Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

Bruinsma, Maaike; Broekhoven, Sarah van; Poelman, Erik H.; Posthumus, M.A.; Müller, Martin; Loon, Joop J. A. van; Dicke, Marcel

doi:10.1007/s00442-009-1459-x

Cited by 56 publications

(50 citation statements)

References 46 publications

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“…This result is consistent with the observations that oxidative stress and electrolyte leakage are induced by insect damage (Bruinsma et al, 2010). Emissions were present throughout the feeding treatment, reflecting continuous damage of foliage during feeding, while emissions decreased drastically after larvae were removed and the stress was relieved (Figs.…”

Section: Discussionsupporting

confidence: 91%

Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage

et al. 2010

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Plant volatile organic compounds (VOCs) elicited in response to herbivory serve as cues for parasitic and predatory insects. Knowledge about quantitative relationships between the extent of herbivore-induced damage and the quantities of VOCs released is scarce. We studied the kinetics of VOC-emissions from foliage of the deciduous tree Alnus glutinosa induced by feeding activity of larvae of the geometrid moth Cabera pusaria. Quantitative relationships between the intensity of stress and strength of plant response were determined. Intensity of biotic stress was characterized by herbivore numbers (0-8 larvae) and by the amount of leaf area eaten. The strength of plant response was characterized by monitoring (i) changes in photosynthesis, (ii) leaf ultrastructure, and (iii) plant volatiles. Net assimilation rate displayed compensatory responses in herbivore-damaged leaves compared with control leaves. This compensatory response was associated with an overall increase in chloroplast size. Feeding-induced emissions of products of the lipoxygenase pathway (LOX products; (E)-2-hexenal, (Z)-3-hexenol, 1-hexanol, and (Z)-3-hexenyl acetate) peaked at day 1 after larval feeding started, followed by an increase of emissions of ubiquitous monoterpenes peaking on days 2 and 3. The emission of the monoterpene (E)-β-ocimene and of the nerolidol-derived homoterpene 4,8-dimethyl-nona-1,3,7-triene (DMNT) peaked on day 3. Furthermore, the emission kinetics of the sesquiterpene (E,E)-α-farnesene tended to be biphasic with peaks on days 2 and 4 after start of larval feeding. Emission rates of the induced LOX products, of (E)-β-ocimene and (E,E)-α-farnesene were positively correlated with the number of larvae feeding. In contrast, the emission of DMNT was independent of the number of feeders. These data show quantitative relationships between the strength of herbivory and the emissions of LOX products and most of the terpenoids elicited in response to feeding. Thus, herbivory-elicited LOX products and terpenoid emissions may convey both quantitative and qualitative signals to antagonists of the herbivores. In contrast, our data suggest that the feeding-induced homoterpene DMNT conveys the information "presence of herbivores" rather than information about the quantities of herbivores to predators and parasitoids.

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Section: Discussionsupporting

confidence: 91%

Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage

et al. 2010

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“…For phenidone (1-phenyl-3-pyrazolidinone) treatment, an aqueous solution of phenidone (2 mM, Sigma-Aldrich, Germany) was sprayed two times as described for JA. The same concentration inhibited endogenous JA synthesis without causing phytotoxicity in earlier studies [22], [29]. ‘Phenidone + JA’ treated flowers received an additional spray of 1 mM JA two times after the final phenidone application.…”

Section: Methodsmentioning

confidence: 89%

The Role of Jasmonates in Floral Nectar Secretion

et al. 2010

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Plants produce nectar in their flowers as a reward for their pollinators and most of our crops depend on insect pollination, but little is known on the physiological control of nectar secretion. Jasmonates are well-known for their effects on senescence, the development and opening of flowers and on plant defences such as extrafloral nectar. Their role in floral nectar secretion has, however, not been explored so far. We investigated whether jasmonates have an influence on floral nectar secretion in oil-seed rape, Brassica napus. The floral tissues of this plant produced jasmonic acid (JA) endogenously, and JA concentrations peaked shortly before nectar secretion was highest. Exogenous application of JA to flowers induced nectar secretion, which was suppressed by treatment with phenidone, an inhibitor of JA synthesis. This effect could be reversed by additional application of JA. Jasmonoyl-isoleucine and its structural mimic coronalon also increased nectar secretion. Herbivory or addition of JA to the leaves did not have an effect on floral nectar secretion, demonstrating a functional separation of systemic defence signalling from reproductive nectar secretion. Jasmonates, which have been intensively studied in the context of herbivore defences and flower development, have a profound effect on floral nectar secretion and, thus, pollination efficiency in B. napus. Our results link floral nectar secretion to jasmonate signalling and thereby integrate the floral nectar secretion into the complex network of oxylipid-mediated developmental processes of plants.

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“…Among the most common herbivores that arrive later in the season is the diamondback moth (Plutella xylostella; Lepidoptera: Plutellidae), which prefers to lay her eggs on herbivore-induced plants over undamaged control plants (22)(23)(24)(25). Here, we studied whether different parasitoid species that…”

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confidence: 99%

Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores

Poelman

Zheng

Zhang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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109

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Plants are exposed to a suite of herbivorous attackers that often arrive sequentially. Herbivory affects interactions between the host plants and subsequently attacking herbivores. Moreover, plants may respond to herbivory by emitting volatile organic compounds (VOCs) that attract carnivorous natural enemies of the herbivores. However, information borne by VOCs is ubiquitous and may attract carnivores, such as parasitoids, that differ in their effectiveness at releasing the plant from its herbivorous attackers. Furthermore, the development of parasitoids within their herbivorous hosts, attacking a given host plant, may influence the elicitation of defensive reactions in the host plant. This may, in turn, affect the behavior of subsequent herbivores attacking the host plant. Here, we show that the species identity of a parasitoid had a more significant effect on defense responses of Brassica oleracea plants than the species identity of the herbivorous hosts of the parasitoids. Consequently, B. oleracea plants that were damaged by caterpillars (Pieris spp.) parasitized by different parasitoid species varied in the degree to which diamondback moths (Plutella xylostella) selected the plants for oviposition. Attracting parasitoids in general benefitted the plants by reducing diamondback moth colonization. However, the species of parasitoid that parasitized the herbivore significantly affected the magnitude of this benefit by its species-specific effect on herbivore-plant interactions mediated by caterpillar regurgitant. Our findings show that information-mediated indirect defense may lead to unpredictable consequences for plants when considering trait-mediated effects of parasitized caterpillars on the host plant and their consequences because of community-wide responses to induced plants.herbivore preference | induced gene transcription | parasitoid-dependent effect A cross their whole kingdom, plants have been found to interact with carnivorous arthropods that act to control herbivorous attackers of the plants. Such interactions between plants and carnivorous arthropods may ultimately increase fitness of the plants (1-3). Plant traits involved in such interactions include those that provide a predator/parasitoid with a resource such as, for example, food or shelter, or with information on the presence and abundance of herbivorous prey/hosts (4, 5). Although resource-and information-mediated indirect defenses of plants have long been collectively viewed within the context of ecological and evolutionary theory of indirect defenses, interactions between plants and carnivorous arthropods based on resource provisioning are distinctly different from those mediated by providing information (6). Whereas resource provisioning can be obligate and is often restricted to interactions with a limited number of carnivorous species, information emitted by herbivore-infested plants is generally ubiquitous, allowing all other organisms to respond to this information (5). Release of herbivore-induced volatile organic compounds (VOCs)...

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Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

Cited by 56 publications

References 46 publications

Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage

Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage

The Role of Jasmonates in Floral Nectar Secretion

Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores

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