Year: 2004
Type: review
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 of herbivore-induced volatiles (Vuorinen et al., 2004a). Yet, it is still unclear why oxidative stress is likely to be significantly higher after herbivore damage. Further studies are needed to help elucidate the roles of these and other plant volatiles. The growing number of reports on genes involved in volatile formation, as described in the following sections, should enable investigators to manipulate volatile emission and test its function in plants. Terpenes, as the largest class of plant secondary metabolites, have many volatile representatives. The majority of hemiterpenes (C5), monoterpenes (C10), sesquiterpenes (C15), and even some diterpenes (C20) have high enough vapor pressures at normal atmospheric conditions to allow significant release into the air. The basic pathway of volatile terpenoid biosynthesis is conveniently treated in three phases: (1) formation of the basic C5 units, (2) condensation of two or three C5 units to form C10, C15, or C20 prenyl diphosphates, and (3) conversion of the resulting prenyl diphosphates to end products. The formation of basic C5 units, isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) proceeds via two alternative pathways: the long known mevalonate pathway from acetyl-CoA and the methylerythritol phosphate pathway from pyruvate and glyceraldehyde-3-phosphate, discovered only in the last 10 years (for review, see Rodriguez-Concepcion and Boronat, 2002). The methylerythritol phosphate pathway, localized in the plastids, is thought to provide IPP and DMAPP for hemiterpene, monoterpene, and diterpene biosynthesis, while the cytosol-localized mevalonate pathway provides C5 units for sesquiterpene biosynthesis. However, metabolic “cross-talk” between the two pathways is prevalent (Schuhr et al., 2003), particularly in the direction from plastids to cytosol (Laule et al., 2003). This issue contains two contributions concerning the regulation of the basic pathways in relation to isoprene formation. Although produced largely by the plastidial pathway, isoprene also seems to arise from extra-plastidial sources, but there is apparently no cross-talk between the two pathways in its formation (Loreto et al., 2004a). The plastidial pathway is controlled by tight feedback regulation on its first step, deoxyxylulose-5-phosphate synthase (Wolfertz et al., 2004). In the second phase of terpene biosynthesis, IPP and DMAPP condense to form geranyl diphosphate (GPP), farnesyl diphosphate (FPP), and geranylgeranyl diphosphate, the precursors of monoterpenes, sesquiterpenes, and diterpenes, respectively. These reactions are catalyzed by short-chain prenyltransferases (Koyama and Ogura, 1999; Liang et al., 2002). FPP is synthesized by a large family of homodimeric prenyltransferases called FPP synthases. However, the situation regarding GPP formation is more complex. While the GPP synthases of Arabidopsis (Bouvier et al., 2000) and grand fir (Abies grandis; Burke and Croteau, 2002) are homodimers, like other short-chain prenyltransferases, those reported from peppermint (Mentha × piperita) leaves (Burke et al., 1999) and the flowers of snapdragon (Antirrhinum majus) and Clarkia breweri (Tholl et al., 2004) are unusual heterodimeric enzymes, with each subunit being a member of the prenyltransferase protein family. The third phase of terpene volatile biosynthesis involves the conversion of the various prenyl diphosphates, DMAPP (C5), GPP (C10), FPP (C15), and geranylgeranyl diphosphate (C20), to hemiterpenes (isoprene and 2-methyl-3-buten-2-ol), monoterpenes, sesquiterpenes, and diterpenes, respectively. These reactions, carried out by a large family of enzymes known as terpene synthases (Cane, 1999; Wise and Croteau, 1999), produce the primary representatives of each skeletal type. The investigation of terpene synthases is a very active area of plant volatile research and this issue contains four contributions describing the isolation of genes of this type from Norway spruce (Picea abies; Martin et al., 2004), Arabidopsis (Chen et al., 2004), cucumber (Mercke et al., 2004), and L. japonicus (Arimura et al., 2004b). These gene sequences give new insights into the evolutionary origin and genetic regulation of terpene synthases. One of the most outstanding properties of these enzymes is their proclivity for making multiple products from a single substrate. Hence, there has been much curiosity about the carbocationic reaction mechanism. The elucidation of the first crystal structures of plant terpene synthases (Starks et al., 1997; Whittington et al., 2002) now puts this work on a much stronger experimental footing. Many terpene volatiles are direct products of terpene synthases, but others are formed through transformation of the initial products by oxidation, dehydrogenation, acylation, and other reaction types. These are discussed in the following section. The terpene pathways are essentially biosynthetic, building up a carbon skeleton, and the immediate products formed by the large family of terpene synthases discussed above are mostly hydrocarbons, although sometimes they contain a hydroxyl group (e.g. linalool synthase produces linalool, a tertiary alcohol). Such compounds are already fairly volatile. In contrast, most other volatile compounds are produced through the shortening of a carbon skeleton, often followed by further modification, or simply by modification of the existing carbon skeleton. Compounds that are already somewhat volatile may also be modified, resulting in enhanced volatility or changed olfactory properties. The majority of these modifications involve the reduction or removal of carboxyl groups, the addition of hydroxyl groups, and the formation of esters and ethers. Each type of modification is catalyzed by a group (or several groups) of related enzymes constituting protein families. Some of these protein families had been previously recognized from biochemical research into nonvolatile compounds but some were only recently identified as part of the research into the biosynthesis of plant volatiles. Modifications for which enzymatic reactions and enzymes have been identified in plants are described below. Representative modification reactions leading to the biosynthesis of compounds with enhanced or changed volatility and olfactory properties. SAM, S-adenosyl-l-Met; CVOMT, chavicol O-methytransferase; SAMT, S-adenosyl-l-Met:salicylic acid carboxyl methytransferase; and BEAT, acetyl-coenzyme A:benzyl alcohol acetyltransferase. Cytochrome P450 enzymes are also very important in the biosynethsis of volatile phenylpropenes such as eugenol and the benzenoid vanillin. Both of these compounds, found in a wide variety of species both in flowers and in leaves, are derived from Phe and share with nonvolatile phenylpropanoids the earlier steps of 4-hydroxylation of cinnamate by 4CH, a P450 enzyme (Frank et al., 1996), and 3-hydroxylation by the newly discovered P450 enzyme that utilizes the shikimic or quinic ester of coumarate rather than coumaric acid or coumaroyl-CoA (Schoch et al., 2001; Gang et al., 2002a). Cytochrome P450 enzymes are crucial in the biosynthesis of volatiles derived from fatty acids, and in particular, in the octodecanoic pathway. Two different P450 enzymes, 9-LOX and 13-LOX, can introduce a peroxide into linoleic acid (18:3) at the respective positions (Howe and Schilmiller, 2002). Subsequent cleavage of the hydrocarbon chain by produces and respectively. The is important of volatiles, the of compounds that are emitted the is and 2002). In addition to the cleavage of linoleic acid at the to also produces a compound that can be to acid (Howe and Schilmiller, 2002). While acid is not by its is are large and family of with representatives found to be involved in the biosynthesis of volatiles. Such enzymes have been in the of volatile and apparently alcohol can short-chain such as and to and that are also found in leaves et al., This of tight substrate to the of by genetic et al., 1999). Some terpene such as and are to by et al., et al., and are by the of the is have and are found in many plants, and its a major floral in many species et al., and is also likely derived from in a reaction catalyzed by a member of the family et al., 2004). A large of plant volatiles contain a hydroxyl group a The group is in a reaction catalyzed by a in which as the plant to share a they into families that share primary et al., 2003). A large family of with involved in the of both volatile and nonvolatile to or has been identified and as the family et al., 2003). of this family have been to the of eugenol to form in flowers of breweri and in the of and also the of chavicol to in the et al., 1997; et al., 2000; Gang et al., a major compound in many is produced from in two reactions catalyzed by two very and et al., 2002; et al., 2002). Both enzymes can out both is more with while is more with et 2002). flowers a compound with three groups, which is synthesized from and can the of the second and third and but not the of also known as et al., 2002; et al., 2002). The enzyme that this also to the but is only related to and et al., 2004). important × to be produced by the of This to be to a wide of including of the pathway such as and alcohol et al., 2002). above as the substrate of a eugenol and important volatile on its and important also contain a group on their The pathways of these compounds share the first steps with the pathway. Gang et demonstrated that eugenol is derived from a the and reactions and the which is catalyzed by This is also likely to be the for although this has not been demonstrated is a member of the family of plants et al., 2003). Some esters are wide in the plant has been reported in floral (Knudsen and 1993), and it is also commonly emitted from vegetative under by or et al., 2001; et al., 2003). enzyme of acid acid carboxyl first reported from breweri flowers et al., 1999). has been identified from several other plant species et al., 2002; et al., et al., et al., 2003). This which as the a new type of plant known as or the first two of the of the first three enzymes identified in this Some enzymes have been to be to also acid a compound to for the group in (for et al., 2004). the other acid carboxyl the enzyme for the snapdragon floral volatile et al., 2000; et al., 2000). are by the Arabidopsis including enzyme that both and (Chen et al., 2003). is not known all of these are involved in the biosynthesis of volatile compounds, but to the family have been to be for the three reactions in the biosynthesis of a nonvolatile in et al., 2003). However, Arabidopsis to acid to form et al., 2001). While this may act as internal in Arabidopsis and other plant it is also emitted from plants (Howe and Schilmiller, and has also been reported in the floral of several plant species (Knudsen et al., it is likely to be formed by most often with but also with such or to volatile compounds is also In all known such plant volatile esters are synthesized by a recently discovered family of plant called after the first of the first four enzymes identified and 2000). The basic reaction catalyzed by these enzymes is the of group from to the hydroxyl group of alcohol Many enzymes are involved in the of nonvolatile compounds such as or derivatives et al., and Croteau, or in steps of pathways that may to the of volatiles such as eugenol et al., 2002a). involved in volatile alcohol acetyl-CoA from breweri which produced et al., alcohol which produces in flowers of Clarkia et al., 2002) and et al., 2004), and in leaves of et al., and which produces and is in leaves of Arabidopsis et al., 2002). The enzymes often wide substrate for both the and the alcohol the alcohol enzyme can also to the alcohol et al., 2004). a enzyme from can use a of such as and and to various such as and et al., 2000; et al., 2004). from has wide substrate et al., 2004), and a enzyme can both and et al., 2003). In such cases, the type of volatile formed in a tissue more on the internal of the than on the and of the enzyme for these et al., et al., 2004). The shortening by two of the chain to the of phenylpropanoids to the formation of benzenoid compounds. The by which this is is not In and metabolic described in this that both the and pathways are involved in the formation of benzenoid compounds in et al., 2004). However, a discovery also that in the of acid a third pathway, via the pathway, may also in plants, as it in et al., 2001). of a volatile compound into the atmosphere on both the of its biosynthesis and the of its progress in the last decade in the isolation and characterization of genes for the formation of volatile compounds has the investigation of the regulation of the biosynthesis of plant volatiles. has been found that volatiles are synthesized in the from which they are in the of plant from which they can into the atmosphere or after being synthesized et al., and 2000; et al., et al., 2004) or in the structures or for found in and et al., Gang et al., 2001; et al., 2002). of volatile compounds is the plant organs in flowers produce the most and the of volatile compounds, which the flowers are for tissue also of volatile organic compounds, which could be by damage or by or et al., and Tumlinson, 1997; et al., 2004a). In such as significant amounts of volatile compounds in the and the emitted volatiles only a of the produced et al., 2000). and emission of volatile compounds is also a emission in flowers and in leaves and the of leaves are and not is not or flowers are for and relatively or decreasing the et al., and 2000; et al., 2000). The temporal in of enzymes for the steps of volatile formation, enzyme protein and the expression of genes that the biosynthesis of volatiles is largely at the of gene expression et al., et al., 2000). is still unclear to and other to this In more than biochemical pathway is for a of volatile compounds from different plant A of the regulation of benzenoid and emission in snapdragon flowers that the emission of and compounds is of individual metabolic pathways and the expression of genes that enzymes involved in the steps of biosynthesis et al., 2003). However, factors that multiple pathways leading to the formation of have not been The of the enzyme for the of the biosynthesis of a volatile is not the only The for the regulation of of volatile compounds also the of substrate in the et al., 2000). In the of enzymes that are to use several such as and the of the type of produced product et al., et al., et al., 2004). The of substrate in the regulation of the biosynthesis of volatile compounds also recently by metabolic the linalool synthase gene under the of the into the between organs in the of the synthesized linalool or its more on the availability of the substrate GPP in the tissue than on the expression of the linalool synthase gene et al., 2001). In peppermint the of which the conversion of to methylerythritol the to GPP and to about a increase in the and Croteau, 2001). regulation of GPP formation can at the of GPP as in snapdragon the subunit can a in GPP biosynthesis (Tholl et al., 2004). regulation of GPP synthase by product and substrate could also to the of the to GPP and to (Tholl et al., 2004). enzymes for the substrate as in the of three synthases and into plants, the of emission in leaves to that on the of the enzymes for while the emission in flowers were that the GPP not et al., 2004). These that while the investigation of the regulation of the steps of volatile biosynthesis is important a of the regulation of the through the biochemical pathway is for the of and emission of secondary volatile compounds. of volatile compounds from flowers and leaves of some plant as well as herbivore-induced volatiles, the The release of floral volatiles in these species a with emission the or which generally with the of potential and is controlled by a or by and et al., et al., as well as volatiles emitted from and leaves, a emission et al., Loreto et al., et al., 2001; and Martin et al., et al., with some emission also controlled by a for in et al., 2002). In flowers the and emission of some volatile compounds, such as the volatile ester is by the of substrate availability which in could be at the of expression of genes encoding the enzymes of its biosynthesis et al., While regulation of isoprene emission is well (Wolfertz et al., 2003), is known to about the molecular for emission of vegetative volatiles. there is a of several between the beginning of herbivore damage and the release of volatile compounds, which could be in by the of the expression of genes for their biosynthesis (Arimura et al., 2004a). volatile compounds are after herbivore damage, they arise from (Pare and Tumlinson, factors such as and can the emission of volatiles and the and of and et al., 2000). In addition, the in emission of floral volatiles which after the et al., 2003). very is known about the release of synthesized volatile compounds from plant In the of release is a function of the properties of the compound and the properties of and membranes (in of monoterpenes which are synthesized in the through which the compound has to of volatile compounds emitted and within the plant tissue that the emission of volatiles is not a function of their volatility but could also involve a and et al., 2000). The membranes of the it or be more to some volatile compounds or the emitted substances may be with different than the volatiles. is known about between various the of the release and these to the regulation of volatile Plants produce a of volatile compounds for both general and advances in with ability to and genes and the enzymes they from many plant have enhanced of plants such compounds and their The of should come from the significance of these volatiles for plant and their on the of plants with their
Source: PLANT PHYSIOLOGY
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: bronze
OpenAlex ID: W2104362138