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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.

SUBMITTER: Wei J

PROVIDER: S-EPMC3039750 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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

Wei Jianing J Wang Lizhong L Zhao Jiuhai J Li Chuanyou C Ge Feng F Kang Le L

The New phytologist 20101011 2

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) p ...[more]

PMID: 21039561

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Project description:Background and aimsMost crops have been dramatically altered from their wild ancestors with the primary goal of increasing harvestable yield. A long-held hypothesis is that increased allocation to yield has reduced plant investment in defence and resulted in crops that are highly susceptible to pests. However, clear demonstrations of these trade-offs have been elusive due to the many selective pressures that occur concurrently during crop domestication.MethodsTo provide a robust test of whether increased allocation to yield can alter plant investment in defence, this study examined fruit chemical defence traits and herbivore resistance across 52 wild and 56 domesticated genotypes of apples that vary >26-fold in fruit size. Ninety-six phenolic metabolites were quantified in apple skin, pulp and seeds, and resistance to the codling moth was assessed with a series of bioassays.Key resultsThe results show that wild apples have higher total phenolic concentrations and a higher diversity of metabolites than domesticated apples in skin, pulp and seeds. A negative phenotypic relationship between fruit size and phenolics indicates that this pattern is driven in part by allocation-based trade-offs between yield and defence. There were no clear differences in codling moth performance between wild and domesticated apples and no overall effects of total phenolic concentration on codling moth performance, but the results did show that codling moth resistance was increased in apples with higher phenolic diversity. The concentrations of a few individual compounds (primarily flavan-3-ols) also correlated with increased resistance, primarily driven by a reduction in pupal mass of female moths.ConclusionsThe negative phenotypic relationship between fruit size and phenolic content, observed across a large number of wild and domesticated genotypes, supports the hypothesis of yield-defence trade-offs in crops. However, the limited effects of phenolics on codling moth highlight the complexity of consequences that domestication has for plant-herbivore interactions. Continued studies of crop domestication can further our understanding of the multiple trade-offs involved in plant defence, while simultaneously leading to novel discoveries that can improve the sustainability of crop production.

Project description:Plants can defend themselves against herbivores through activation of defensive pathways and attraction of third-trophic-level predators and parasites. Trophic cascades that mediate interactions in the phytobiome are part of a larger dynamic including the pathogens of the plant itself, which are known to greatly influence plant defenses. As such, we investigated the impact of a phloem-limited bacterial pathogen, Candidatus Liberibacter asiaticus (CLas), in cultivated citrus rootstock on a well-studied belowground tritrophic interaction involving the attraction of an entomopathogenic nematode (EPN), Steinernema diaprepesi, to their root-feeding insect hosts, Diaprepes abbreviatus larvae. Using belowground olfactometers, we show how CLas infection interferes with this belowground interaction by similarly inducing the release of a C12 terpene, pregeijerene, and disconnecting the association of the terpene with insect presence. D. abbreviatus larvae that were not feeding but in the presence of a CLas-infected plant were more likely to be infected by EPN than those near uninfected plants. Furthermore, nonfeeding larvae associated with CLas-infected plants were just as likely to be infected by EPN as those near noninfected plants with D. abbreviatus larval damage. Larvae of two weevil species, D. abbreviatus and Pachnaeus litus, were also more attracted to plants with infection than to uninfected plants. D. abbreviatus larvae were most active when exposed to pregeijerene at a concentration of 0.1 μg/μl. We attribute this attraction to CLas-infected plants to the same signal previously thought to be a herbivore-induced plant volatile specifically induced by root-feeding insects, pregeijerene, by assessing volatiles collected from the roots of infected plants and uninfected plants with and without feeding D. abbreviatus. Synthesis. Phytopathogens can influence the structuring of soil communities extending to the third trophic level. Field populations of EPN may be less effective at host-finding using pregeijerene as a cue in citrus grove agroecosystems with high presence of CLas infection.

Project description:Ocean Acidification (OA) will influence marine ecosystems by changing species abundance and composition. Major effects are described for calcifying organisms, which are significantly impacted by decreasing pH values. Direct effects on commercially important fish are less well studied. The early life stages of fish populations often lack internal regulatory mechanisms to withstand the effects of abnormal pH. Negative effects can be expected on growth, survival, and recruitment success. Here we study Norwegian coastal cod, one of the few stocks where such a negative effect was experimentally quantified, and develop a framework for coupling experimental data on OA effects to ecological-economic fisheries models. In this paper, we scale the observed physiological responses to the population level by using the experimentally determined mortality rates as part of the stock-recruitment relationship. We then use an ecological-economic optimization model, to explore the potential effect of rising CO2 concentration on ecological (stock size), economic (profits), consumer-related (harvest) and social (employment) indicators, with scenarios ranging from present day conditions up to extreme acidification. Under the assumptions of our model, yields and profits could largely be maintained under moderate OA by adapting future fishing mortality (and related effort) to changes owing to altered pH. This adaptation comes at the costs of reduced stock size and employment, however. Explicitly visualizing these ecological, economic and social tradeoffs will help in defining realistic future objectives. Our results can be generalized to any stressor (or stressor combination), which is decreasing recruitment success. The main findings of an aggravation of trade-offs will remain valid. This seems to be of special relevance for coastal stocks with limited options for migration to avoid unfavorable future conditions and subsequently for coastal fisheries, which are often small scale local fisheries with limited operational ranges.

Dataset Information

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

Publications

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

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