Plant Volatiles as a Defense against Insect Herbivores

Abstract

Leaves normally release small quantities of volatile chemicals, but when a plant is damaged by herbivorous insects, many more volatiles are released. The chemical identity of the volatile compounds varies with the plant species and with the herbivorous insect species. These volatiles attract both parasitic and predatory insects that are natural enemies of the herbivores. They may also induce defense responses in neighboring plants. Such chemicals, which function in communication between and among species, as well as those that serve as messengers between members of the same species, are called semiochemicals (from the Greek “semeion,” a mark or signal) (Law and Regnier, 1971). Semiochemicals emitted from a diverse group of plants and insects mediate key processes in the behavior of specific insects. Volatile phytochemicals can serve as airborne semiochemicals, promoting or deterring interactions between plants and insect herbivores. For example, wheat seedlings without herbivore damage attract aphids, whereas odors released from wheat seedlings with a high density of aphids repel other aphids (Quiroz et al., 1997). For swallowtail butterflies, volatiles from host plants enhance the effect of contact stimulants, increasing landing rates and oviposition relative to non-host plants (Feeny et al., 1989). Schematic representation indicating an increase of volatile compounds released by plants in response to insect feeding triggered by an interaction of elicitors such as volicitin in the oral secretions of insect herbivores with damaged plant tissue. Volatile semiochemicals are then used by natural enemies of herbivores such as parasitoid wasps to locate their hosts. Biosynthetic pathways leading to the release of plant volatiles. Indole, a product of the shikimic acid pathway, is formed from indole-3-glycerol-P either as an intermediate in Trp biosynthesis or by a Trp-independent pathway leading to a family of nitrogen-containing defense compounds (e.g. 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one) (Frey et al., 1997). Sesquiterpenes are synthesized via the isopentenyl pyrophosphate (IPP) intermediate following the classical mevalonate pathway, whereas monoterpenes and diterpenes are synthesized via an alternative IPP pathway with glyceraldehyde-3-P and pyruvate identified as the direct precursors of IPP (Lichtenthaler et al., 1997). The mevalonate pathway is localized in the cytosol and reactions for the non-mevalonate pathway are localized in plastids. The homoterpene (E)-4,8-dimethyl-1,3,7-nonatriene and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene are derived from their 15 and 20 carbon precursors, farnesyl- and geranylgeranyl-pyrophosphate, respectively, by a series of enzymatic steps with the overall loss of four carbon units (Donath and Boland, 1994). The green-leaf volatiles are derived from linolenic acid via a 13-hydroperoxylinolenic acid intermediate (Blee, 1998). This oxidized linolenic acid, instead of losing water and committing the molecule down the defense signaling jasmonic acid pathway, is cleaved to form two fragments of 12 and six carbon units (Fig. 3). The variety of green-leaf volatiles are formed from this second pathway by multiple rearrangement steps of the six-carbon (Z)-3-hexenal. An undamaged plant maintains a baseline level of volatile metabolites that are released from the surface of the leaf and/or from accumulated storage sites in the leaf. These constitutive chemical reserves, which often include monoterpenes, sesquiterpenes, and aromatics, accumulate to high levels in specialized glands or trichomes (Paré and Tumlinson, 1997a). In addition, green-leaf odors consisting of a blend of saturated and unsaturated six-carbon alcohols, aldehydes, and esters are produced by autolytic oxidative breakdown of membrane lipids and are released when leaves are mechanically damaged. This pattern of constitutive compounds has been analyzed in the field for perennials, including beech (Tollsten and Müller, 1996) and ash (Markovic et al., 1996) trees, as well as under greenhouse conditions for many herbaceous annuals, including brussels sprouts (Mattiacci et al., 1994) and cucumber (Takabayashi et al., 1994). Plants respond to insect feeding damage by releasing a variety of volatiles from the damaged site, and the profile of the volatiles emitted is markedly different from those of undamaged or mechanically damaged plants. In cotton, breakage of leaf glands causes stored terpenes to be re-leased in much higher levels, and the emissions of lipoxygenase pathway green-leaf volatiles are also increased. While the release of these metabolites correlates closely with leaf damage from insect feeding (Loughrin et al., 1994), a subset of terpenes, the nitrogen-containing compound indole, and hexenyl acetate are also released in much higher levels with insect feeding, but in a diurnal cycle that is decoupled from short-term insect damage. These compounds, linalool and (E)-β-ocimene (monoterpenes), (E,E