Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions

State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China.
New Phytologist (Impact Factor: 7.67). 10/2010; 189(2):557-67. DOI: 10.1111/j.1469-8137.2010.03491.x
Source: PubMed


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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    • "However, the phytohormones JA and SA are also known to regulate the production of plant volatiles (Dicke et al., 1999; Ozawa et al., 2000; Lou et al., 2005). Herbivoryinduced plant volatiles (HIPVs) play vital roles in enabling herbivores and their natural enemies to locate their food from a distance (Dicke et al., 1990; Turlings et al., 1995; Bruce et al., 2005; Wei et al., 2007; Dicke and Baldwin, 2010; Bruce and Pickett, 2011). Although a few studies have explored such negative SA–JA crosstalk in plant–herbivore–natural enemy interactions (Zhang et al., 2009; Thaler et al., 2010), to date it is largely unknown how SA–JA negative crosstalk affects host-plant selection behaviour of herbivores. "
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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.
    Full-text · Article · Jun 2014 · Journal of Experimental Botany
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    • "Previous research indicated that several JA-overexpression mutants exhibit greater resistance against insects than wild-type plants424344. Wei et al. (2011) showed that there are ecological trade-offs between JA-dependent direct and indirect defences in genetically modified plants22. Our previous research indicated that the JA-overexpression tomato mutant 35S was resistant to B. tabaci under a high O3 concentration and whitefly infestation and there was a reduction in the fitness of conspecific B. tabaci that fed on three previously infested tomato genotypes that differed in the JA pathway4546. "
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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.
    Full-text · Article · Jun 2014 · Scientific Reports
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    • "In other systems, a key role of JA signalling pathway in regulating indirect plant defence, that is, the volatile-mediated attraction of parasitoids or predators, has been well demonstrated (Thaler et al. 2002; Ament et al. 2004; Bruce et al. 2008; Girling et al. 2008; Bruinsma et al. 2009; Wei et al. 2011) and a few studies have shown that JA-dependent indirect plant defence offers benefits under field conditions (Thaler 1999; Heil et al. 2001). As yet, the role of other signalling pathways in attracting natural enemies of herbivores was not known, although it has been indicated that the SA-signalling plays a role in regulating certain herbivore-induced plant volatile emissions (Ozawa et al. 2000; Van Poecke & Dicke 2002). "
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    ABSTRACT: Herbivore attack induces plants to mobilize chemical defences, including the release of volatiles that attract natural enemies of the herbivore. This commonly involves the jasmonic acid (JA) pathway. However, phloem-feeding whiteflies specifically trigger salicylic acid (SA)-signalling, thereby suppressing JA-based defences and enhancing host plant suitability.Here, we show with Arabidopsis thaliana plants that the whitefly parasitoid Encarsia formosa outsmarts this apparent host plant manipulation by exploiting the SA-triggered emission of β-myrcene. Assays with various Arabidopsis mutants and phytohormone and gene-expression analyses reveal that the whiteflies induce the accumulation of endogenous SA, thereby enhancing the expression of SA-regulated genes, one of which encodes ocimene/myrcene synthase, which resulted in the recruitment of parasitoids under greenhouse conditions. Performance assays confirmed that whiteflies directly benefit from suppressing JA-based defences.Taken together, we conclude that by activating SA-signalling whitefly feeding suppresses direct, JA-based defences, but that parasitoids can adapt to this by exploiting specific, SA-induced volatile emissions for host location.Our work further confirms that herbivory contributes to selective pressure governing the evolution of inducible volatile signals as indirect plant defences.
    Full-text · Article · Dec 2013 · Functional Ecology
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