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The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes (Marschner Review for the "Rhizosphere 3" Special Issue)

2012-1-19, Turlings, Ted, Hiltpold, Ivan, Rasmann, Sergio

Background Entomopathogenic nematodes (EPNs) are tiny parasitic worms that parasitize insects, in which they reproduce. Their foraging behavior has been subject to numerous studies, most of which have proposed that, at short distances, EPNs use chemicals that are emitted directly from the host as host location cues. Carbon dioxide (CO2) in particular has been implicated as an important cue. Recent evidence shows that at longer distances several EPNs take advantage of volatiles that are specifically emitted by roots in response to insect attack. Studies that have revealed these plant-mediated interactions among three trophic levels have been met with some disbelief. Scope This review aims to take away this skepticism by summarizing the evidence for a role of root volatiles as foraging cues for EPNs. To reinforce our argument, we conducted olfactometer assays in which we directly compared the attraction of an EPN species to CO2 and two typical inducible root volatiles. Conclusions The combination of the ubiquitous gas and a more specific root volatile was found to be considerably more attractive than one of the two alone. Hence, future studies on EPN foraging behavior should take into account that CO2 and plant volatiles may work in synergy as attractants for EPNs. Recent research efforts also reveal prospects of exploiting plant-produced signals to improve the biological control of insect pests in the rhizosphere.

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Restoring a maize root signal that attracts insect-killing nematodes to control a major pest

2009, Degenhardt, Jörg, Hiltpold, Ivan, Köllner, Tobias G., Frey, Monika, Gierl, Alfons, Gershenzon, Jonathan, Hibbard, Bruce E., Ellersieck, Mark R., Turlings, Ted

When attacked by herbivorous insects, plants emit volatile compounds that attract natural enemies of the insects. It has been proposed that these volatile signals can be manipulated to improve crop protection. Here, we demonstrate the full potential of this strategy by restoring the emission of a specific belowground signal emitted by insect-damaged maize roots. The western corn rootworm induces the roots of many maize varieties to emit (E)-β-caryophyllene, which attracts entomopathogenic nematodes that infect and kill the voracious root pest. However, most North American maize varieties have lost the ability to emit (E)-β-caryophyllene and may therefore receive little protection from the nematodes. To restore the signal, a nonemitting maize line was transformed with a (E)-β-caryophyllene synthase gene from oregano, resulting in constitutive emissions of this sesquiterpene. In rootworm-infested field plots in which nematodes were released, the (E)-β-caryophyllene-emitting plants suffered significantly less root damage and had 60% fewer adult beetles emerge than untransformed, nonemitting lines. This demonstration that plant volatile emissions can be manipulated to enhance the effectiveness of biological control agents opens the way for novel and ecologically sound strategies to fight a variety of insect pests.

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Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests and to improve crop yield

2012, Hiltpold, Ivan, Turlings, Ted

In most agro-ecosystems the organisms that feed on plant roots have an important impact on crop yield and can impose tremendous costs to farmers. Similar to aboveground pests, they rely on a broad range of chemical cues to locate their host plant. In their turn, plants have co-evolved a large arsenal of direct and indirect defense to face these attacks. For instance, insect herbivory induces the synthesis and release of specific volatile compounds in plants. These volatiles have been shown to be highly attractive to natural enemies of the herbivores, such as parasitoids, predators, or entomopathogenic nematodes. So far few of the key compounds mediating these so-called tritrophic interactions have been identified and only few genes and biochemical pathways responsible for the production of the emitted volatiles have been elucidated and described. Roots also exude chemicals that directly impact belowground herbivores by altering their behavior or development. Many of these compounds remain unknown, but the identification of, for instance, a key compound that triggers nematode egg hatching to some plant parasitic nematodes has great potential for application in crop protection. These advances in understanding the chemical emissions and their role in ecological signaling open novel ways to manipulate plant exudates in order to enhance their natural defense properties. The potential of this approach is discussed, and we identify several gaps in our knowledge and steps that need to be taken to arrive at ecologically sound strategies for belowground pest management.

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Belowground chemical signaling in maize: When simplicity rhymes with efficiency

2008, Hiltpold, Ivan, Turlings, Ted

Maize roots respond to feeding by larvae of the beetle Diabrotica virgifera virgifera by releasing (E)-beta-caryophyllene. This sesquiterpene, which is not found in healthy maize roots, attracts the entomopathogenic nematode Heterorhabditis megidis. In sharp contrast to the emission of virtually only this single compound by damaged roots, maize leaves emit a blend of numerous volatile organic compounds in response to herbivory. To try to explain this difference between roots and leaves, we studied the diffusion properties of various maize volatiles in sand and soil. The best diffusing compounds were found to be terpenes. Only one other sesquiterpene known for maize, alpha-copaene, diffused better than (E)-beta-caryophyllene, but biosynthesis of the former is far more costly for the plant than the latter. The diffusion of (E)-beta-caryophyllene occurs through the gaseous rather than the aqueous phase, as it was found to diffuse faster and further at low moisture level. However, a water layer is needed to prevent complete loss through vertical diffusion, as was found for totally dry sand. Hence, it appears that maize has adapted to emit a readily diffusing and cost-effective belowground signal from its insect-damaged roots.

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Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm

2012, Hiltpold, Ivan, Hibbard, Bruce Elliott, French, B. W., Turlings, Ted

Aims The use of entomopathogenic nematodes in the biological control of soil insect pests is hampered by the costly and inadequate application techniques. As a possible solution we evaluated a nematode encapsulation approach that offers effective application and may possibly attract the pest by adding attractants to the capsule shell. Methods Heterorhabditis bacteriophora nematodes, which show high virulence against the maize root pest Diabrotica virgifera virgifera, were encapsulated in a polysaccharide shell derived from the algae Laminaria ssp. Shells of varying thickness and composition were evaluated. Results Nematodes readily survived the encapsulation process and were able, varying with shell thickness and temperature, to break through the shell and subsequently infect hosts. The added attractants and feeding stimulants to the shell attracted the pest larvae as much as maize roots. In field trials, encapsulated H. bacteriophora nematodes were more effective in controlling D. v. virgifera than those sprayed in water over the soil surface, but in these trials the addition of stimulants did not increase the control efficiency. Conclusions The study demonstrates that nematodes can be successfully applied in capsules in the field. Further improvements are needed to make the capsules a cost effective alternative to conventional field application of nematodes.