenous jasmonic acid also decreased suitability of foliage for the beet armyworm,Spodoptera exigua Hubner in the laboratory. Based on these results, we conducted an experiment to measure the effects of jasmonic acid spray under field conditions. We provide the first evidence that jasmonic acid spray on field plants induces production of chemical defenses above the levels found in unsprayed controls. Exogenous jasmonic acid sprayed on plants in agricultural plots increased levels of polyphenol oxidase and proteinase inhibitors. Because application of jasmonic acid induces these defensive compounds at low concentrations in a manner similar to natural wounding, it may prove to be a useful tool for stimulating plant resistance to insects in the field.
Plants defend themselves against attack from insects and pathogens with various resistance strategies. The jasmonate and salicylate signaling pathways are two induced responses that protect plants against these attackers. Knowledge of the range of organisms that are affected by each response is important for understanding how plants coordinate their defenses against multiple attackers and the generality of effect of different resistance mechanisms. The jasmonate response is known to protect plants against a wide range of insect herbivores; in this study, we examined the role of the jasmonate response in susceptibility to eight pathogens with diverse lifestyles in the laboratory and field. Recent biochemical models suggest that the lifestyle of the pathogen (necrotroph versus biotroph) should predict whether the jasmonate response will be involved in resistance. We tested this by examining the susceptibility of wild-type (cv Castlemart with no known genes for resistance to the pathogens used) and jasmonate-deficient mutant tomato (Lycopersicon esculentum) plants (def1) and by employing rescue treatments of the mutant. Plant susceptibility to five of the eight pathogens we examined was reduced by the jasmonate response, including two bacteria (Pseudomonas syringae and Xanthomonas campestris), two fungi (Verticillium dahliae and Fusarium oxysporum f. sp. lycopersici), and an oomycete (Phytophthora infestans). Susceptibility to three fungi was unaffected (Cladosporium fulvum, Oidium neolycopersici, and Septoria lycopersici). Our results indicate that the jasmonate response reduces damage by a wide range of pathogens from different lifestyles, a result that contrasts with the emerging picture of diseases on Arabidopsis. Thus, the generality of jasmonate-based resistance of tomato challenges the view that ecologically distinct plant parasites are resisted via different mechanisms.
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