Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions.
ABSTRACT Recent studies on plants genetically modified in jasmonic acid (JA) signalling support the hypothesis that the jasmonate family of oxylipins plays an important role in mediating direct and indirect plant defences. However, the interaction of two modes of defence in tritrophic systems is largely unknown. In this study, we examined the preference and performance of a herbivorous leafminer (Liriomyza huidobrensis) and its parasitic wasp (Opius dissitus) on three tomato genotypes: a wild-type (WT) plant, a JA biosynthesis (spr2) mutant, and a JA-overexpression 35S::prosys plant. Their proteinase inhibitor production and volatile emission were used as direct and indirect defence factors to evaluate the responses of leafminers and parasitoids. Here, we show that although spr2 mutant plants are compromised in direct defence against the larval leafminers and in attracting parasitoids, they are less attractive to adult flies compared with WT plants. Moreover, in comparison to other genotypes, the 35S::prosys plant displays greater direct and constitutive indirect defences, but reduced success of parasitism by parasitoids. Taken together, these results suggest that there are distinguished ecological trade-offs between JA-dependent direct and indirect defences in genetically modified plants whose fitness should be assessed in tritrophic systems and under natural conditions.
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ABSTRACT: We experimentally examined the effects of elevated O3 and whitefly herbivory on tomato volatiles, feeding and oviposition preferences of whiteflies and behavioural responses of Encarsia formosa to these emissions on two tomato genotypes, a wild-type (Wt) and a jasmonic acid (JA) defence-enhanced genotype (JA-OE, 35S). The O3 level and whitefly herbivory significantly increased the total amount of volatile organic compounds (VOCs), monoterpenes, green leaf volatiles (GLVs), and aldehyde volatiles produced by tomato plants. The 35S plants released higher amount of total VOCs and monoterpene volatiles than Wt plants under O3+herbivory treatments. The feeding and oviposition bioassays showed that control plants were preferred by adult whiteflies whereas the 35S plants were not preferred by whiteflies. In the Y-tube tests, O3+herbivory treatment genotypes were preferred by adult E. Formosa. The 35S plants were preferred by adult E. formosa under O3, herbivory and O3+herbivory treatments. Our results demonstrated that elevated O3 and whitefly herbivory significantly increased tomato volatiles, which attracted E. formosa and reduced whitefly feeding. The 35S plants had a higher resistance to B. tabaci than Wt plant. Such changes suggest that the direct and indirect defences of resistant genotypes, such as 35S, could strengthen as the atmospheric O3 concentration increases.Scientific reports. 01/2014; 4:5350.
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ABSTRACT: 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.Proceedings of the National Academy of Sciences 04/2014; · 9.81 Impact Factor
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ABSTRACT: The jasmonic acid (JA) and salicylic acid (SA) signalling pathways, which mediate induced plant defence responses, can express negative crosstalk. Limited knowledge is available on the effects of this crosstalk on host-plant selection behaviour of herbivores. We report on temporal and dosage effects of such crosstalk on host preference and oviposition-site selection behaviour of the herbivorous spider mite Tetranychus urticae towards Lima bean (Phaseolus lunatus) plants, including underlying mechanisms. Behavioural observations reveal a dynamic temporal response of mites to single or combined applications of JA and SA to the plant, including attraction and repellence, and an antagonistic interaction between SA- and JA-mediated plant responses. Dose-response experiments show that concentrations of 0.001mM and higher of one phytohormone can neutralize the repellent effect of a 1mM application of the other phytohormone on herbivore behaviour. Moreover, antagonism between the two signal-transduction pathways affects phytohormone-induced volatile emission. Our multidisciplinary study reveals the dynamic plant phenotype that is modulated by subtle changes in relative phytohormonal titres and consequences for the dynamic host-plant selection by an herbivore. The longer-term effects on plant-herbivore interactions deserve further investigation.Journal of Experimental Botany 06/2014; 65(12):3289-3298. · 5.79 Impact Factor