Insects turn up their noses at sweating plants

Green plants are now being widely touted in both the popular press and scientific literature as factories for biofuels. However, like many factories, plants emit a variety of gaseous byproducts directly into the atmosphere. Besides carbon dioxide, oxygen, and water vapor, a host of terpenes are released, ranging from the simple 5-carbon compound isoprene (2-methyl-1,3-butadiene) to the 10-carbon monoterpenes and the 15-carbon sesquiterpenes (1). Terpene emission from plants has been widely studied by atmospheric chemists because of its prominent effects on ozone levels and aerosol formation (2). Plant biologists have also joined in to determine what roles emitted terpenes might have in the lives of the plants that release them. Two main lines of inquiry have been followed.

One group of investigators has focused on isoprene, examining the ability of this compound to protect plants from various abiotic stresses. Isoprene can be likened to a gaseous sweat. Not only is its production and release stimulated by heat, but it also ameliorates the effects of thermal and oxidative stresses on the plant's photosynthetic apparatus (2–5).

A second group of investigators has been concerned with the monoterpenes and sesquiterpenes emitted by plants after herbivory. These compounds often function as cries for help, attracting predators and parasitic wasps that attack herbivores (6–9). Curiously, there has been little interaction between these two lines of study until now.

This issue of PNAS presents the results of a very successful collaboration among Jörg-Peter Schnitzler, one of the world's most renowned isoprene researchers, Marcel Dicke, one of the top experts on herbivore-induced terpenes, and two of their very talented coworkers (10). The work reveals that isoprene has unexpected ecological impact.

The Odor of Isoprene Repels Insects

Loivamäki et al. (10) used a line of Arabidopsis thaliana genetically transformed to produce and release isoprene, a compound not normally found in A. thaliana. They studied the effects of this plant on two caterpillar species and two species of caterpillar enemies, all of which are normally associated with plants of the Brassicaceae family, which includes A. thaliana. The two enemies are specialist parasitic wasps that lay their eggs inside one of the caterpillar species (Fig. 1). As the larval wasps develop, their hosts feed less than unparasitized caterpillars and eventually die when the adult wasp emerges. The female wasps find their host caterpillars by using volatile compounds released from plants during insect feeding.

Fig. 1.

Plant pest control in action. A parasitic wasp (Diadegma sp.) laying its eggs in the larva of an herbivore, the diamondback moth (Plutella xylostella). The larva will eventually die when the adult wasp emerges. Egg-laying parasitic wasps of this species fond their hosts via chemical cues, but are repelled by isoprene, a compound not released by food plants of their caterpillar host. [Reproduced with permission from Tibor Bukovinszky, Wageningen University (Copyright 2008, BugsinthePicture.com).]

As part of their carefully-planned investigation, Loivamäki et al. (10) found that the host caterpillars were not affected by the presence of isoprene; caterpillars fed, grew, and the adult butterflies laid eggs equally on isoprene-emitting A. thaliana and nonemitting controls. One of the parasitic wasp species also appeared to be indifferent to isoprene, but egg-laying females of the second wasp species, Diadegma semiclausum (Fig. 1), were consistently repelled by the volatiles of isoprene-emitting plants whether the plants were being fed upon by the caterpillar host or not. When an isoprene standard was added to the air passing over the control line, D. semiclausum females were also repelled. To confirm these surprising observations, Loivamäki et al. next turned to electrophysiology. Careful electrical measurements on the antenna revealed that D. semiclausum was able to detect and respond to isoprene at a low level, but the other wasp species was not, corresponding perfectly with the results of the behavioral experiments.

Isoprene Odor: Orientation Cue for Insects

These fascinating results represent one of the first times that isoprene, long discussed in the plant physiology literature, has been shown to have an ecological function. The study nicely complements another interesting recent report (11) revealing that isoprene emitted from transgenic tobacco can deter feeding by the tobacco hornworm caterpillar. It is not surprising that a common plant volatile, such as isoprene, is involved in interactions with insect herbivores as insects often exploit chemical cues to find food, mates, shelter, and oviposition sites. The ability of isoprene to repel parasitic wasps seeking a specific caterpillar species for oviposition can be rationalized by considering that isoprene is released by only a limited group of plant species, including various oaks, poplars, and willows, most of which are woody (12). None of these species is a host for the caterpillar sought by D. semiclausum. Hence isoprene is a good negative cue for this specialist parasitoid. Negative cues are also used by other insects such as conifer bark beetles, which are repelled by volatile compounds characteristic of broad-leaved trees (13, 14). For a tiny insect searching a vast area for an oviposition site, knowing where not to search may be almost as important as knowing where to search. The repulsion of D. semiclausum could also be attributed to a direct inhibitory action of isoprene on its olfactory receptors. But, this explanation seems less likely because isoprene did not repel the other parasitoid species tested.

To test the role of isoprene in mediating host-finding behavior in insects, a promising next step would be to examine the behavior of an insect parasitoid whose host does feed on an isoprene-emitting plant species. Will such an insect be attracted by isoprene rather than repelled? Such experiments might advantageously be conducted with a poplar taxon such as Populus x canescens, which naturally emits isoprene and for which a line genetically transformed to eliminate isoprene production has already been created (3).

Isoprene Odor: A Weapon in Plant–Plant Competition

From the plant's perspective, the repulsion of enemies of its herbivores by volatiles is hardly a welcome event because enemies can significantly reduce feeding damage and make an important contribution to plant fitness (15, 16). Yet a plant growing near an isoprene-emitting neighbor could find its survival threatened when herbivore enemies attracted by its odoriferous cries of help are chased away by the repulsive smell of its neighbors. Such a possibility suggests a whole new way in which plants might have been evolutionarily selected to wage war on neighbors that compete with them for light, water, and nutrients. By producing isoprene or another repulsive volatile, they might effectively drive away herbivore enemies and increase the level of damage to neighboring plants.

Scenarios like these hint at a vast landscape of complex interactions among plants and associated insects that could be mediated by volatile compounds. To explore this terrain, transgenic plants with altered odor profiles should be useful experimental tools. When terpene-based odors are under study, researchers can exploit the terpene synthase gene family, which encodes proteins producing a wide range of terpene volatiles from ubiquitous intermediates of plant metabolism (17). Overexpression of terpene synthase genes in plants can be used to endow plants with the capacity to make new compounds or mixtures of compounds that may not be conveniently accessible by chemical synthesis, and so give them entirely new odors (6, 9). And, as demonstrated so well by Loivamäki et al. (10), plants with novel smells are valuable tools for discovering new ecological interactions.