Biochemistry of Plant Volatiles

Abstract

Plants have a penchant for perfuming the atmosphere around them. Since antiquity it has been known that both floral and vegetative parts of many species emit substances with distinctive smells. The discovery of the gaseous hormone ethylene 70 years ago brought the realization that at least some of the compounds emitted may have physiological significance without any distinctive smell to humans. At present, more than 1,000 low M r organic compounds have been reported to be emitted from plants, although a comprehensive list is available only for floral volatiles (Knudsen et al., 1993). Our knowledge of the occurrence and distribution of plant volatiles has been significantly extended in the last 15 years thanks to the adoption of simple, sensitive methods for headspace sampling and the availability of relatively inexpensive bench-top instruments for gas chromatography-mass spectrometry. The substances reported are largely lipophilic products with molecular masses under 300. Most can be assigned to the following classes (in order of decreasing size): terpenoids, fatty acid derivatives including lipoxygenase pathway products, benzenoids and phenylpropanoids, C5-branched compounds, and various nitrogen and sulfur containing compounds. Nearly all of these classes are emitted from vegetative parts as well as flowers (Knudsen et al., 1993), and some are even emitted from roots (Steeghs et al., 2004). A major discovery of the last decade is that plants commonly emit much greater amounts and varieties of volatiles after herbivore damage, and not just from the site of injury (Pare and Tumlinson, 1999). Major progress in plant volatile research, as in other areas of plant biology, has come from the use of molecular and biochemical techniques. A large number of genes encoding enzymes of volatile biosynthesis have recently been reported. In vitro characterization of the heterologously expressed enzymes, especially determination of their substrate and product specificity, has helped clarify the pathways of volatile formation. In addition, investigation of the spatial and temporal patterns of gene expression has provided new information on the factors regulating the emission of plant volatile compounds. In this update, we survey the latest advances on the biosynthesis and regulation of plant volatiles, beginning with a brief review of the function of these substances. Perhaps the greatest mysteries surrounding volatiles concern their function in the life of the plant. While it is generally assumed that compounds emitted from flowers serve to attract and guide pollinators (Reinhard et al., 2004), only scattered attempts have been made to demonstrate the ability of individual substances to attract specific pollinators. Many floral volatiles have anti-microbial or anti-herbivore activity (DeMoraes et al., 2001; Friedman et al., 2002; Hammer et al., 2003), and so could also act to protect valuable reproductive parts of plants from enemies. Among vegetative volatiles, the most intensively studied substance is isoprene, a simple five-carbon terpene emitted from the foliage of many woody species (Sharkey and Yeh, 2001b). The function of isoprene is still controversial, and this compound may act to increase the tolerance of photosynthesis to high temperatures by stabilizing the thylakoid membranes (Sharkey et al., 2001a) or by quenching reactive oxygen species (Loreto and Velikova, 2001). The release of volatiles from vegetative organs following herbivore damage seems to be a general property of plant species. Contributions to this special issue cover herbivore-induced volatiles from cabbage (Brassica oleracea; Vuorinen et al., 2004b), cucumber (Cucumis sativus; Mercke et al., 2004), Lotus japonicus (Arimura et al., 2004b), and maize (Zea mays; Degen et al., 2004). These substances have been demonstrated to serve as indirect plant defenses. That is, they attract arthropods that prey upon or parasitize herbivores, thus minimizing further damage to plant tissue (Pare and Tumlinson, 1999; Dicke and Van Loon, 2000). In some cases, herbivore-induced volatiles may also act as direct defenses, repelling (DeMoraes et al., 2001; Kessler and Baldwin, 2001) or intoxicating (Vancanneyt et al., 2001) herbivores and pathogens (Andersen et al., 1994). The possibility that these substances also act in plant-plant communication has been discussed (Arimura et al., 2000; Dicke and Bruin, 2001; Engelberth et al., 2004). Herbivore-induced volatiles could additionally have physiological roles within the plant, with their release being a consequence of their volatility and membrane solubility. Like isoprene, some herbivore-induced monoterpenes and sesquiterpenes have the potential to combine with various reactive oxygen species (Hoffmann et al., 1997; Bonn and Moortgat, 2003), and so could protect against internal oxidative damage (Delfine et al., 2000; Loreto et al., 2004b). In fact, ozone fumigation has recently been reported to promote the emission o