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Critical Reviews in Plant Sciences Publication details, including instructions for authors and subscription information: http://tandfprod.literatumonline.com/loi/bpts20 Plant Volatiles: Recent Advances and Future Perspectives Natalia Dudareva a , Florence Negre a , Dinesh A. Nagegowda a & Irina Orlova a a Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, 47907, IN Available online: 18 Jan 2007

To cite this article: Natalia Dudareva, Florence Negre, Dinesh A. Nagegowda & Irina Orlova (2006): Plant Volatiles: Recent Advances and Future Perspectives, Critical Reviews in Plant Sciences, 25:5, 417-440 To link to this article: http://dx.doi.org/10.1080/07352680600899973

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Natalia Dudareva, Florence Negre, Dinesh A. Nagegowda and Irina Orlova Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907

Table of Contents

I. INTRODUCTION ...... 418

II. FUNCTIONS OF PLANT VOLATILES ...... 418 A. Volatiles and Plant Reproduction ...... 418 B. Volatiles and Plant Defense ...... 420 C. Role of Plant Volatiles in Tritrophic Interactions ...... 420 D. Role of Plant Volatiles in Plant-Plant Interactions ...... 421 E. Role of Plant Volatiles in Belowground Defense ...... 422 F. Role of Plant Volatiles in Abiotic Stresses ...... 422

III. ANALYSIS OF PLANT VOLATILES ...... 423

IV. BIOSYNTHESIS OF PLANT VOLATILES ...... 423 A. Terpenoids ...... 423 B. Volatile Fatty Acid Derivatives ...... 427 C. Phenylpropanoids/Benzenoids ...... 427 D. Amino-Acid Volatile Derivatives ...... 429

V. REGULATION OF PLANT VOLATILE EMISSION ...... 429

VI. SIGNAL TRANSDUCTION PATHWAYS REGULATING VOLATILE EMISSION ...... 430

VII. METABOLIC ENGINEERING OF VOLATILE EMISSION ...... 431

VIII. CONCLUSIONS ...... 432

IX. ACKNOWLEDGMENTS ...... 432

REFERENCES ...... 433 Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011

leaves, flowers, and fruits into the atmosphere and from roots Volatile compounds act as a language that plants use for their into the soil, defend plants against herbivores and pathogens or communication and interaction with the surrounding environment. provide a reproductive advantage by attracting pollinators and To date, a total of 1700 volatile compounds have been isolated seed dispersers. Plant volatiles constitute about 1% of plant sec- from more than 90 plant families. These volatiles, released from ondary metabolites and are mainly represented by terpenoids, phenylpropanoids/benzenoids, fatty acid derivatives, and amino acid derivatives. In this review we focus on the functions of plant volatiles, their biosynthesis and regulation, and the metabolic en- gineering of the volatile spectrum, which results in plant defense Address correspondence to Natalia Dudareva, Department of Horti- improvement and changes of scent and aroma properties of flowers culture and Landscape Architecture, Purdue University, West Lafayette, and fruits. IN 47907. E-mail: [email protected]

417 418 N. DUDAREVA ET AL.

Keywords plant volatiles, terpenoids, phenylpropanoids, plant of plant volatile research and its many different aspects ranging defense, plant-plant interactions, signal transduction, from genomics and biochemistry to ecology as well as the use metabolic engineering of many different plant systems, this review is not intended to be entirely comprehensive. Instead, we will focus on a few major topics with examples drawn from selected systems. I. INTRODUCTION Plants, as sedentary organisms, have to adjust to the surround- II. FUNCTIONS OF PLANT VOLATILES ing environment during their life cycle. To compensate for their immobility, plants have evolved various mechanisms for their A. Volatiles and Plant Reproduction interactions with the environment including the release of ar- In nature, all organisms are under selective pressure to maxi- rays of volatile compounds from their leaves, flowers and fruits mize their reproductive success. Within the plant kingdom more into the atmosphere and from roots into the soil. At present, than a quarter of a million species belong to flowering plants, a total of 1700 volatile compounds have been described from most of which are animal pollinated. To attract pollinators and more than 90 plant families (Knudsen and Gershenzon, 2006). seed disseminators and thus to ensure reproductive and evolu- These volatiles constitute about 1% of plant secondary metabo- tionary success, many of these flowering species release diverse lites known to date and are mainly represented by terpenoids, blends of volatile compounds from their flowers and fruits in phenylpropanoids/benzenoids, fatty acid and amino acid deriva- addition to visual and tactile cues (Figure 1) (Buchmann and tives (Dudareva et al., 2004). Volatile compounds are typically Nabhan, 1996; Dudareva and Pichersky, 2000). While flowers lipophilic liquids with high vapor pressures and can cross mem- could be identical in their color or shape, there are no two floral branes freely and be released into the atmosphere or soil in the scents that are exactly the same due to a large diversity of volatile absence of a diffusion barrier (Pichersky et al., 2006). compounds and their relative abundances and interactions within The chemical composition of plant-emitted volatile blends the scent bouquet (Knudsen and Tollsten, 1993; Knudsen et al., and their intensity can carry information about the plants’ phys- 1993). Thus, floral scent is a signal which pollinators can iological status and the stresses they have been subjected to. use to discriminate a particular flower whose nectar and/or The primary functions of airborne volatiles are to defend plants pollen is the reward. In addition to attracting insects to flowers against herbivores and pathogens or to provide a reproductive ad- and guiding them to food resources within the flower, floral vantage by attracting pollinators and seed dispersers (Reinhard volatiles are essential in allowing insects to discriminate among et al., 2004; Pichersky and Gershenzon, 2002). Volatilesemitted plant species and even among individual flowers of a single from vegetative tissues, as a part of the plant defense system, species. can directly repel (De Moraes et al., 2001; Kessler and Baldwin, Floral scent bouquets may contain from one to 100 volatiles, 2001) or intoxicate (Vancanneyt et al., 2001) microbes and an- but most species emit between 20 and 60 different compounds imals, or attract natural predators of attacking herbivores, in- (Knudsen and Gershenzon, 2006). The total amount of emit- directly protecting the plant via tritrophic interactions (Mercke ted floral volatiles varies from the low picogram range to more et al., 2004; Arimura et al., 2004b; Degen et al., 2004). By than 30 µg/h with the largest amounts produced by flowers releasing volatiles, a signaling plant not only reduces the num- of various beetle- and moth-pollinated species (Knudsen and ber of attacking herbivores (Kessler and Baldwin, 2001) but can Gershenzon, 2006). Closely related plant species that rely on also warn the neighboring plants about the herbivore or pathogen different types of insects for pollination produce different odors, attack (Shulaev et al., 1997). These warnings induce the expres- reflecting the olfactory sensitivities or preferences of the polli- sion of defense genes or emission of volatiles in neighboring nators (Henderson, 1986; Raguso and Pichersky, 1995). By pro-

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 plants (Arimura et al., 2000; Birkett et al., 2000; Ruther and viding species-specific signals, flower fragrances facilitate an Kleier, 2005; Farag et al., 2005) or prime these plants to re- insect’s ability to learn particular food sources, thereby increas- spond faster to future herbivore attack (Engelberth et al., 2004; ing its foraging efficiency. Within a species, the level of scent Kessler et al., 2006). Volatiles emitted from roots can contribute emission changes in response to endogenous diurnal rhythms, to a belowground defense system by acting as antimicrobial flower age, pollination status and environmental conditions such or antiherbivore substances, or by attracting enemies of root- as light, temperature, and moisture status (Dudareva et al., 2004). feeding herbivores (Rasmann et al., 2005). Over the past decade The perceptual properties of any mixture of volatile com- there has been significant progress in plant volatile research as a pounds are different from the perceptual properties of their in- result of the increasing sensitivity of analytical instrumentation dividual constituents and are a function of the number of com- and improvements in molecular and biochemical approaches, pounds, their relative concentrations, the intensity of the scent which has led to a better understanding of function, biosynthe- that arises from all the compounds within a bouquet and an sis and regulation of plant volatiles. Here we review the func- animal’s previous experiences with odors (Wright and Smith, tions of plant volatiles, their biosynthesis and regulation, and 2004a, 2004b). To date, there is very little information about metabolic engineering leading to improvement of plant defense, how insects respond to individual components found in floral scent and aroma of flowers and fruits. Due to the complexity scents, even though it is known that they are able to distinguish PLANT VOLATILES 419

FIG. 1. An overview of volatile-mediated plant interactions with the surrounding environment. Plant-animal interactions include the attraction of pollinators and seed disseminators by floral and fruit volatiles, attraction/repellence of herbivores, and attraction of natural enemies of attacking herbivores both in atmosphere and rhizosphere. Aboveground plant-plant interactions comprise elicitation or priming of defense responses in healthy undamaged leaves of the same plant or in the neighboring unattacked plants. Belowground, these interactions include allelopathic activity on the germination and growth of competitive neighboring plants. Volatiles released from reproductive organs and roots also have antimicrobial activity thus protecting the plants from pathogen attack. In addition, isoprene, a leaf volatile confers photoprotection and thermotolerance.

between complex floral scent mixtures. Also, it is still unclear analyzed using gas chromatography coupled with electroan- whether insect pollinators use only a few compounds present tennogram detection (GC-EAD), all three major compounds of in a scent for floral identification, or whether they use infor- P. axillaries scent, benzaldehyde, benzyl alcohol, and methyl- mation from all the scent compounds. However, recently it has benzoate, elicit very high responses (Hoballah et al., 2005). been shown that honeybees are capable of using all of the floral EAD-recordings from the nocturnal hawk moth Sphinx perel- volatiles to discriminate subtle differences in the scent of four egans yielded preferentially strong responses to the same three snapdragon cultivars emitting the same volatile compounds but compounds (Raguso and Light, 1998), suggesting that many at different levels (Wright et al., 2005). Moreover, the ability moths may use the same compounds to locate nectar sources, of honeybees to distinguish between cultivars expands with the although rank orders of sensitivity may differ. Moreover, odor Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 increasing intensity of floral scent. emission from moth-pollinated flowers correlates with nocturnal In contrast to bees, moths use odor cues over longer dis- moth activity and flower-volatile composition is adapted to the tances (Dobson, 1994) and therefore odor quantity has to be antennal perception of these pollinators (Hoballah et al., 2005). higher in order to be detected. Moth-pollinated Clarkia brew- Many floral volatiles have antimicrobial or antifungal activity eri flowers emit a strong sweet floral scent rich in linalool (DeMoraes et al., 2001; Friedman et al., 2002; Hammer et al., and aromatic esters in contrast to closely related bee-pollinated 2003), and could also act to protect valuable reproductive plant Clarkia concinna flowers which emit less compounds and at organs from pathogens (Figure 1). Volatiles involved in antimi- lower levels (Raguso and Pichersky, 1995). Similarly, hawk crobial defense are often produced in pistils and/or nectaries, as moth pollinated Petunia axillaries flowers release high levels of was shown for linalool and linalool oxide in flowers of Clarkia several compounds and elicit significantly higher responses from species (Pichersky et al., 1994; Dudareva et al., 1996) and for the Manduca sexta antenna than flowers of the closely related sesquiterpene and monoterpene formation in Arabidopsis flow- bee-pollinated Petunia integrifolia, which emit almost exclu- ers (Chen et al., 2003; Tholl et al., 2005). sively benzaldehyde (Hoballah et al., 2005). When the antenna- Volatile compounds emitted from fruits determine the over- responses to the individual components of the floral scent were all aroma properties and taste, and thus could play a role in 420 N. DUDAREVA ET AL.

the attraction of animal seed dispersers (Figure 1) (Goff and tion of mechanical damage and low- or high-molecular-weight Klee, 2006). In double-choice experiments, fruit bats (Pteropus elicitors from attacking herbivores induce volatile emission pumilus and Ptenochirus jagori) were able to detect and locate through the release of stored compounds or lead to an in- fruits as well as assess their state of ripeness exclusively by their creased formation of existing and/or de novo biosynthesis of odor (Luft et al., 2003). Olfactory cues emanating from the food new volatile compounds (Pare and Tumlinson, 1997; Turlings source might be especially important in food location for noc- et al., 1998). There is a lag period between treatment and sub- turnal foragers which have limited access to visual cues, as was sequent volatile release. Some volatiles including terpenes, in- suggested for owl monkeys (Aotus nancymai) (Bolen and Green, dole, and methyl salicylate, do not usually emit for hours after 1997). the beginning of herbivore damage. However, almost immedi- ately after wounding and the onset of herbivory plants release green leaf volatiles (GLV), six-carbon aldehydes, alcohols, and B. Volatiles and Plant Defense esters, which are considered as typical wound signals (Hatanaka, In the past two decades it has been well documented that for 1993). Within a species the volatile blends emitted upon herbi- self-protection plants produce blends of volatile compounds in vore attack differ quantitatively and qualitatively (Gouinguene vegetative tissues in response to damage and herbivore attack. et al., 2001; Scutareanu et al., 2003; Krips et al., 2001) with Odor blends emitted by herbivore-infested plants are complex some compounds in common (e.g., methyl salicylate and some mixtures, often composed of more than 200 different com- terpenoids). The differences between volatile blends emitted pounds, many of which occur as minor constituents (Dicke and from plants of one species infested by different herbivores van Loon, 2000). Emitted volatiles can directly affect herbi- are usually smaller than among different plant species (Tak- vores’ physiology and behavior due to their toxic, repelling, abayashi et al., 1991). The composition of herbivore-induced or deterring properties (Bernasconi et al., 1998; De Moraes plant volatiles also can be influenced by various abiotic factors, et al., 2001; Kessler and Baldwin, 2001; Vancanneyt et al., including soil and air humidity, temperature, light intensity and 2001; Aharoni et al., 2003). They can also attract enemies of fertilization rate. Young corn plants, in response to herbivory attacking herbivores, such as parasitic wasps, flies or predatory by caterpillars, produced the highest level of induced volatiles mites, which can protect the signaling plant from further damage when kept in a relatively dry soil, about 60% relative humidity, (Dicke et al., 1990; Turlings et al., 1990; Vet and Dicke, 1992; temperatures between 22◦C and 27◦C with high light intensity, Pare and Tumlinson, 1997; Drukker et al., 2000; Kessler and and with continuous fertilization of the soil (Gouinguene and Baldwin, 2001). Moreover, some volatile compounds can me- Turlings, 2002). In spite of high variability of emitted volatiles diate both direct and indirect defenses, deterring lepidopteran and effect of abiotic conditions on their emission, predators oviposition and attracting herbivore enemies as was found in are able to distinguish infestations by its host from infesta- Nicotiana attenuata (Figure 1) (Kessler and Baldwin, 2001). tions by non-host closely related herbivore species. By exploit- The most common volatile signals involved in direct and in- ing herbivore-specific volatile emissions, the specialist parasitic direct defenses include metabolites of the lipoxygenase (LOX) wasp Cardiochiles nigriceps, for example, is able to distinguish pathway, the shikimic acid pathway, and products of the ter- between infestations by host, Heliothis virescens, and non-host, penoid pathway (monoterpenes, sesquiterpenes, homoterpenes) Helicoverpa zea,onphylogenetically distant species such as (see below) (Pichersky and Gershenzon, 2002). The particular maize, cotton, and tobacco (De Moraes et al., 1998). How- response, whether it is to attract a carnivore or repel an herbi- ever, elevated atmospheric CO2 concentration could weaken the vore, depends strongly on the level of plant induction (Horiuchi plant response induced by herbivore attack leading to a distur- et al., 2003; Heil, 2004; Gols et al., 2003) as well as on the bance of signaling to the third trophic level (Vuorinen et al.,

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 ability of the carnivores and parasitoids to discriminate differ- 2004). ent odor blends (Dicke, 1999a). It should, however, be noted that herbivore-induced volatiles are not always beneficial to damaged plants: in some instances, other nonspecific herbivores could be C. Role of Plant Volatiles in Tritrophic Interactions attracted by these volatile signals, resulting in increased attack The tritrophic plant-herbivore-carnivore interactions for the plant (Horiuchi et al., 2003; Bolter et al., 1997). (Figure 1), since first suggested in 1980 (Price et al., 1980), are The emitted volatiles generally induced by elicitors in the widely spread in the plant kingdom. To date this phenomenon herbivore saliva or oral secretion can be both plant and/or her- has been reported in more than 23 plant species in combination bivore species specific (De Moraes et al., 1998; (Takabayashi with a diverse range of herbivore and natural enemy species et al., 1995; Dicke, 1999a). The composition of different odor (Dicke, 1999b). One of the best-studied examples for this type blends also strongly depends on the type of damage, for ex- of tritrophic interaction includes interactions between lima bean ample, herbivore feeding or oviposition (Hilker and Meiners, plants (Phaseolus lunatus), herbivorous spider mites (Tetrany- 2002; Hilker et al., 2002). While some volatiles are constitu- chus urticae), and carnivorous mites (Phytoseiulus persimilis). tively emitted by undamaged healthy plants, the combined ac- Other systems are also very well characterized for this type of PLANT VOLATILES 421

tritrophic interactions, including small annual plants as well as D. Role of Plant Volatiles in Plant-Plant Interactions long-lived trees. Infestation of lima bean leaves by spider mites Volatiles released from herbivore-infested plants also medi- triggers the release of volatiles which attract the predatory mites ate plant-plant interactions and may induce the expression of that prey on the spider mites (Takabayashi and Dicke, 1996). defense genes and emission of volatiles in healthy leaves on the Similar to insect feeding activity, insect egg deposition can same plant or of neighboring unattacked plants, thus increasing induce emission of plant volatiles which attract egg parasitoids their attractiveness to carnivores and decreasing their suscepti- (Anderson and Alborn, 1999; Hilker and Meiners, 2002). This bility to the damaging herbivores (Figure 1) (Dicke et al., 1990; occurs soon after herbivore egg deposition, allowing the plant Arimura et al., 2002, 2004b; Ruther and Kleier, 2005). Using spi- to defend itself against pests before any damage has occurred, der mites (Tetranychus urticae) and predatory mites (Phytoseiu- i.e., before the larvae have hatched from the eggs (Hilker et al., lus persimilis), it has been shown that not only the attacked plant 2002). Moreover, herbivore- and wound-induced volatiles but also neighboring plants became more attractive to predatory released by the infested plant attract predators or parasitoids mites and less susceptible to spider mites (Bruin et al., 1992). of the damaging herbivores in plant-caterpillar-parasitoid Tetranychus urticae-infested lima bean leaf volatiles induce (Dicke and van Loon, 2000) and plant-caterpillar-predatory bug the expression of several genes encoding pathogenesis-related interactions (Kessler and Baldwin, 2001). (PR) proteins, lipoxygenase (LOX), phenylalanine ammonia- The high chemical diversity within the herbivore-induced lyase (PAL), and farnesyl pyrophosphate synthase (FPS) in the volatile mixtures complicated the identification of the com- neighboring lima bean leaves (Arimura et al., 2000a). This effi- pound(s) actually responsible for signaling herbivore enemies. cient induction of defense genes in plants exposed to herbivore- Earlier attempts to dissect the volatile signals emitted by induced volatiles is the result of activation of the multifunctional herbivore-damaged leaves of lima bean (Dicke et al., 1990) and signaling cascades involving ethylene and jasmonic acid (JA) maize (Turlings et al., 1991) failed to identify a specific com- (Arimura et al., 2002) (see below). pound responsible for enemy attraction, suggesting that mix- Release of herbivore-induced volatiles occurs both locally tures constitute the active signal. However, it was shown that the from damaged tissues and systemically from undamaged tis- application of individual plant volatiles, such as methyl salicy- sues and displays distinct temporal patterns (Schmelz et al., late and the C16-homoterpene 4,8,12-trimethyl-1,3(E),7(E),11- 2001; Arimura et al., 2004b). Nicotiana tabacum, for exam- tridecatetraene [(E,E)-TMTT], in behavioral experiments can ple, releases several herbivore-induced volatiles exclusively at attract predatory mites (De Boer and Dicke, 2004; De Boer night. These nocturnally emitted compounds repel female moths et al., 2004). Recent progress in the isolation of genes encoding (Heliothis virescens), which search for oviposition sites during enzymes responsible for the formation of plant volatile com- the night (De Moraes et al., 2001). Diurnal rhythm of volatile pounds allowed the use of genetic engineering as a novel tool emissions was shown from beet armyworm-damaged cotton to investigate the role of individual signaling compounds in me- leaves (Loughrin et al., 1994) and lima bean leaves infested with diating tritrophic interactions. The attraction of the predatory Spodoptera littoralis (Arimura et al., 2005). Similarly, local hy- mite Phytoseiulus persimilis to the sesquiterpene alcohol (3S)- brid poplar (Populus trichocarpa × deltoids) leaves attacked by (E)-nerolidol was recently demonstrated with transgenic Ara- forest tent caterpillar and systemic non-infested leaves released bidopsis overexpressing strawberry nerolidol synthase, a terpene very similar blends of volatiles consisting of (E)-β-ocimene synthase (TPS) (Kappers et al., 2005). These results suggested along with five or six other mono-, sesqui-, and homoterpene that (3S)-(E)-nerolidol is a component of the volatile signal that compounds with maximum emission during the light period attracts the predatory mites to spider mite-infested plants. Over- (Arimura et al., 2004b). Interestingly, (E)-β-ocimene could also expression in Arabidopsis thaliana of another terpene synthase act as a possible plant-to-plant signal in uninfested lima bean β Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 gene, the corn TPS10 gene, which forms (E)- -farnesene, (E)- plants thus up-regulating the signaling pathway of JA and ethy- α-bergamotene, and other herbivore-induced sesquiterpene hy- lene (Arimura et al., 2000, 2002). Other signaling molecules in- drocarbons released from maize upon herbivory by lepidopteran volved in intra- and inter-plant communication include methyl larvae, increased attractiveness of these transgenic plant to the jasmonate (MeJA) (Farmer, 2001), methyl salicylate (MeSA) parasitic wasps Cotesia marginiventris (Schnee et al., 2006). (Shulaev et al., 1997), and (Z)-3-hexenol (Farag et al., 2005; The wasps’ behavior in the olfactometer bioassays indicated that Ruther and Kleier, 2005). Exposure of intact maize plants to the mixture of TPS10 sesquiterpenes can be a genuine signal in (Z)-3-hexenol induces the emission of a volatile blend, which attracting these parasitoids to herbivore-damaged maize. These is typically released after caterpillar feeding and attracts natural examples show that once the biosynthetic genes for volatile for- enemies of the herbivores (Ruther and Kleier, 2005). mation are known, transgenic plants have a great potential to In addition to direct elicitation, exposure to volatile com- deliver individual volatiles or volatile mixtures for bioassays, pounds from attacked plants may lead to priming of plant de- which will allow the functional identification of potential volatile fense responses in the neighboring plants (Figure 1). Priming signals, either individually or in combinations, involved in in- by volatiles prepares the plant to respond more rapidly and teractions among organisms. intensively against subsequent attack by herbivorous insects 422 N. DUDAREVA ET AL.

(Engelberth et al., 2004; Kessler et al., 2006). Maize seedlings Recently, the sesquiterpene (E)-β-caryophyllene was identi- pre-exposed to individual GLV compounds such as (Z)-3- fied as a first root-insect–induced belowground plant signal that hexenal, (Z)-3-hexen-1-ol, and (Z)-3-hexenyl acetate, or to the strongly attracts an entomopathogenic nematode Heterorhab- blend of volatiles released from damaged plants, responded to ditis megidis under in situ laboratory and field conditions wounding and beet armyworm (Spodoptera exigua) caterpillar (Rasmann et al., 2005). Maize roots released this sesquiterpene regurgitant treatment with enhanced jasmonic acid production in response to feeding by larvae of the beetle Diabrotica vir- and an increased release of sesquiterpenes when compared with gifera virgifera,amaize pest that is currently invading Europe. plants that had been similarly damaged and treated but not ex- Afivefold higher nematode infection rate of D. v. virgifera larvae posed to the volatiles (Engelberth et al., 2004). Priming of native was found on a maize variety that produced the signal than on a Nicotiana attenuata by clipped sagebrush-released volatiles re- variety that did not, indicating the existence of communication sulted in lower total herbivore damage of tobacco plants and between plant roots and the third trophic level in the rhizosphere. in higher mortality rate of young Manduca sexta caterpillars Volatiles released by roots into the soil may also exhibit al- (Kessler et al., 2006). These examples show that priming by lelopathic activity by reducing the germination and growth of volatile compounds provides a different way of responding to competitive neighboring plants as was recently shown for 1.8- the threat of insect herbivory via the incomplete turning on of cineole (Figure 1) (Romagni et al., 2000; Singh et al., 2002). Its defense-related processes and reducing biochemical investment phytotoxic effect on seed germination and growth is probably in defenses in receiver plants until the onset of actual attack the result of an inhibition of both nuclear and organelle DNA (Engelberth et al., 2004; Kessler et al., 2006). While priming by synthesis in the root apical meristem (Nishida et al., 2005) and volatile compounds could be one of the mechanisms involved in changes in the root phospholipid and sterol composition (Zunino plant-plant signaling in nature, its underlying molecular mecha- and Zygadlo, 2005). nism and ecological relevance of the particular interactions still In contrast to aboveground interactions of plant with other remain to be determined. organisms, communication in the rhizosphere and belowground signaling are most likely limited to immediate neighbors and competitors and are restricted by the mobility of many soil or- E. Role of Plant Volatiles in Belowground Defense ganisms and the relatively low transport rates of root-emitted The induced emission of volatiles is not limited solely to compounds in the soil (Van der Putten et al., 2001; Baldwin aerial parts of a plant. Plants also release volatiles from their et al., 2002). roots with chemical and structural diversity comparable to those found in emissions from aerial plant organs. Similar to above- ground volatile compounds, root volatiles can contribute to a F. Role of Plant Volatiles in Abiotic Stresses belowground defense system by acting as antimicrobial or an- In addition to an involvement of plant volatiles in defense and tiherbivore substances, or by attracting enemies of root-feeding reproductive processes, volatile isoprenoids are able to protect herbivores (Figure 1). Infection of Arabidopsis roots with either plants from heat damage and allow them to maintain photosyn- compatible bacterial (Pseudomonas syringae strain DC3000) thetic rates thus enhancing plant thermotolerance at elevated or fungal (Alternaria brassicola) pathogens or root-feeding in- temperatures (Figure 1) (Sharkey et al., 2001, Loreto et al., sects (Diuraphis noxia) triggers the rapid emission of 1,8-cineole 1998; Copolovici et al., 2005; Penuelas et al., 2005; reviewed (Steeghs et al., 2004). 1,8-Cineole is an oxygenated monoter- in Sharkey and Yeh, 2001). Blocking of monoterpene emission pene with antimicrobial activity (Hammer et al., 2003; Pina-Vaz in Quercus ilex (L.) leaves with fosmidomycin, a specific in- et al., 2004), the formation of which is catalyzed in Arabidopsis hibitor of the plastidial isoprenoid biosynthetic pathway, re-

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 by a root-specific TPS (Chen et al., 2004; Ro et al., 2006). 1,8- sulted in the decrease of the photosynthetic thermotolerance. Cineole may also exhibit a toxic and deterrent effect on certain However, fumigation with the relatively low atmospheric con- insects (Tripathi et al., 2001) thus contributing to direct plant de- centrations of monoterpenes partly restored the heat stress re- fense. Volatilesemitted by roots of a coniferous plant Thuja occi- sistance (Copolovici et al., 2005). Similarly, fumigation with dentalis upon attack by weevil larvae Otiorhynchus sulcatus was exogenous isoprene of fosmidomycin-fed leaves of red oak shown to attract the entomopathogenic nematode Heterohabdi- (Quercus rubra) and kudzu (Pueraria lobata [Willd.] Ohwi.) in- tis megidis (Boff et al., 2001; van Tol et al., 2001). Similarly, creased the ability of photosynthetic apparatus to recover from the infestation of turnip roots with root-feeding larvae (Delia a brief high temperature exposure (Sharkey et al., 2001). These radicum) induced a systemic release of volatiles which attract the results suggest that heat tolerance of monoterpene- and isoprene- specialist parasitoid Trybliographa rapae (Neveu et al., 2002). nonemitting plants may be significantly improved by fumigation In the latter tritrophic system parasitoid-attracting volatiles were from the nearby growing emitting species during warm windless emitted not only by the root itself but also by undamaged leaves days in the Mediterranean canopies (Copolovici et al., 2005). of a damaged plant. Unfortunately, the nature of attractants in- Although the exact mechanism by which isoprene or monoter- volved in these belowground plant-mediated interactions is still penes confer thermotolerance is not known, it has been proposed unknown. that at high temperature thylakoid membranes become leaky PLANT VOLATILES 423

(Pastenes and Horton, 1996; Bukhov et al., 1999) and isoprene are released from the ad/absorbent fiber by thermal desorption could enhance hydrophobic interactions by residing in the thy- during gas chromatography. In contrast, solvent desorption often lakoid membrane for a short time. Isoprene may also enhance used in dynamic headspace allows multiple analyses of collected hydrophobic interactions within large membrane-bound protein samples in GC, GC/MS, and GC-EAD (gas chromatography- complexes (e.g., photosystem II), thus avoiding the fragmenta- electroantennogram detection). tion of these protein complexes (reviewed in Sharkey and Yeh, The necessity of real time detection and analysis of plant 2001). volatiles has prompted the use of proton-transfer-reaction Volatile isoprenoids may also serve as antioxidants protect- mass spectrometry (PTR-MS) and portable artificial noses in ing plants against a range of stresses including ozone-induced volatile research. While these techniques can provide new in- oxidative stress (Loreto et al., 2001; Loreto and Velikova, 2001) sights into the kinetics of plant volatile releases, they can not and singlet oxygen accumulation (Affek and Yakir, 2002). When distinguish between different compounds of the same mass monoterpene emission was inhibited by fosmidomycin, Quer- or retention time respectively (D’Alessandro and Turlings, cus ilex (L.) leaves became susceptible to the ozone resulting in 2006). a rapid and significant reduction of photosynthesis, accumula- tion of reactive oxygen species such as hydrogen peroxide, and IV. BIOSYNTHESIS OF PLANT VOLATILES membrane peroxidation monitored by increasing concentrations Plant volatiles are low-molecular-weight compounds (below of malonyldialdehyde (Loreto et al., 2004). All these symp- 300 Da) and can be divided into three major classes, terpenoids toms have been also observed following inhibition of isoprene (also known as isoprenoids), phenylpropanoids/benzenoids, and biosynthesis in isoprene-emitting plants (Loreto and Velikova, fatty acid derivatives. In addition, volatiles derived from amino 2001) showing the importance of isoprene emission in protect- acids are often present in scent and aromas released from flowers ing leaves against oxidative damage. Although the mechanism and fruits. Although volatile compounds are synthesized via a of isoprene protection of plants against oxidative stress still re- few major biochemical pathways (Figure 2), various forms of mains unclear, it has been shown that isoprene may have a direct enzymatic modifications such as hydroxylations, acetylations, ozone quenching property rather than inducing resistance at the and methylations, add to the diversity of emitted volatiles by membrane level (Loreto et al., 2001). increasing their volatility at the final step of their formation (Dudareva et al., 2004; Gang, 2005). III. ANALYSIS OF PLANT VOLATILES The vital functions of volatile compounds in the plant life cycle and consequently the increasing scientific interest in A. Terpenoids biochemistry, physiology, and ecology of these metabolites re- The terpenoids compose the largest class of plant secondary sulted in the development of sensitive methods for headspace metabolites with many volatile representatives. Hemiterpenes sampling and analysis of volatiles. These methods and their ad- (C5), many monoterpenes (C10), sesquiterpenes (C15), homoter- vantages and disadvantages are thoroughly discussed in recent penes (C11and C16), and some diterpenes (C20)haveahigh vapor reviews (Tholl et al., 2006; D’Alessandro and Turlings, 2006). pressure allowing their release into the atmosphere (Figure 3). In short, methods including static and dynamic collection of All terpenoids originate from the universal five carbon pre- volatiles on an adsorbent followed by thermal or solvent des- cursors, isopentenyl diphosphate (IPP) and its allylic isomer orption and chromatographic separation and mass spectrometric dimethylallyl diphosphate (DMAPP), which are derived from analysis by gas chromatography/mass spectrometry (GC/MS) two alternative pathways (Figure 2). In the cytosol, IPP is synthe- are widely used nowadays for identification of volatile com- sized from three molecules of acetyl-CoA (Qureshi and Porter, 1981; Newman and Chappell, 1999) by the classical mevalonic Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 pounds released by plants (D’Alessandro and Turlings, 2006; Tholl et al., 2006). Depending on the goal of a particular ex- acid (MVA) pathway (McCaskill and Croteau, 1995), while periment, volatiles could be collected from an entire intact plant in plastids, it is derived from pyruvate and glyceraldehyde- or parts of an intact plant (in situ) or alternatively from de- 3-phosphate via the methyl-erythritol-phosphate (MEP) path- tached plant parts (ex situ) enclosed in an air-tight container. way (Eisenreich et al., 1998; Lichtenthaler, 1999; Rohmer, While in static headspace analysis there is no air circulation in 1999) discovered in the last decade (for review, see Rodriguez- the container, in dynamic sampling, air is continuously recy- Concepcion and Boronat, 2002). Although the subcellular cled (“closed-loop stripping”) or constantly taken up from the compartmentation of MVA and MEP pathways allows them to outside, passed over the plant sample and through an absorbent operate independently, metabolic “crosstalk” between these two trap (pull and push-pull systems) (Tholl et al., 2006). The solid pathways mediated by specific metabolite transporters (Bick and phase microextraction (SPME) technique is commonly used in Lange, 2003) was recently discovered (Schuhr et al., 2003), par- static sampling for qualitative and semi-quantitative analysis of ticularly in the direction from plastids to cytosol (Hemmerlin plant volatiles with detection limits in the ppbv (parts per billion et al., 2003; Laule et al., 2003; Dudareva et al., 2005). by volume) (Tholl et al., 2006). This technique allows a one- In plastids, DMAPP generated from the MEP pathway is used time analysis of collected samples since SPME-trapped volatiles by isoprene synthases (Silver and Fall, 1995; Schnitzler et al., 424 N. DUDAREVA ET AL.

FIG. 2. Metabolic pathways leading to the biosynthesis of various volatile compounds in plants. Pathway names are italicized, volatile compounds areinbold and enzymes are boxed. Abbreviations: Acetyl-CoA, acetyl coenzyme-A; AOS, allene oxide synthase; DAHP, 3-deoxy-D-arabino-heptulosonate 7-phosphate; DHS, 3-dehydroshikimic acid; DMAPP, dimethylallyl diphosphate; DXP, 1-deoxy-D-xylulose 5-phosphate; DXR, DXP reductoisomerase; DXS, DXP synthase; Ery4P, erythrose 4-phosphate; F6P, fructose 6-phosphate; FPP, farnesyl diphosphate; FPPS, FPP synthase; GA-3P, glyceraldehyde-3-phosphate; G6P, glucose 6-phosphate; GGPP, geranylgeranyl diphosphate; GGPPS, GGPP synthase; GPP, geranyl diphosphate; GPPS, GPP synthase; HMG-CoA, 3-hydroxy-3-methylglutaryl-CoA; HMGR, 3-hydroxy-3-methylglutaryl-CoA reductase; HPL, fatty acid hydroperoxide lyase; IGL, indole-3-glycerol phosphate lyase; Indole-3GP, indole 3-glycerol phosphate; IPP, isopentenyl diphosphate; JMT, jasmonic acid carboxyl methyl transferase; LOX, lipoxygenase; MEP, 2-C-methyl-D-erythritol 4-phosphate; MVA, mevalonate; PAL, phenylalanine ammonia lyase; PEP, phosphoenolpyruvate; Phe, phenylalanine.

1996; Miller et al., 2001) for isoprene formation (Schwender (Poulter and Rilling, 1981; Ogura and Koyama, 1998). The con- et al., 1997; Rodriguez-Concepci´on and Boronat, 2002). The densation of one molecule of DMAPP with three molecules Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 isolation and characterization of isoprene synthases from kudzu of IPP by the action of geranylgeranyl pyrophosphate synthase and aspen suggested that the conformation of their active sites (GGPPS) yields GGPP, the C20 diphosphate precursor of diter- with two phenylalanine residues at opposite ends confers speci- penes (Ogura and Koyama, 1998; Koyama and Ogura, 1999). ficity for the five-carbon substrate rather than precursors of the Following the formation of the acyclic precursors GPP, FPP, larger isoprenoids (Sharkey et al., 2005). In the cytosol and in and GGPP, a wide range of structurally diverse cyclic and plastids, IPP and DMAPP are used by prenyltransferases to pro- acyclic monoterpenes, sesquiterpenes, and diterpenes is gen- duce prenyl diphosphates. In cytosol, the condensation of two erated through the action of a large family of enzymes known molecules of IPP and one molecule of DMAPP catalyzed by as terpene synthases/cyclases (TPSs) (Cane, 1999; Wise and the enzyme farnesyl pyrophosphate synthase (FPPS) results in Croteau, 1999). One of the most outstanding properties of these the formation of FPP (C15), the natural precursor of sesquiter- enzymes is their proclivity for making multiple products from penes (McGarvey and Croteau, 1995). In plastids, a head-to- a single prenyl diphosphate substrate (Bohlmann et al., 1998; tail condensation of one molecule of IPP and one molecule of Steele et al., 1998; Martin et al., 2004). For example, two DMAPP catalyzed by geranyl pyrophosphate synthase (GPPS) sesquiterpene synthases were found to be responsible for a mix- forms GPP (C10), the universal precursor of all the monoterpenes ture of 20 sesquiterpenes found in the Arabidopsis floral volatile PLANT VOLATILES 425 Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011

FIG. 3. Representative structures of different volatile isoprenoids, amino-acid and fatty acid derivatives released from plants.

blend (Tholl et al., 2005). Also, a single terpene synthase (TPS1) pounds emitted by herbivore-damaged maize plants. Arabidop- produces three acyclic sesquiterpenes, (E)-β-farnesene, (3R)- sis myrcene/ocimene synthase converts GPP into myrcene (56% (E)-nerolidol, and (E,E)-farnesol (Schnee et al., 2002), out of of total hydrocarbon product), (E)-β-ocimene (20%), and small which (E)-β-farnesene and a metabolite of (E)-nerolidol, (3E)- amounts of cyclic monoterpenes (each <5%) (Bohlmann et al., 4,8-dimethyl-1,3,7-nonatriene (DMNT), are prominent com- 2000) while a monoterpene synthase from Perilla frutescens 426 N. DUDAREVA ET AL.

FIG. 4. Phylogenetic tree illustrating the relationship of various terpene synthases. Subfamilies are divided based on cluster analysis (Bohlmann et al., 1998; Aubourg et al., 2002). Sequence analysis was performed using CLUSTAL X, and the nearest neighbor-joining method was used to create trees. Only a subset of the known plant TPS is shown in this tree.

produces myrcene (53.8%), sabinene (20.9%), linalool (19.8%) b comprises angiosperm monoterpene synthases that contain and limonene (5.5%) (Hosoi et al., 2004). However, not all ter- the RRx8W motif (Bohlmann et al., 1998). TPS-c and TPS-e pene synthases make multiple products. Two specialized single subfamilies are represented by the angiosperm copalyl diphos- product monoterpene synthases were shown to be responsible for phate synthase and kaurene synthase, respectively, (Bohlmann the biosynthesis of myrcene and (E)-β-ocimene, the two dom- et al.,1998), diterpene synthases involved in early steps of gib- inant isoprenoids of snapdragon floral scent (Dudareva et al., berellin biosynthesis and secondary metabolism (MacMillan

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 2003). All terpenoid synthases require a divalent metal ion as and Beale, 1999). TPS-d includes gymnosperm monoterpene, the only cofactor for catalysis and the multiple enzymatic prod- sesquiterpene and diterpene synthases (Martin et al., 2004). ucts are the result of the combination of a wide array of pos- While linalool synthase from Clarkia breweri represents the sible carbocationic intermediates and their multiple metabolic only member of TPS-f subfamily, linalool synthase from Ara- fates (Wise and Croteau, 1999; Cane, 1999; Davis and Croteau, bidopsis along with snapdragon myrcene and (E)-β-ocimene 2000). synthases and strawberry nerolidol synthase belong to a newly To date more than 100 terpene synthases have been iso- defined TPS-g subfamily (Dudareva et al., 2003). Members of lated and characterized from different plant species. They be- this subfamily lack the RRx8W motif that is a distinctive fea- long to the terpene synthase (TPS) gene family, which has ture of all functionally characterized monoterpene synthases of been divided into seven subfamilies (designated TPS-a through TPS-b and TPS-d groups (Dudareva et al., 2003; Aharoni et al. TPS-g) based on sequence relatedness, functional assessment, 2004). Although it is possible to assign new TPS genes into one and gene architecture (Figure 4) (Bohlmann et al., 1998; Trapp of the three major classes of terpene synthases (mono-, sesqui- and Croteau, 2001; Aubourg et al., 2002; Martin et al., 2004). and diterpene synthases) based on the sequence comparison, The TPS-a subfamily consists of angiosperm sesquiterpene syn- analysis of active recombinant enzyme is required to know its thases and a diterpene synthase, casbene synthase, while TPS- exact biochemical function (Bohlmann et al., 1998). PLANT VOLATILES 427

Many of the terpene volatiles are direct products of terpene and constitute another large class of plant volatiles (Figure 3). synthases, while others are formed through alterations of the They are derived from C18 unsaturated fatty acids including primary terpene skeletons made by TPSs by hydroxylation, de- linoleic acid or linolenic acid, which undergo dioxygenation in hydrogenation, acylation, and other reaction types (Dudareva a reaction catalyzed by lipoxygenases (LOX) (Figure 2) (Feuss- et al., 2004). 3-Hydroxylation of limonene by a P450 enzyme ner and Wasternack, 2002). These enzymes, comprising a large yields the formation of trans-isopiperitenol, a volatile compound family of nonheme iron containing fatty acid dioxygenases, found in mint (Lupien et al., 1999), while 6-hydroxylation of can catalyze the oxygenation of polyenoic fatty acids at C9 or limonene by another P450 enzyme results in the formation of C13 positions (the enzyme is then referred to as 9-LOX or 13- trans-carveol, which undergoes further oxidation by nonspe- LOX, respectively), yielding two groups of compounds, the 9- cific dehydrogenase to form carvone, a major aroma volatile hydroperoxy and the 13-hydroperoxy derivatives of polyenoic of caraway fruits (Bouwmeester et al., 1998, 1999). Another fatty acids. These derivatives can be further metabolized by an monoterpene alcohol, geraniol, was also found to be converted array of enzymes, including allene oxide synthase (AOS) and to the corresponding aldehyde by dehydrogenases in the glands hydroperoxyde lyase (HPL), which represent two branches of of sweet basil (Iijima et al., 2006). On the other hand, an acety- the lipoxygenase pathway yielding volatile compounds. In the lation of geraniol by acetyltransferase generates geranyl acetate AOS branch of the lipoxygenase pathway, 13-hydroxyperoxy (Shalit et al., 2003), a volatile compound found in the scent linolenic acid is converted to 12,13-epoxy octadecatrienoic acid of many plant species (Bauer et al., 2001). Recently, reduction by AOS (Feussner and Wasternack, 2002). A series of subse- of geraniol to (S)-citronellol, the precursor of the potent odor- quent enzymatic reactions leads to the formation of jasmonic ant rose oxide, was confirmed enzymatically in grape mesocarp acid, which can in turn be converted to the volatile ester, methyl (Luan et al., 2005). jasmonate, by the enzyme jasmonic acid carboxyl methyltrans- Modification reactions are also involved in the formation of ferase (Figure 2) (Seo et al., 2001; Song et al., 2005). terpenoids with irregular acyclic C16 and C11 carbon skeletons, In the HPL branch of the LOX pathway, the oxidative cleav- so called homoterpenes, which are mainly emitted from in- age of hydroperoxy fatty acids through the action of HPL leads jured tissues. Although the exact biosynthetic routes to homoter- to the formation of short chain C6-orC9-volatile aldehydes penes, (E,E)-TMTT (C16) and (E)-DMNT (C11) still remain (e.g., 3-hexenal or 3,6-nonadienal) and the corresponding C12- unclear, it is believed that they are derived from geranyl-linalool or C9-ω fatty acids (e.g., 12-oxo-dodecenoic acid or 9-oxo- (C20) and (3S)-(E)-nerolidol (C15), respectively, by oxidative nonanoic acid) (Figure 2). HPLs belong to the CYP74 family of degradation possibly catalyzed by cytochrome P450 enzymes cytochrome P450 enzymes (Matsui et al., 1996) with different (G¨abler et al., 1991; Donath and Boland, 1994; Degenhardt and substrate specificity: some HPLs act either specifically on 13- Gershenzon, 2000). Apart from homoterpenes, plants produce hydroperoxides (13-HPLs) (Howe et al., 2000; Kandzia et al., other irregular volatile terpenoids with carbon skeletons rang- 2003; Fukushige and Hildebrand, 2005) or on 9-hydroperoxides ing from C8 to C18 derived from carotenoids (C40) (Figure 2) (9-HPLs) (Kim and Grosch, 1981; Mita et al., 2005), other HPLs (Knudsen and Gershenzon, 2006; Auldridge et al., 2006b). β- accept both 9- or 13-hydroperoxides as substrates (9/13-HPLs) ionone, β-damascenone or dihydroactinidiolide are examples of (Matsui et al., 2000) HPL C6-aldehyde products can be further volatile carotenoid derivatives which can be found in the scent converted to their isomers by spontaneous rearrangement or of flowers such as Rosa hybrida, Osmanthus fragrans or Freesia by alkenal isomerases, or they can be reduced to alcohols by hybrida,orinthe aroma of fruits and vegetables such as Aver- the action of alcohol dehydrogenases (ADH) (Grechkin, 1998; rhoa carambola (starfruit) or Lycopersicon esculentum (tomato) Prestage et al., 1999; Akacha et al., 2005). (Figure 3) (Kaiser, 2002; Winterhalter and Rouseff, 2002). In

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 general, the biosynthesis of carotenoid-derived volatile com- pounds occurs via three steps: an initial dioxygenase cleavage C. Phenylpropanoids/Benzenoids yielding apocarotenoids, followed by enzymatic transformations Phenylpropanoids and benzenoids derived from L- of these apocarotenoids leading to the formation of polar aroma phenylalanine constitute a large class of structurally diverse precursors, and finally acid-catalyzed conversions of these pre- volatile compounds involved in plant reproduction and defense cursors to volatile compounds (Winterhalter and Rouseff, 2002). (Figure 5). Unlike terpenoids, for which extensive information However, in some cases a volatile product is the result of the is available about their biosynthesis (Wise et al., 1998; Chappell, initial dioxygenase cleavage step, as was shown for β-ionone 1995; Bohlmann et al., 1998), little is known about the entire bio- in Arabidopsis (Schwartz et al., 2001, 2004; Auldridge et al., chemical pathways leading to the formation of phenylpropenes 2006a), tomato and petunia (Simkin et al., 2004a, 2004b). and their derivatives. In the first step of phenypropanoid biosyn- thesis, L-phenylalanine (Phe) is converted to trans-cinnamic acid in a reaction catalyzed by L-phenylalanine ammonia-lyase B. Volatile Fatty Acid Derivatives (PAL) (Figure 2). In the next steps, shared with the lignin/lignan Volatile fatty acid derivatives such as trans-2-hexenal, cis-3- biosynthetic pathway up to the phenylpropenol (monolignol) hexenol and methyl jasmonate are abundant in the plant kingdom stage, a variety of hydroxycinnamic acids, aldehydes and 428 N. DUDAREVA ET AL.

FIG. 5. Representative structures of different volatile phenylpropanoids/benzenoids released from plants.

alcohols are formed from trans-cinnamic acid via a series of ogous to that underlying β-oxidation of fatty acids and proceeds hydroxylation and methylation reactions, which occur at the through the formation of four CoA-ester intermediates. The level of hydroxycinnamic acid esters and their corresponding CoA-independent–non-β-oxidative pathway involves hydration aldehydes and alcohols (Humphreys and Chapple, 2002). of the free trans-cinnamic acid to 3-hydroxy-3-phenylpropionic Some of these intermediates could be converted to volatile acid and side chain degradation via a reverse aldol reaction with compounds as was shown in basil and petunia for eugenol and formation of benzaldehyde, which is then oxidized to benzoic isoeugenol, which are formed from coniferyl acetate in reaction acid by an NADP+-dependent aldehyde dehydrogenase. Recent catalyzed by eugenol synthase and isoeugenol synthase, in vivo stable isotope labeling and computer-assisted metabolic respectively (Koeduka et al., 2006). Eugenol and isoeugenol flux analysis revealed that both the CoA-dependent–β-oxidative β

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 could undergo further methylation to yield methyleugenol and and CoA-independent–non- -oxidative pathways are involved isomethyleugenol. Enzymes catalyzing these O-methylations in the formation of benzenoid compounds in Petunia hybrida have been isolated and characterized from sweet basil (Gang (Boatright et al., 2004). et al., 2002) and Clarkia breweri (Wang et al., 1997). Similarly, In contrast, the biosynthesis of volatile C6-C2 compounds, methylchavicol could be produced from chavicol by chavicol such as phenylacetaldehyde and phenylethanol, does not oc- O-methyltransferase (Gang et al., 2002), however, the exact cur via trans-cinnamic acid and is in competition with trans- biochemical route to chavicol still remains unclear. cinnamic acid synthesis for Phe utilization (Boatright et al., Benzenoid compounds also originate from trans-cinnamic 2004). Recently, it has been shown that in petunia phenylac- acid as a side branch of the general phenylpropanoid pathway etaldehyde is formed directly from Phe via an unusual combined (Figures 2 and 5). Their synthesis requires the shortening of decarboxylation-amine oxidation reaction catalyzed by pheny- trans-cinnamic side chain by a C2 unit, for which several routes lacetaldehyde synthase (Kaminaga et al., 2006). On the other have been proposed. The side chain shortening could occur hand, in tomato its biosynthesis occurs via two separate steps, the via a CoA-dependent–β-oxidative pathway, CoA-independent– first step involving decarboxylation of Phe to phenylethylamine non-β-oxidative pathway, or via the combination of these two (Tieman et al., 2006). Moreover, it has been suggested that in mechanisms. The CoA-dependent β-oxidative pathway is anal- tomato phenylacetaldehyde is converted to 2-phenylethanol by PLANT VOLATILES 429

2-phenylacetaldehyde reductase (Tieman et al., 2006). However, alcohol acetyltransferase (Dudareva et al., 1998), Clarkia feeding experiments with deuterium-labeled Phe suggested that benzoyl-CoA:benzyl alcohol benzoyltransferase (D’Auria et al., in petunia phenylacetaldehyde is not the only precursor for 2- 2002), petunia benzoyl-CoA:benzyl alcohol/phenylethanol phenylethanol and the major flux to the latter goes through a benzoyltransferase (Boatright et al., 2004), melon AATs different route, possibly through phenylpyruvate and phenyllac- (Yahyaoui et al., 2002; El-Sharkawy et al., 2005), apple AAT tic acid as has been recently reported in rose flowers (Watanabe (Defilippi et al., 2005), wild strawberry and banana AATs et al., 2002; Boatright et al., 2004). (Beekwilder et al., 2004). Although we still know very little about the enzymes and genes responsible for the metabolic steps leading to phenyl- propanoids/benzenoids, significant progress has been made in V. REGULATION OF PLANT VOLATILE EMISSION the discovery of common modifications, such as hydroxylation, Our understanding of the regulation of plant volatile emis- acetylation, and methylation of downstream products (Dudareva sion and signal transduction pathways involved is still largely in et al., 2004). its infancy with probably less than 10% of genes responsible for volatile biosynthesis identified to date. Nevertheless, it has been shown that plant volatiles are synthesized de novo in undam- D. Amino-Acid Volatile Derivatives aged or damaged tissues from which they are emitted, and their While volatile phenylpropanoids/benzenoids originate from production is both spatially and temporally regulated (Dudareva the amino acid Phe, other amino acids, such as alanine, valine, et al., 1996; Par´e and Tumlinson, 1997). Of various plant or- leucine, isoleucine, and methionine, serve as precursors for a gans, flowers in scented species and fruits produce the most di- wealth of plant volatiles including aldehydes, alcohols, esters, verse and the highest amount of volatile compounds, which peak acids, and nitrogen- and sulfur-containing volatiles (Figure 3). when flowers are ready for pollination and fruits are fully ripe. In Most of the information available to date on the biosynthesis some plant species, conifers for example, the most diverse mix- of amino acid-derived volatiles in plants is based on precursor tures and large quantities of terpenoid volatiles are emitted from feeding experiments with radio-labeled, stable-isotope-labeled, foliage and stems (Keeling and Bohlmann, 2006). In general, or unlabeled precursors. The general scheme of biosynthesis the biosynthesis of volatiles occurs in epidermal cells of plant is thought to proceed in a similar way as that in bacteria or tissues (e.g., petals or roots) allowing an easy escape into the yeast, where these pathways have been studied more exten- atmosphere (Kolosova et al., 2001b; Scalliet et al., 2006; Effmert sively (Dickinson et al., 1998, 2000; Beck et al., 2002; Tavaria et al., 2006) or rhizosphere (Chen et al., 2004). In vegetative or- et al., 2002). Amino acids can undergo an initial deamination gans, plant volatiles may be synthesized in surface glandular or transamination leading to the formation of the correspond- trichomes (Pichersky et al., 2006) and then secreted from the ing α-keto acid. Subsequent decarboxylation followed by re- cells and stored in a sac created by the extension of the cuti- ductions, oxidations and/or esterifications give rise to aldehy- cle (Gang et al., 2001; Turner et al., 2000). Terpenoid volatiles des, acids, alcohols and esters (Reineccius, 2006). Branched- in conifers are produced in specialized anatomical structures, chain volatile alcohols, aldehydes and esters in fruits such as resin cells or ducts, that are located within other tissues of stem banana, apple, strawberry and tomato arise from the branched- and needles (Franceschi et al., 2005; Keeling and Bohlmann; chain amino acids leucine, isoleucine and valine (Hansen and 2006) from which they can be released upon disruption by me- Poll, 1993; Rowan et al., 1996; Wyllie and Fellman, 2000; chanical wounding or herbivory (Miller et al., 2005). The exact Perez et al., 2002; Goff and Klee, 2006). These amino acids mechanisms of volatile transport from the site of biosynthe- can also be the precursors of acyl-CoAs, which are used in sis to the atmosphere is still an open question. However, it has

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 alcohol esterification reactions catalyzed by alcohol acyl- been proposed to involve four steps: i) trafficking within the transferases (AATs). Indeed, isoleucine could give rise to cell, ii) transport across the plasma membrane and cell wall; iii) 3-methylbutanol and 2-methylbutyryl-CoA, both used in an transfer through the cuticle, and iv) evaporation at the surface of esterification reaction to yield the ester 3-methylbutyl 2- the cuticle (reviewed in Jetter, 2006). methylbutanoate in banana (Wyllie and Fellman, 2000). Me- The formation of volatiles follows similar developmental pat- thionine could be the precursor of sulphur-containing volatiles terns in all of the plant organs examined, increasing during the such as dimethyldisulfide and volatile thioesters (Wyllie and early stages of organ development (when leaves are young and Leach, 1992; Wyllie et al., 1995). In strawberry, it has been not fully expended, fruits are not yet mature, or when flowers suggested that alanine serves as a precursor for volatile ethyl are ready for pollination) and then either remaining relatively esters (Perez et al., 1992), which can be produced by the constant or decreasing over the organs’ life span (Bouwmeester strawberry alcohol acyltransferase SAAT (Aharoni et al., 2000; et al., 1998; Dudareva and Pichersky, 2000; Gershenzon et al., Beekwilder et al., 2004). A number of such alcohol acyltrans- 2000). The concurrent temporal changes in activities of enzymes ferases, catalyzing the formation of volatile esters from alcohols responsible for the final steps of volatile formation, enzyme and acyl-CoAs derived from amino acids, have been isolated protein levels, and the expression of corresponding structural in flowers and fruits. They include Clarkia acetyl-CoA:benzyl genes suggest that the developmental biosynthesis of volatiles 430 N. DUDAREVA ET AL.

is regulated largely at the level of gene expression (Dudareva step of their biosynthesis is elevated but also the flux through the et al., 1996; McConkey et al., 2000). Transcriptional regulation pathways leading to their immediate precursors is upregulated. also contributes to the spatial (local and systemic) and temporal Indeed, herbivore infestation induces the expression of genes herbivore-induced release of volatiles (Arimura et al., 2004a), involved in terpenoid biosynthesis including FPP and GGPP levels of which positively correlate with induced transcript lev- synthases in poplar and tomato, respectively (Arimura et al., els of the corresponding genes, as was shown in corn (Shen et al., 2004a; Kant et al., 2004). The role of substrate in the regulation 2000; Schnee et al., 2002), poplar (Arimura et al., 2004a), Lotus of the biosynthesis of floral or vegetative volatile compounds japonicus (Arimura et al., 2004b), and Sitka spruce (Miller et al., was also recently confirmed via metabolic engineering (Lucker 2005). Similarly, exposure of undamaged plants to volatiles from et al., 2001; Vancanneyt et al., 2001; Guterman et al., 2006). an herbivore-infested neighbor upregulates the expression of Emission of volatiles from flowers, undamaged and herbi- genes involved in defense metabolism (Arimura et al., 2000). vore attacked leaves often exhibit distinct diurnal or nocturnal This upregulation could explain, at least in part, a several hours patterns (De Moraes et al., 2001; Lerdau and Gray, 2003; Martin delay between the beginning of herbivore damage and the release et al., 2003; Arimura et al., 2004a) and can be controlled by a cir- of induced volatiles. When volatile compounds are released im- cadian clock (Kolosova et al., 2001a; Lu et al., 2002). While the mediately after herbivore damage, they arise from stored pools involvement of substrate availability in the regulation of rhyth- (Pare and Tumlinson, 1997). mic emission of floral volatiles and isoprene was shown for some In general, more than one biochemical pathway is often species (Kolosova et al., 2001a; Br¨uggemann and Schnitzler, responsible for a blend of volatile compounds released from 2002) little information is known about the molecular mecha- agiven plant tissue under different physiological conditions. nisms responsible for inducible rhythmic emission of vegetative A comparative analysis of the regulation of benzenoid and volatiles. monoterpene emission in snapdragon flowers revealed that the Environmental factors such as light intensity, atmospheric orchestrated emission of phenylpropanoid and isoprenoid com- CO2 concentration, temperature, relative humidity, and nutrient pounds is regulated upstream of individual metabolic pathways status can greatly influence the emission of volatiles (Staudt and and includes the coordinated expression of genes that encode en- Bertin, 1998; Gershenzon et al., 2000; Gouinguene and Turlings, zymes involved in the final steps of scent biosynthesis (Dudareva 2002). In addition, in flowers, pollination leads to a decrease et al., 2000, 2003). Recent use of microarray analysis in the in scent emission, which begins after successful fertilization investigation of plant-insect interactions also showed orches- (Negre et al., 2003). Ethylene was found to play a major role in trated complex transcriptional changes in the expression of genes this process through the downregulation of expression of scent involved in volatile emissions in plant defense (Hermsmeier biosynthetic genes (Negre et al., 2003; Underwood et al., 2005). et al., 2001; Kant et al., 2004; Ralph et al., 2006). Linking However, in contrast to vegetative defense-inducible emission the transcriptome information with volatile profiling could lead where signal transduction cascades are under extensive inves- to the discovery of new genes involved in the regulation and tigation, the exact signaling mechanisms regulating volatile formation of volatile compounds. Such an approach was suc- emission fluctuations due to the environmental or physiologi- cessfully used for the isolation of (E,E)-α-farnesene and (E)- cal factors listed above still await further examination. β-caryophyllene synthases responsible for the synthesis of im- portant constituents of the volatile blend emitted by cucumber after spider mite infestation (Mercke et al., 2004). Similarly, this VI. SIGNAL TRANSDUCTION PATHWAYS approach resulted in the isolation of the first transcription fac- REGULATING VOLATILE EMISSION tor ODORANT1 involved in the regulation of the production of Recent advances in the field of plant volatile metabolism have

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 scent volatiles in P. hybrida cv Mitchell (Verdonk et al., 2005). uncovered the complexity of formation of volatile compounds However, transcription factors that regulate multiple biosyn- and revealed that the intracellular signaling network involved thetic pathways leading to herbivore-induced volatile emission in the modulation of their formation still remains elusive. The have not yet been discovered. available data to date about signaling pathways that lead to the The level of the enzyme responsible for the final step of the herbivore-induced indirect plant defenses are summarized in a biosynthesis of a particular volatile is not the only limiting fac- recent review by Arimura et al. (2005). While there is no in- tor. The amount and/or type of product formed, in some cases, formation about activation of signal transduction cascades by is determined by the availability of substrates for the final re- volatile compounds in plant-plant interactions, it has been shown action, especially for enzymes with broad substrate specificity that upon feeding, herbivores introduce into a plant a variety of (e.g., some carboxyl methyltransferases and acyltransferases) elicitors including lytic enzymes (Mattiacci et al.,1995; Musser (Effmert et al., 2005; D’Auria, 2006). The level of available sub- et al., 2002) or fatty-acid-amino-acid conjugates (FAC) (Alborn strate (DMAPP) for isoprene synthase is also involved in the con- et al., 1997; Pohnert et al., 1999; Halitschke et al., 2001), which trol of the rate of leaf isoprene emission in oak (Br¨uggemann and are present in the insect oral secretions and regurgitants. These Schnitzler, 2002). In the case of herbivore-induced volatile for- elicitors interact with the plasma membrane of plant cells at the mation, not only the expression of genes responsible for the final site of damage and lead to a strong Ca2+-dependent membrane PLANT VOLATILES 431

potential depolarization in the bite zone with a transient mem- response specificity (Kessler and Baldwin, 2002). The “delicate” brane potential hyperpolarization in the close vicinity followed balance between JA and SA may be involved in control and co- by a constant depolarization throughout the entire attacked leaf ordination of induced defenses leading to emission of character- (Maffei et al., 2004). Mechanical damage alone causes mem- istic blends of herbivore-induced volatiles from attacked plants brane potential depolarization yet without the involvement of (Engelberth et al., 2001). By discriminating insect biting from Ca2+ influx and leads to the activation of mitogen-activated mechanical wounding, both pathways might also prevent unnec- protein kinases (MAPK) after a single mechanical wounding essary defense activation (Arimuara et al., 2005). However, the event (Seo et al., 1995; Zhang and Klessig, 1998). In tobacco, fundamental differences between signaling pathways recruited it has been suggested that an MAPK takes part in the wound- after mechanical wounding or herbivory still remain mostly un- induced signal transduction by upregulation of expression of known. In the past, experiments addressing this issue used a plastidial ω-3 fatty acid desaturase, which converts cell plasma single mechanical wounding event as a control for herbivore membrane linoleic acid to linolenic acid, a precursor of jasmonic feeding, which did not reflect the extent of damaged tissue and acid (JA) (Kodama et al., 2000). Similarly, in tomato and Ara- the length of attack, leading to the conclusion that mechanical bidopsis, wounding by attacking herbivores could induce phos- wounding alone was not sufficient for the induction of herbivore- pholipases, which mediate the release of linolenic acid from induced volatile profiles. However, a more realistic continuous cell membrane phospholipids (Narv´aez-V´asquez et al., 1999; mechanical damage by a recently developed mechanical cater- Wang et al., 2000). The release of linolenic acid and subsequent pillar, MecWorm, which mimicked real insect damage, induced activation of the octadecanoid pathway results in JA increase, virtually the same volatile blend as from actual herbivore feeding which alters the expression of herbivore-responsive genes and although with quantitative differences. This continuous mechan- triggers the accumulation and release of secondary metabolites, ical damage therefore represents a valuable model to dissect the including volatile terpenoids (Schittko et al., 2000; Halitschke role and impact of wounding versus elicitors on herbivore in- and Baldwin, 2003; Halitschke et al., 2001). duced signal transduction pathways in the future (Mith¨ofer et al., The activation of JA biosynthesis alone cannot account for 2005). The availability and/or generation of transgenic plants si- all wounding or herbivore induced responses. Ethylene and sal- lenced in volatile biosynthetic pathways (“mute” emitters) and icylic acid (SA) represent other well-known players involved in signal transduction pathways (“deaf” receivers), as was recently signaling cascades. Herbivore infestation, artificial wounding, used in Nicotiana attenuata (Paschold et al., 2006), will provide and exposure of plant to herbivore-induced volatiles activate apowerful tool to determine key compounds and signaling cas- ethylene biosynthesis and its emission (O’Donnell et al., 1996; cades involved in plant-plant interactions. Arimura et al., 2002). Similarly, the induced responses to herbi- vore or pathogen attack require elevated levels of SA (Bi et al., 1997; Engelberth et al., 2001; Ozawa et al., 2000; Durner et al., VII. METABOLIC ENGINEERING OF VOLATILE 1997). While SA could act antagonistically towards JA, crosstalk EMISSION between ethylene and octadecanoid pathways can be either syn- In the past decade, numerous attempts have been made to ergistic or antagonistic depending on a plant species, attack- modify the volatile formation in plants via metabolic engineer- ing herbivores, and the developmental and physiological state ing to improve scent and aroma quality of flowers and fruits of the attacked plant (Rojo et al., 2003). The accumulation of or to enhance crop protection through direct and indirect plant SA after treatment of lima bean leaves with the fungal elicitor defense (L¨ucker et al., 2006; Dudareva and Pichersky, 2006; alamethicin was shown to interfere with the biosynthetic path- Degenhardt et al., 2003; Aharoni et al., 2005). In general, the waydownstream of 12-oxophytodienoic acid, reducing the rapid bioengineering of volatiles can be achieved either through the

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 accumulation of JA and subsequently decreasing the emission modification of existing pathways (e.g., upregulation of one or of all JA-linked volatiles (Engelberth et al., 2001). Synergistic more steps or redirection of flux to a desirable compound by effects of JA and ethylene have been reported also in lima bean blockage of competing pathways) or by the introduction of new leaves and maize plants where treatments with ethylene or its gene(s) or branchways normally not found in the host plant. Not precursor, 1-aminocyclopropane-1-carboxylic acid, enhanced all attempts in modulating volatile profiles have been success- volatile emission induced by JA (Schmelz et al., 2003; Horiuchi ful, but they did uncover unexpected problems, such as a lack of et al., 2001). In contrast, herbivore damage of tobacco plants substrate availability and the metabolism of newly synthesized led to ethylene release, which suppressed JA-induced nicotine compounds. accumulation, thus reducing plant defense (Winz and Baldwin, The first successful improvement of volatile-based direct 2001). Several other signaling molecules such as abscisic acid, plant defense was accomplished by overexpressing a dual auxin and spermine may also contribute to plant defense re- linalool/nerolidol synthase (FaNES1) from strawberry in Ara- sponses by acting synergistically with JA and ethylene (reviewed bidopsis chloroplasts. Linalool and its derivatives produced by in Arimura et al., 2005). the transgenic plants significantly repelled an agricultural pest, To date it is accepted that herbivore attack involves several the aphid Mysus persicae,indual-choice assays (Aharoni et al., signal cascades, the interactions among which may determine 2003). Switching the subcellular localization of FaNES1 to 432 N. DUDAREVA ET AL.

the mitochondria, which contains the sesquiterpene precursor alcohol dehydrogenase resulted in the formation of new com- FPP, lead to the formation of (3S)-(E)-nerolidol and its deriva- pounds (Lewinsohn et al., 2001) or changes in the levels and/or tive, the C11 homoterpene (E)-DMNT, two signaling volatiles ratios of aroma-determining short-chain aldehyde and alco- which attracted the carnivorous predatory mites (Phytoseiulus hols (Wang et al., 1996; Speirs et al., 1998; Prestage et al., persimilis), improving plant indirect defense (Kappers et al., 1999). While the impact of alcohol dehydrogenase activity on 2005). Indirect defense of Arabidopsis was also improved by flavor discrimination by humans showed that higher levels of overexpression of terpene synthase TPS10 from maize respon- alcohols were associated with more intense ripe fruit flavor sible for the formation of (E)-β-farnesene, (E)-α-bergamotene (Speirs et al., 1998), taste trials were not performed in the other and some other herbivore-induced sesquiterpenes (Schnee et al., cases. 2006). An increase in cis-3-hexanal, a major green leaf volatile, was VIII. CONCLUSIONS achieved in transgenic tobacco plants overexpressing the yeast The current information available on the biology, ecology and acyl-CoA 9 desaturase and an insect acyl-CoA 11 desat- biochemistry of plant volatiles shows that extensive progress urase. The expression of these transgenes resulted in elevated has been made in the past decade although a lot of questions levels of 16:1 fatty acids, which increased 13-LOX activity cat- remain unsolved. Little is known about the function of individ- alyzing the first step to hexenal production from α-linolenic acid ual compounds in plant-plant and plant-insect interactions, the (Hong et al., 2004). While the effect of elevated levels of cis-3- signaling cascades involved in perception of volatile compounds hexanal on insect behavior was not investigated in this study, the and/or induction of their biosynthesis are still unclear, and the negative effect of 3-hexanal on aphid performance was shown evolutionary and ecological relevance of plant volatile emission in transgenic potato plants with depletion of HPL responsible awaits further investigations. Major challenges lay in the devel- for the cleavage of fatty acid hydroperoxides to C aldehydes 6 opment of novel model systems and the ecological realism of (Vancanneyt et al., 2001). Taken together, these results suggest experiment settings since not all studies performed to date were that plant defense responses to pests and pathogens could be carried out under natural conditions, for example, using high improved by increasing cis-3-hexanal formation. concentrations of volatile exposure or a single damage event as In contrast to metabolic engineering of vegetative volatiles a control for wounding. where the effect of altered emission profiles on insect behavior Recent use of transcriptomic and metabolomic approaches in wasinvestigated, the impact of changes in floral and fruit aromas plant volatile research resulted in isolation of new biosynthetic on insect or animal attraction has not yet been studied. Percep- genes and contributed to our understanding of the regulatory tion assessments were limited to sensory evaluations by humans, properties of the pathways involved in volatile formation. The whose odor threshold perception is much lower than that of most future promising development of comparative analysis of tran- animals or insects (Stockhorst and Pietrowsky, 2004; Vosshall, scriptomic, proteomic, and metabolomic datasets in both emit- 2000). Thus, metabolic engineering of floral and fruit volatiles ters (plants) and receivers (plants, insects/animals) will provide was considered successful only when the obtained changes in important new insights into the highly complex process of plant volatile profiles were significant enough for human detection. interactions with the surrounding environment and highlight new Numerous attempts have already been made to modify the scent targets for metabolic engineering. The identification of transcrip- bouquet, albeit without success due to different reasons includ- tion factors that regulate the orchestrated emission of volatiles ing the absence of suitable substrates for the introduced reaction originating from different metabolic pathways, the understand- (Beekwilder et al., 2004), modification of the scent compound ing of the intracellular metabolite trafficking and the mechanism into a non-volatile form (L¨ucker et al., 2001), insufficient levels of the release process should significantly improve our success

Downloaded by [USP University of Sao Paulo] at 10:56 08 August 2011 of emitted volatiles for olfactory detection by humans, or mask- in metabolic engineering of plant volatiles. The use of mutants ing of introduced compound(s) by other volatiles (Lavy et al., or transgenic plants (antisense or RNAi-silenced) will allow us 2002). However, successful genetic engineering of floral and to determine the key compounds involved in plant-insect and fruit volatiles was accomplished in a few cases. The introduc- plant-plant interactions. The knowledge derived from these ar- tion of three citrus monoterpene synthases in tobacco resulted in eas of research could be used for the development of improved drastic changes in the volatile profile emitted from flowers and agronomic traits in crops such as pest and disease resistance, leaves of the transgenic plants sufficient for olfactory detection weed control, improved fragrance of ornamentals and pollina- by humans (L¨ucker et al., 2004; El Tamer et al., 2003). Also, tion of seed crops, enhanced aroma of fruits and vegetables, and the olfactory enhancement of floral fragrance was achieved in the production of pharmaceuticals in plants. transgenic carnations where the metabolic flux was redirected from anthocyanin pathway towards benzoic acid, a precursor of methylbenzoate (Zuker et al., 2002). IX. ACKNOWLEDGMENTS To date, fruit aromas were modified only in tomato. The We thank Dr. Eran Pichersky, Dr. David R. Gang, Dr. Andre introduction of Clarkia breweri linalool synthase gene, the Kessler, and Dr. Jorg Bohlmann for their critical review of overexpression of a yeast 9-desaturase or nonspecific tomato the manuscript. We apologize to all of the authors whose PLANT VOLATILES 433

contribution to this field was not cited due to space restrictions. cleavage dioxygenase family demonstrates the divergent roles of this multi- Work in the authors’ laboratory is supported by the U.S. National functional enzyme family. Plant J. 45: 982–993. Science Foundation (grant numbers MCB-0212802 and MCB- Auldridge, M. E., McCarty, D. R., anf Klee, H. J. 2006b. Plant carotenoid cleav- age oxygenases and their apocarotenoid products. Curr. Opin. Plant Biol. 9: 0331333), the U.S. Department of Agriculture (grant numbers 1–7. 2003-35318-13619 and 2005-35318-16207), the U.S. Israel Bi- Baldwin, I. T., Kessler, A., and Halitschke, R. 2002. Volatile signaling in plant- national Agriculture Research and Development funds (grant plant-herbivore interactions: What is real? Curr. Opin. Plant Biol. 5: 351– number US-3437-03), and Fred Gloeckner Foundation, Inc. This 354. paper is contribution No 2006-17931 from Purdue University Bauer, K., Garbe, D., and Surburg, H. 2001. 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