Sites of synthesis, biochemistry and functional role of plant volatiles

Abstract

All plants are able to emit volatile organic compounds (VOCs) and the content and composition of these molecules show both genotypic variation and phenotypic plasticity. VOCs are involved in plant–plant interactions and for the attraction of pollinating and predatory insects. The biochemistry and molecular biology of plant VOCs is vast and complex, including several biochemical pathways and hundreds of genes. In this review the site of synthesis, the biosynthesis and the functional role of VOCs are discussed.

Full text

Sites of synthesis, biochemistry and functional role of plant volatiles
M.E. Maffei
⁎
Plant Physiology Unit, Department of Plant Biology, Innovation Centre, University of Turin, Via Quarello 11/A, 10135 Turin, Italy
Received 7 January 2010; received in revised form 3 March 2010; accepted 8 March 2010
Abstract
All plants are able to emit volatile organic compounds (VOCs) and the content and composition of these molecules show both genotypic
variation and phenotypic plasticity. VOCs are involved in plant–plant interactions and for the attraction of pollinating and predatory insects. The
biochemistry and molecular biology of plant VOCs is vast and complex, including several biochemical pathways and hundreds of genes. In this
review the site of synthesis, the biosynthesis and the functional role of VOCs are discussed.
© 2010 SAAB. Published by Elsevier B.V. All rights reserved.
Keywords: Chemical defense; Molecular biology; Physiology; Plant secretory structures; Terpenes; Volatile organic compounds (VOCs)
1. Introduction
Volatile organic compounds (VOCs) are products emitted
into the atmos phere from natural sources in marine and
terrestrial environments (Guenther et al., 1995; Lerdau et al.,
1997; Chappell, 2008) and the majority of VOCs entering the
atmosphere are of biogenic origin. In fact, over 90% of natural
emission of VOCs is related to plants species with dominant
sources of VOCs being forests all over the world; the most
important among them is the Amazonian rainforest. Plants emit
400–800 Tg C/yr as hydrocarbons, an amount equivalent to the
sum of biogenic and anthropogenic methane emissions
(Guenther et al., 1995), while up to 36% of the assimilated
carbon is released as complex bouquets of VOCs (Kesselmeier
and Staudt, 1999; Kesselmeier, 2001; Kesselmeier et al., 2002).
Unlike methane, plant-produced VOCs are extremely reactive
in the troposphere, with life-times ranging from minutes to
hours (Lerdau et al., 1997), contributing to the aerosol that
scatters the ligh t to produce the blue sky.
VOCs are released from leaves, flowers and fruits into the
atmosphere and from roots into the soil. To humans, pollinator-
attracting floral VOCs have been a source of olfactory pleasure
since anti quity, and we also use a large number of aromatic
plants as flavorings, preservatives, and herbal remedies
(Pichersky and Gershenzon, 2002; Pichersky et al., 2006).
The primary functions of airborne VOCs are to defend plants
against herbivores and pathogens, to attract pollinators, seed
dispersers, and other beneficial animals and microorganisms,
and to serve as signals in plant–plant communication (Dudareva
and Pichersky, 2008). In some plants, released VOCs may also
act as wound sealers ( Penuelas and Llusia, 2004).
Some VOCs might be dangerous for human 's health when
presen t at higher concentrations (Jahodar and Klecakova,
1999), and plant-emitted VOCs are also major precursors of
tropospheric phytotoxic compounds (Padhy and Varshney,
2005). Since some VOCs can act as precursors of photochem-
ical smog, their level is one of the fundamental parameters for
the assessment of atmospher e quality (Ulman and Chilmonc-
zyk, 2007). VOCs can regulate the oxidative capacity of the
troposphere, carbon monoxide, O
3
and aerosol budgets, and
together with high concentration of nitrogen oxides in the
sunlight they form more phytotoxic O
3
(Vuorinen et al., 2005).
Furthermore, VOCs have also been shown to be involved in the
formation of secondary aerosols in the atmosphere, which have
implications for the radiative balance of the earth (Padhy and
Varshney, 2005).
Routine measurements of VOCs in air have shown that
average concentrations are very much smaller than those used in
laboratory experiments designed to study the effects of VOCs
on plants. However, maxi mum hourly concentrations of some
A
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doi:10.1016/j.sajb.2010.03.003

VOCs can be 100 times larger than the average, even in rural air
(Cape, 2003).
This review aims to collect most of the information
available on the ability of plants to produce VOCs and to
explore their sites of synthesis, biochemistry and functional role.
2. Plant VOCs
Chemically, VOCs belong to the large group of terpenoids
(homo-, mono-, di-, sesquiterpenoids), fatty acid derived C
6
-
volatiles and derivatives, phenylpropanoid aromatic compounds
(like methyl salicylate, MeSA, and indole), as well as certain
alkanes, alkenes, alcohols, esters, aldehydes, and ketones
(Pichersky and Gershenzon, 2002; Holopainen, 2004; Arimura
et al., 2005, 2009; Baldwin et al., 2006; Wu and Baldwin, 2009).
Today more than 1700 volatile compounds have been isolated
from more than 90 plant families, constituting approximately 1%
of all plant secondary metabolites (Pichersky and Gershenzon,
2002). The composition of VOCs emitted by plants also depends
on the mode of damage such as single wounding, continuous
wounding (Mithöfer et al., 2005), herbivore feeding (Paré and
Tumlinson, 1996), and egg deposition (Hilker and Meiners,
2002). Some VOCs emitted after insect feeding can serve as
repellents to the attacking insect itself as a direct defense, as well
as attractants to the natural enemies of the attacking insect as
indirect defenses (Kessler and Baldwin, 2001). An herbivore-
induced VOC blend may comprise more than 200 compounds
(Dicke and Van Loon, 2000). In addition to attracting the natural
enemies of the egg and larval stages, herbivore-induced plant
volatiles (HIPVs) can also decreas e the oviposition rates of the
attacking herbivores and thus can be considered both direct and
indirect defense systems (Dicke and Van Loon, 2000; Kessler
and Baldwin, 2001). Besides addressing organisms from other
trophic levels, induced VOCs also act on neighbored leaves of
other plants (Arimura et al., 2000; Engelberth et al., 2004; Heil
and Silva Bueno, 2007). Moreover, the volatile production
generally shows a pronounced rhythmicity by emitting the
volatiles mostly during the light phase (Arimura et al., 2008b).
Furthermore, the production of VOCs is activated by elicitors
from oral secretions of the attacking insect herbivore (Truitt
et al., 2004; Truitt and Pare, 2004; Schmelz et al., 2006).
Although defenses might benefit plants, the expression of plant
resistance can be costly in the absence of plant enemies (Bergelson
and Purrington, 1996; Strauss et al., 2002). Since the synthesis of a
chemical represents an investment of energy and resources for the
organism if the benefits it gets from this investment are
reasonable, evolution will keep this trait, yet the opposite is also
true: if the use of resources does not benefit the organism, this
adaptation may persist or it will eventually disappear (Macias et
al., 2007). Since the production of VOCs can be limited by both
light and soil nutrients is likely to incur considerable costs, at least
under certain growing conditions (Heil, 2008).
3. Sites of synthesis of plant VOCs
Plants express different types of secondary metabolites as
defense strategy against biotrophs, ranging from the constitutive
and inducible synthesis of bioactive natural products to the
production of structural traits (Ballhorn et al., 2008). Many
VOCs, particularly most monoterpenes and sesquiterpenes, are
synthesized and stored in special secretory tissues, which occur
in most vascular plants. The secreted material is usually
eliminated from the secretory cells outside the plant or into
specialized intercell ular spaces (Fahn, 1988). Certain plant
species accumulate VOCs in resin ducts, or glandular trichomes
and such compounds can be released in large amounts as
soon as these structures are ruptured by herbivore feeding or
movements on the plants' surface (Duke et al., 2000 ). Since
many of the constitutive defense compounds may be toxic at
high concentrations to the plant itself, the plant must be able to
generate and store such substances without poisoning itself. The
obvious strategy to overcome this problem is to store VOCs as
inactive precursors, for instance as glycosides (Jerkovic and
Mastelic, 2001), or in extracellular compartments, as in the case
of glandular trichomes. Secretory tissues are usually classified
according to the substance they produce and trichomes, ducts
and cavities are mainly involved in VOC production.
3.1. Glandular trichomes
Several plant species store VOCs in specialized glandular
trichomes (Gershenzon et al., 2000) which release their conten ts
in response to tis sue damage, thus deterring herbivores or
inhibiting microbial growth (Langenheim, 1994). Glandular
trichomes secreting VOCs are present in Lamiaceae, Aster-
aceae, Geran iaceae, Solanaceae and Cannabinaceae. Their
morphology may vary among families although two general
types of trichomes are frequently present: capitate trichomes,
which consist of a basal cell, one to several stalk cells and one to
few secretory cells (Fig. 1A –B) and peltate trichomes,
comprising a basal epidermal cell, a short stalk cell and a
secretory head consisting of several secretory cell s arranged in
one layer (Fig. 1C–F). Whatever the exact nature of the capitate
gland secretory products, it is clear that the bulk of the VOCs is
produced by and stored in the peltate glandular trichomes
(Maffei et al., 1989; Turner et al., 2000). This general scheme of
glandular trichome structure can reach a further complexity in
some families where trichome s are multicellular and biseriate,
with one to several pairs of cell s in the stalks and the secretory
heads (Fahn, 1988)(Fig. 1C). In many cases, VOCs are
accumulated inside the cuticular layer but outside the plant cell
wall, either alone or along with other compounds which can be
of a very different chemical nature and lipo-hydrophilicity.
Being protodermal extrusions, glandular trichomes are present
on plant surfaces, with particular reference to leaf blades,
flowers and, in some cases, seeds. Although the presence of
terpene synthases in trichomes has been well documented
(Bertea et al., 2006), the regulation of their expression in
trichomes remains obscure. In tomato (Lycopersicon esculen-
tum Mill.), the expression of the monoterpene synthase LeMTS1
in stems and petioles was predominantly detected in trichomes
and could be induced by jasmonic acid (JA) treatment (Van
Schie et al., 2007). To elucidate the biosynthetic pathway and to
isolate and charact erize genes involved in the biosynthesis of
613M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

terpenoids including artemisinin in Artemisia annua L.,
glandular trichomes were used as an enriched source for
biochemical and molecular biological studies (Bertea et al.,
2006). The accumulation of VOCs in developing plants could,
in theory, be influenced by both the rate of terpene synthesis and
the rate of terpene loss. Maffei et al. (1986, 1989) using
scanning electron microscopy to estimat e gland numbers and
densities on developing leaves, fou nd that yo ung leaves
contained fewer glandular trichomes than older leaves,
indicating an evident gland production during leaf growth. It
is interesting to note that in many plant species new glandular
trichomes are continually produced during leaf growth and that
newly initiated glands do occur together with mature glands in
growing regions, such that neighboring glands within the same
leaf zone are often of different ages. Circumstantial evidence
based on ultrastructural correlation, specific labeling and
subcellular fractionation studies indicates that at least the
early steps of monoterpene biosynthesis occur in trichome
plastids (Turner et al., 1999), while nuclear hypertrophy has
been observed in the secret ory cells of both peltate and capitate
trichomes (Berta et al., 1993).
3.2. Secreting ducts and cavities
Other secreting structures producing constitutive VOCs are
less visible because hidden in deep tissues of the plant. These
are secreting ducts and cavities that consist of relatively large
intercellular spaces lined by an epithelium of secretory cells
(Fahn, 1988). In this case also, bioactive VOCs are stored and
represent a constitutive defense ready to be delivered in case of
rupturing of tissues. Resin ducts are typical of evergreens such
as the Pinaceae, but are also present in several other plant
families such as the Myrtaceae, Asteraceae, Umbelliferae and
Leguminosae. These tissues generate by the progressive
separation of cells (schizogeny) with the creation of a large
intercellular space inside which secretion accumulates (Fahn,
1988). Fig. 1G shows a cross-section of a Scots pine needle. In
this family, resin ducts are present all over the plant body, from
leaves to roots, and they accumulate VOCs which are used as a
chemical weapon against herbivore and pathogen atta ck.
Secretory cavities are typical of families such as Rutaceae,
Clusiaceae, Myrtaceae and some others. Unlike resin ducts,
secretory cavities originate both by schizogeny and lysigeny
(disruption — lysis of cell walls and mixing of protoplasts).
Typical structures are those present in the skin of citrus fruits
(Fig. 1H). Compression of surrounding tissues forces the
secretion to get out and the ensuing release of compounds into
the environment repres ents, in this case also, a constitutive
chemical defense.
3.3. Secretory cells in flowers and roots
Other tissues able to produce lipophilic substances are
represented by secretory cells that accumulate the secreted
products inside their vacuoles. This is the case of VOCs
produced by the odorous roots of the grass Vetiveria zizanioides
Nash (vetiver). Vetiver VOCs are produced in secretory cells
localized in the first cortical layer outside the endodermis of
mature vetiver roots (Viano et al., 1991a,b; Maffei, 2002).
Fig. 1I shows a cross-section of vetiver root, where the essential
oil-producing cells are evidenced by treatment with Sudan
Black B (Maffei, 2002). Recentl y, by using culture-based and
culture-independent approaches to analyze the microbial
community of the vetiver root, Del Giudice et al. (2008)
demonstrated the presence of a broad phylogenetic spectrum of
bacteria, including α, β, and γprote obacteria, high-G + C-
content gram-positive bacteria, and microbes belonging to the
Fibrobacteres/Acidobacteria group. The same group isolated
root-associated bacteria and showed that most of them were able
to grow by using vetiver sesquiterpenes as a carbon source and
to metabolize them releasing into the medium a large number of
compounds typically found in commercial vetiver oils. Several
of these bacteria were also able to induce gene expression of a
vetiver sesquiterpene synthase (Del Giudice et al., 2008). These
results support the intriguing hypothesis that bacteria may have
a role in essential oil biosynthesis opening the possibility to use
them to maneuver the vetiver oil molecular structure. These
results a re in accordance with those obtained by Viano et al.
(1991a,b) who analysed vetiver root ultrastructure using
electron transmission microscopy and detected essential oil
crystals in the inner cortical layer close to the endodermis.
According to these authors the secretion of the essential oil
occurs in this region and successively reaches the whole cortex.
VOCs can be synthesized by a variety of other anatomical
structures such as solitary cells and areas of epidermal cells. The
typical fragrance of flowers results from VOCs occurring in
form of small droplets in the cytoplasm of the epidermal and
neighboring mesophyll cells of sepals (Fa hn, 1988). In flowers,
the biosynthesis of VOCs usually occurs in epidermal cells,
allowing an e asy escape of VOCs into the atmosphere
(Kolosova et al., 2001). Flowers usually produce their attractive
fragrance in osmophores or in conical cells located on the petals
(Fig. 1J). These cells do not stock VOCs but release them into
the air (Caissard et al., 2004). In species belonging to the
Orchidaceae and Araceae, VOCs produced by o smophores
produce also amines and ammonia (Pridgeon and Stern, 1983).
Although these stored and induced VOCs have useful roles,
non-terpene-emitting species also survive the onslaught of
herbivores and competition, and can set seed (Owen and
Penuelas, 2005). In fact, lack of specific anatomical structures
for VOC storage does not imply negligible internal VOC
concentrations (Niinemets et al., 2004).
3.4. Extrafloral nectar
Constitutive defenses are not restricted to direct defenses.
Central American Acacia species secrete extrafloral nectar to
attract and nourish ants that defend the host plant against
herbivores. This form of indirect defense can be inducible as
well as constitutive. In the latter case the plants are obligatory
inhabited by symbiotic ants. Interestingly, phylogenetic anal-
ysis revealed that the inducibility of extrafloral nectar secretion
is the ancestral (plesiomorphic) state and the constitutive nectar
flow represents the derived (apomorphic) state within the genus
614 M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

Acacia (Heil et al., 2004). In response to herbivory, plants like
Lima bean (Phaseolus lunatus L.) also secrete extrafloral nectar,
that attracts predatory arthropods, mainly ants, and therefore
serves as an indirect defense (Heil, 2004a). In many cases,
plants do not rely on a single defense strategy but employ a
complex array of different defensive mechanisms. Wild Lima
beans significantly benefited from induced increased nectar
production in terms of less leaf damage, and higher growth rates
and seed production, respectively (Kost and Heil, 2008).
Moreover, volatiles released by damaged lima bean leaves
could induce extrafloral nectar in neighboring plants (Kost and
Heil, 2006) as well as in undamaged leaves of the same shoots
(Heil and Silva Bueno, 2007). When lima bean plants were
exposed to (Z)-3-hexenyl acetate, a substance natur ally released
from damaged lima bean, a significant increases in EFN
secretion was found (Heil et al., 2008). Also, plants growing in
the wild, which had been induce d by exogenous application of
the phytohormone jasmonic acid (JA), responded by increasing
both their VOC emission and EFN secretion (Heil, 2004b). It
has been demonstrated that an artificial increase of the amount
of available EFN benefits lima bean in nature by attracting
predacious and para sitoid arthropods and re cent findings
suggest that EFN plays an even more important role as an
indirect defense of lima bean than VOCs or any other JA-
responsive trait (Kost and Heil, 2008).
4. Main biochemical pathways of plant VOCs
De novo biosynthesis and emission of VOCs include products
of the lipoxygenase (LOX) pathway, such as oxylipins, green leaf
volatiles (GLVs), as well as many terpenoids, including isoprene,
some carotenoid derivatives, indoles and phenolics, including
methyl salicylate (MeSA) and aromatic VOCs (Tholl et al., 2006;
Tholl, 2006). A schematic representation of the volatilome tree is
depicted in Fig. 2.
4.1. Isoprenoids
All isoprenoids are produced from the precursors dimethylallyl
diphosphate (DMAPP) and its isomer isopentenyl diphosphate
(IPP), which are synthesized by the deoxyxylulo se-5-phosph ate
(DXP) pathway (also known as the MEP pathway) in the chloro-
plasts and by the mevalonate (MVA) pathway in the cytoplasm (see
ref. Kesselmeier and Staudt, 1999, for a review of the evolutionary
and f unctional history of the two pathways for IPP and DMAPP
synthesis). Some exchange and/o r cooperation is thoug ht to exist
between these two pathways and the two pathways probably
operate under different physiological conditions within the cell and
depend on th e cell and plastid de velopmental state (Wanke et al.,
2001). The evidence that a small amount of cross-talk between the
two pathways might occur, implies that the pathways are not com-
pletely autonomous (Holopainen, 2004). It is proposed that C
10
precursors of monoterpenes are predominantly synthesized within
plastids by the MEP pathway, whereas precursors of sesquiterpenes
are produced via the classical MVA pathway. However, it has to be
noted that monoterpenes and sesquiterpenes, along with the
hemiterpene isoprene, are VOCs that represent only a small pro-
portion of the d iverse group o f isopre noid plant produc ts ( Owen
and Penuelas, 2005).
Isoprene (2-methyl-1,3-butadiene) is the simplest terpenoid
(hemiterpene) emitted by plants; it is synth esized from DMAPP
by the action of isoprene synth ase. The biosynthesis and
functional physiology of isoprene have been recently reviewed
(Sharkey et al., 2008).
Some VOCs, such as β-ionone, are not derived directly from
isoprenoid pyrophosphates but instead from the cleavage of
tetraterpenes such as carotenoids, by the action of carotenoid
cleavage dioxygenases (CCDs) (D'Auria et al., 2002)(Fig. 2,
branch A).
Highly volatile monoterpenes (C
10
) have two isoprene units,
whereas sesquiterpenes have three isoprene units (C
15
), based
on the classification or Ruzicka. Monoterpenes are typical leaf
products whereas sesquiterpenes are typical flower fragrances
(Dudareva et al., 2006); although considerable amounts of
monoterpenes and sesquiterpenes are produced in leaf glandular
trichomes (see Fig. 1) and are emitted from the herbivore-
damaged foliage and roots (see below).
Homoterpenes, such as 4,8-dimethylnona-l,3,7-triene
(DMNT) and 4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT)
are the most typical compounds related to herbivore feeding. The
biosynthesis of TMTT and DMNT, has been proposed to proceed
via an oxidative degradation by P450 enzymes of the diterpene
geranyl linalool and the sesquiterpene (E)-nerolidol as precursors,
respectively (Holopainen, 2004; Arimura et al., 2005, 2009)
(Fig. 2, branch A and B).
A large, structurally diverse number of terpenoids are
yielded by a large family of terpene synthases (TPS) using
geranyl diphosphate (GPP) and farnesyl diphosphate (FPP) as
substrates and many distinct TPSs that synthesize monoterpenes
and sesquiterpenes (the bulk of terpenoid VOCs) have been
characterized from various plants (Owen et al., 1997, 2001; Lin
et al., 2007; Arimura et al., 2008a,b, 2009; Wu and Baldwin,
2009). Metabolic engineering of VOCs can be achiev ed through
the modifica tion of existing pathways, for instance by up- or
down-regulation of one or more biosynthetically steps or by the
re-direction of metabolite fluxes to a desired compound by
blockage of competing pathways. Otherwise, the introduction
of new genes or branch-ways that are normally not present in
the host plant can be accomplished. There are several examples
of successful applications of these methods. By overexpressing
a dual linalool/nerolidol synthase (FaNES1) from strawberry in
chloroplasts of the model plant Arabidopsis thaliana (L.)
Heynh. it has been demonstrated that linalool and its derivatives
significantly repelled aphids (Aharoni et al., 2005). Direction of
FaNES1 to another compartment, the mitochondria, which
contains the sesquiterpene precur sor FPP, leads to the formation
of nerolidol and its derivative, the C
11
homoterpene DMNT;
both volatiles attracted carnivorous predatory mites thus
improving plant indirect defense (Kapp ers et al., 2005).
4.2. Oxylipins
Oxylipins originate from polyunsaturated fatty acids which
are released from chloroplast membranes by lipase activity and
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that represents the substrate for numer ous other oxygenated
compounds including jasmonates (which comprise JA, methyl
JA, JA amino a cid conjugates and further JA met abolites) as
well as the source for GLV biosynthesis. LOXs form
hydroperoxides from linolenic (18:3) or linoleic acids (18:2).
With linolenic acid as the substrate, (13S)-hydr operoxyoctade-
catrienoic acid (13-HPOT) or (9S)-hydroperoxyoctadecatrie-
noic acid (9-HPOT) are formed, whereas with linoleic acid as
the substrate (13S)-hydroperoxyoctadecadienoic acid (13-
HPOD) and (9S)-hydroperoxyoctadecad ienoic acid (9-HPOD)
are formed (Wasternack, 2007). Discrete 9-LOX and 13-LO X
pathways have been proposed to explai n the occurrence of
numerous oxylipins (Howe and Schilmiller, 2002 ). Octadeca-
noids and jasmonates originate from 13-allene oxide synthase
(13-AOSs) activity, whereas aldehydes, ω-oxo fatty acids and
alcohols are formed by the activity of hydroperoxy lyases (13-
HPLs ). GLVs are synthesized via the LOX (lipoxygenase)
pathway from C
18
polyunsaturated fatty acids including linoleic
acid and linolenic acids (Dudareva, 2005). The C
18
acids are
cleaved to C
12
and C
6
compounds by hydroperoxide lyases
(Engelberth et al., 2004). The first C
6
GLV compound
synthesized by the LOX/lyase pathway is 3-Z-hexenal which
is then converted to other GLVs such as 2-hexenal (leaf
aldehyde), 3-hexenol (leaf alcohol) and 3-hexenyl acetate (leaf
ester) (Shiojiri et al., 2006). 3-Hexenyl acetate is formed from a
reaction b etween 3-hexenol and acetyl-CoA, a reaction
catalysed by an acyltransferase (D'Auria et al., 2007). While
GLVs are usually defined as saturated and unsaturated C
6
alcohols, aldehydes and esters, it has been recently shown that
C
5
compounds (2-pentenyl acetate and 2-pentenol) can be
constituents of the GLVs as well (Connor et al., 2008 ). The
biosynthesis of oxylipins has been recently reviewed (Waster-
nack, 2007) (see also Fig. 2, branch C).
4.3. Volatile aromatic compounds
Another large class of VOCs consists of compounds
containing an aromatic ring. VOCs containing nitrogen or
sulfur are synthesized by cleavage reactions of modified amino
acids or their precursors. For example, the volatile indole is
made in maize by the cleavage of indole-3-glycerol phosphate,
an intermediate in tryptophan biosynthesis (Koeduka et al.,
2006). Indole has been identified as one of the blend of VOCs
emitted from maize in response to herbivore damage and the
production and release of indole in plants has been shown to be
an active process in which the de novo synthesis is triggered in
response to insect feeding (Pare and Tumlinson, 1997b). Maize
seedlings contain indol e as an intermediate in at least two
biosynthetic pathways . The BX1 enzyme catalyzes the
conversion of indole-3-glycerol phosphate (IGP) to indole,
which is further converted to the defense-related secondary
metabolite DIMBOA [2,4-dihydroxy-7-methoxy-2H-1,4-ben-
zoxazin-3(4H)-one]. Indole also serves as the penultimate
intermediate in the formation of tryptophan by tryptophan
synthase. In maize plants, a gene has been characterised as IGP
lyase, which catalyses the formation of free indole from IGP and
the induction pattern of Igl parallels the emission of free indole
from the whole plant (Frey et al., 2000). The effect of wounding
on indole emission is relatively small and this response could
indicate that a certa in thres hold of Igl induction has to be
exceeded for notable indol e production to occur (Frey et al.,
2000)(Fig. 2, branch D).
Other aromatic VOCs include phenylalanine-derived com-
pounds. Eugenol is a reduced version of coniferyl alcohol, a lignin
precursor, while phenylacetaldehyde, a compound present in
tomato fruit, is derived from phenylalanine by decarboxylation
and oxidative removal of the amino group (Pichersky et al., 2006).
Propenyl- and allyl-phenols, such as methyl chavicol (estragole),
p-anol as well as eugenol, have gained importance as flavoring
agents and also as putative precursors in the biosynthesis of 9,9′-
deoxygenated lignans, many of which have potential medicinal
applications (Gang et al., 2001). The biosynthesis of chavicol was
shown to occur via the phenylpropanoid pathway to p-coumaryl
alcohol, which can be reduced to form p-dihydrocoumaryl
alcohol, followed by dehydration to afford chavicol, as well as
formation of p-methoxycinnamyl alcohol, with further side-chain
modification to afford methyl chavicol (Vassao et al., 2006)
(Fig. 2,branchE).
SA is synthesized by two pathways: one deriving from
benzoate via cinnamate, the other via isochorismate. MeSA is
synthesized via a reaction catalyzed by a methyltransferase
whereby a methyl group is transferred from the donor molecule
S-adenosine-methionine (SAM) to the carboxyl group of SA.
SA methyltransferase (SAMT) has been characterized in several
plant species including the model plant Arabidopsis (Vassao
et al., 2006)(Fig. 2, branch E and F).
VOCs derived by oxidative cleavage and decarboxylation of
various fatty acids result in the production of shorter-chain
volatiles with aldehyde and ketone moieties that often serve as
precursors for the biosynthesis of other VOCs (Pichersky et al.,
2006).
Besides detection, isolation and characterisation of enzym es
and genes involved in the formation of many VOCs, the
structures o f enzymes after crystallisation are n ow being
investigated and this information gives us hints on the catalytic
mechanisms as well as probable evolutionary origins of these
enzymes (Petersen, 2007).
5. Induced production of VOCs
While flower scents are usually released in an ontogenetically
programmed way, the quantity and quality of VOCs that are
released from vegetative plant parts and roots can change
dramatically when plants are stressed (Heil, 2008). In induced
processes, rather than in the case of constitutive defenses, the
recognition of the attacking insect and the subsequent signaling of
the alarm is the prerequisite for a fast and efficient defense. Many
forms of induced defense are not restricted to local responses at
the wounding site, but can be detected systemically throughout
the plant. Thus, induced defenses also involve the synthesis and
accumulation of various VOCs that influence insect attraction/
deterrence and inhibit insect growth and development.
There are two types of plant inducible defenses: direct
defenses and indirect defenses. Direct defenses include any plant
616 M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

traits that by themselv es affect the susceptibility of host plants to
insect attacks (Kessler and Baldwin, 2002), whereas indirect
defenses include plant traits that by themselves do not affect the
susceptibility of host plants, but can serve as attractants to
natural enemies of the attacking insect (Chen, 2008). After
release from leaves, flowers, and fruits to the atmosphere and
from roots into the soil, plant VOCs defend plants against
herbivores and pathogens or provide reproductive advantages by
attracting pollinators (Chen, 2008). Moreover, certain volatiles
may act as airborne signals that boost direct and indirect defenses
in remote parts of the same plants or neighboring plants (Heil
and Silva Bueno, 2007; Ton et al., 2007). However, it has to be
noted that herbivore-induced emission of plant VOCs is not
limited to higher plants. It has been recently shown the arsenic
hyper-accumulating fern, Pteris vittata responds to herbivore
wounding events by emitting several sesquiterpenes (Imbiscuso
et al., 2009 ). The same sesquiterpenes are used by higher plants
to attract insects in the field (Il'ichev et al., 2009).
Insect egg deposition induces a plant volatile pattern that
attracts egg parasitoids and induces the change of plant surface
chemicals, thus arresting the egg parasitoids by contact cues in
the vicinity of the eggs (Hilker and Meiners, 2002, 2006).
Indirect plant responses to insect egg deposition require
modification of the biosyn thetic activity of the terpenoid
pathways, since changes of the quantity and/or quality of the
plant's terpenoid volatiles have been detected for several plant
species with eggs (Fatouros et al., 2008).
Generally speaking, inducible defenses consist of three
steps: surveillance, signal transduction, and the production
of defensive chemicals (Chen, 2008). In the first step, the
plant's surveillance system detects parasite attacks by specific
recognition of signals. The detected signals are then transduced
through a network of signal transduction pathways, which
eventually lead to the production of defense chemicals (Maffei
et al., 2007a,b; Wu and Baldwin, 2009). In all cases, induction
of plant VOC can be triggered by both biotic and abiotic stress
(Arimura et al., 2009). In the next sections we will examine the
role of induced VOCs in plant defense against p athogens and
piercing/sucking/chewing herbi vores as well as the induced
physiological response of VOCs to environmental stresses.
5.1. Plant VOCs and the response to biotic stress
The VOC bouquet of biotically stressed plants typically
consists of green leaf volatiles (GLVs), terpenoids, methyl
jasmonate (MeJA), MeSA, methanol, ethylene, and other
substances. Total VOC emission from herbivore-damaged plants
can be nearly 2.5-fold higher than emissions from intact plants and
this observation also sustains the hypothesis that local biotroph-
induced VOCs might have substantial role in tropospheric
processes (Holopainen , 2004). The insect feeding-induced
emission of volatiles has been demonstrated for several higher
plant species (Van Poecke and Dicke, 2004b), among others the
model plant A. thaliana (Van Poecke and Dicke, 2004a), maize
(Zea mays L.) (Turlings et al., 1990), Lima bean (P. lunatus)
(Arimura et al., 2008b), Nicotiana attenuata Torr. (Kessler and
Baldwin, 2001; Gaquerel et al., 2009; Wu and Baldwin, 2009),
Medicago truncatula Gaertn. (Arimura et al., 2008a), and spruce
(Pinus glabra Walter) (Martin et al., 2003), as well as for lower
plants like ferns (Imbiscuso et al., 2009). In general, VOCs can
carry various types of information: (I) for herbivores to localize
their host plants, (II) for indirect defense employing a third trophic
level by attracting natural enemies of the plant's offender, and for
(III) neighboring plants and (IV) distant parts of the same plant,
respectively, to adjust their defensive phenotype accordingly
(Heil and Silva Bueno, 2007). Herbivore-induced VOCs represent
phenotypically plastic responses of plants to herbivory, which
result in changes in interactions between individuals in the insect–
plant community (Snoeren et al., 2007). Moreover, genetic
variations within herbivore species affect VOCs production and
there is a relationship between variations in the dispersing
behavior of some insects (e.g. spider mite) and VOCs production
(Maeda et al., 2007
).
Using VOCs as the only source of information, carnivores
can discriminate between plants infested by different herbivore
species (e.g. hosts and non-hosts) and between different plants
infested by the same herbivore. However, it must be considered
that the majority of herbivore-induced VOCs are also
constitutively released from flowers (Dudareva et al., 2006;
Pichersky et al., 2006). Overall, the current picture demon-
strates a high functional diversity in VOC-mediated communi-
cation within and among organisms, but it leaves us with the
open question of how misunderstandings in all these commu-
nications are avoided (Heil and Silva Bueno, 2007).
Some insects can locate their hosts even though the host
plants are often hidden among an array of other plants, and plant
volatiles play an important role in this host-location process
(Bruce et al., 2005). Furthermore, these VOC-mediated
interactions of plant s with organisms of higher trophic levels
suggest that they communicate similarly with e ach other
(Maffei et al., 2007b ). However, VOC exposure alone, without
actual herbivore attack, may directly increase the production of
defenses. Alternatively, VOC exposure may allow nearby
plants to ready their defenses for immediate use once the
herbivores move from the neighboring plant to attack the
‘‘listening’’ receiver (Arimura et al., 2000; Baldwin et al., 2006;
Heil and Silva Bueno, 2007; Gaquerel et al., 2009; Wu and
Baldwin, 2009).
Volatiles from primary host plants may also attract other
insects, as is the case of male aphids (Powell and Hardie, 2001;
Powell et al., 2006). Parasitoids also use herbivore-induced
responses to assess habitat profitability and adapt patch
residence time (Tentelier and Fauvergu e, 2007). Furthermore,
herbivore-induced plant volatiles emissions are inducible by
other biotrophs as well as abiotic agents (Holopainen, 2004)
(see next section).
Some substances are immediately released after damage and
cause the characteristic odor of freshly mowed pastures, the so
called GLVs (Arimura et al., 2009). GLVs seem not to be
enhanced by elicitors, and, therefore, their release has been
described as instantaneous “bleeding” from damage sites.
However, two related herbivores can lead to the emission of
distinctive ratios of GLVs in the same plant species (Degen et
al., 2004). A rapid formation of C
6
-volatiles after wounding not
617M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

only serves as protection agains t herbivores or pathogens, but
may also be toxic for the plant itself. The majority of GLVs are
isomers of hexenol, hexenal or hexenyl acetate. Some
preformed GLVs ‘bleed’ instantaneously from disrupted tissue,
but the rest of these compounds are released rapidly upon
damage, since the first intermediate of the octadecanoid
cascade, 13-hydroperoxylinolenic acid, also acts as an interme-
diate for the synthesis of 6-carbon volatiles (Walling, 2000;
Gatehouse, 2002). In contrast, the release of esters such as
MeJA and MeSa, of monoterpenes such as limonene, linalool or
β-ocimene, and of sesquiterpenes, such as α-bergamotene, β-
caryophyllene and farnesene, typically starts 24 h after attack
(Dudareva et al., 2006; Pichersky et al., 2006). Growth
conditions (particularly daylength) may affect the ratio of
VOCs present in the emission blend, even though the response
to herbivory and nutrient availability are similar (Ibrahim et al.,
2008). Transgenic Arabidopsis plants with an altered biosyn-
thesis for GLV showed striking responses when subjected to
herbivory and HPL sense plants showed a significant increase in
GLV production after herbivory, compared with controls. By
contrast, in HPL antisense Arabidopsis plants GLV formation
decreased and attracted fewer parasitoids than the control
(Shiojiri et al., 2006). These data indicate that the genetic
modification of VOCs biosynthesis could be an approach to
improve plant and, in particular, crop resistance against pest
attacks. Induced resistance is often associated with the ability
for a faster and stronger activation of defense responses upon an
attack by pathogens or insects. This physiological state is
referred to as priming (Heil and Silva Bueno, 2007; Ton et al.,
2007). Priming of corn plants by GLV released from damaged
plants caused yet undamaged corn plants to produce JA and
VOCs more intensively and rapidly in respon se to caterpillar-
caused damage compa red with plants that wer e damaged
without this pre-treatment.
The type of feeding damage clearly affects the VOCs
produced, and a part of the biochemical explanation is that leaf
chewers in general induce only JA signaling, while piercing-
sucking herbivores and pathogens tend to induce salicylic acid-
mediated resistance pathways as well (Smith and Boyko, 2007).
Indications for a role of JA for pathogen defense in potato arose
from reports that exogenous application of JA leads to local and
systemic protection against subsequent pathogen attack (Cohen et
al., 1993; Pozo et al., 2004). The blend of volatile compounds
emitted by tomato plants infested with the potato aphid
(Macrosiphum euphorbiae Thomas) has been studied compara-
tively with undamaged and aphid-infested plants. Aphid-infested
plants were significantly more attractive towards Aphidius ervi
Haliday than undamaged plants. However, collection of the
volatiles and analysis by gas chromatography revealed only
quantitative differences between uninfested and aphid-infested
plants (Sasso et al., 2007; Guerrieri and Digilio, 2008).
Also plant pathogens induce the production of VOC, which
because of their antimicrobial activities probably inhibit the
spread of the pathogen into plant tissues. In addition, tomato
mutants deficient in the biosynthesis of the octadecanoid pathway
are highly susceptible to small leaf-feeding mites and thrips
whereas MeJA treatment restores resistance (Holopainen, 2004).
Several tomato VOCs produced by leaves such as 2-hexenal, 2-
nonenal, 2-carene, β-caryophyllene, β-phellandrene, guaiacol,
MeSA, benzyl alcohol, and eugenol, are effective in inhibiting the
pathogen Botrytis cinerea. Among these constituents, 2-hexenal
and 2-nonenal showed the strongest inhibitory effect. Some
VOCs, such as 2-hexenal and MeSA, are plant-produced signals
that activate plant defense genes (He et al., 2006).
In general, VOCs can be considered as infochemicals that
mediate many interactions in a plant–insect community, both
above and below ground (Bezemer and van Dam, 2005).
Because volatile isoprenoids are reactive, and are likely to
undergo rapid changes and transformations (physical, chemical
and/or biological) in the soil system, a considerabl e proportion
of rhizosphere sources of VOCs may not diffuse through soil to
the atmospher e (Lin et al., 2007). Feeding on roots even can
induce changes in the volatile bouquet released from the aerial
parts of a plant, although the ecological relevance of this
observation remains elusive (Soler et al., 2007a, b) and the
potential abund ance and specific effects of VOCs in the
rhizosphere environment are still not known. Due to the lack of
reliable sampling, there have been few direct measurements of
monoterpene emissions or exudations from root systems in
natural environments, or even from roots of plants growing in
pots (Lin et al., 2007). The rhizosphere of Pinus species is a
strong and previously un-characterized source of volatile
isoprenoid emissions and these are likely to impact significantly
on rhizosphere function (Lin et al., 2007). In general, below
ground interactions and their putative impact on above ground
events and activities (and vice versa) is a topic of increasing
interest and worth to be more intensively investigated
(Mithoefer et al., 2009). Even below ground the emission of
volatiles is an efficient trait: in maize roots the sesquiterpene
(
E)-β-caryophyllene is necessary to attract entomopathogenic
nematodes to roots damaged by the ferocious maize pest
Diabrotica virgifera virgifera Le Conte (Fig. 3). Maize varieties
that lack this signal have been shown to be far more vulnerable
to maize pest (Rasmann et al., 2005; Rasmann and Turlings,
2007). In Vetiver roots, emission of a complex blend of
sesquiterpene hydrocarbons and alcohols repels insects and
protect the plant from microbial attacks ( Maffei, 2002; Del
Giudice et al., 2008). Studying the effects of belowground
herbivory on aboveground tritrophic signaling and vice-versa
emphasizes the important role of plants in bridging interactions
between spatially distinct components of the ecosystem
(Rasmann and Turlings, 2007).
Plants that are merely primed for enhanced defense after the
reception of distress signals, for example via VOCs from nearby
plants or adjacent leaves, are better protected in an environment
of herbivore pressure, without suffering from costly energy
investments in defense mechanisms. The phenomenon of
volatile-induced priming against insects also fits in the ecolo-
gical context of costs and benefits. Therefore, an additional
agronomical benefit can be expected if the emissions of the
appropriate volatiles were to be enhanced in crop plants
(Turlings and Ton, 2006).
Plant VOCs that have elicited antennal responses were also
attractive to parasitoids in behavioral experiments. The summed
618 M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

neural activity of antennal olfactory receptors can be measured
using the gas chromatography-electroantennographic detection
(GC-EAD) technique. Using plants upon which herbivores are
feeding and investigating by GC-EAD the VOCs released, it is
possible to identify a range of compounds that are electrophys-
iologically active and which may subsequently prove to be
Fig. 1. Secretory structures producing VOCs in higher plants. (A) Capitate glandular trichome present on the leaf surface of Mentha lavanduliodora Sacco. (B) DAPI
staining reveals polymorphic nuclei in the secretory cells of capitate glandular trichomes in Mentha x piperita L. (C) Cross-section of a biseriate peltate glandular
trichome of Artemisia annua L.; arrows indicate a dense osmiophilic deposit in the extracellular space facing the secretory cells [(from Duke et al., 2000), reprinted
with permission]. (D) Cross section of a monoseriate peltate glandular trichome of Mentha spicata L.; the essential oil accumulates in the subcuticular space between
the cuticle and the secretory cell's cell wall. Oil droplets accumulate and merge into a single essential oil deposit. (E) Scanning electron microscopy view of developing
stages of peltate glandular trichomes in M. lavanduliodora Sacco; young trichomes show cell divisions and the lack of essential oil accumulation. (F) Scanning electron
microscopy view of a mature peltate glandular trichome in M. lavanduliodora showing particulars of the stalk cell. (G) Needles of gymnosperms show the presence of
resin ducts; arrow indicates the cavity where resin is secreted. (H) Citrus fruit skin shows the presence of secreting cavities of lysigenous origin. (I) Cross-section of a
Vetivceria zizanioides root stained with Sudan Black B, showing oil-producing cells within the last layer of the cortical parenchyma. (J) Scanning electron micrograph
of conical cells from the inner epidermis of Antirrhinum flower petals [from (Kolosova et al., 2001), reprinted with permission)]. bc = basal cell; cu = cuticle; E =
endodermis; eo = essential oil-storing cells; O = drop of essential oil; sc = secretory cell; st = stalk cell.
619M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

active in behavioural assays as repellents of insect pests
(Mithoefer et al., 2009). Although electrophysiological techni-
ques have the advantage of online identification of the
electrophysiologically active VOCs, these compounds are not
always behaviorally active to insects ( Bjostad, 1998). The
behavioral significance of these compounds therefore needs to
be evaluated in behavioral experiments. Y-tube olfactometric
assays demonstrated that headspace volatile extracts collected
from leaf miner-damaged, or artificially damaged, bean plants
were more attractive to naive females of the parasitoid insect
Opius dissitus than those collected from healthy plants (Bjostad,
1998).
Aerial interaction of the wild tobacco (N. attenuata)
and sagebrush (Artemisia tridentata subsp. Tridentate Nutt.)
is the best-documented example of between-plant signaling via
above-ground VOCs in nature but at the same time highlights
the difficulty of predicting how plant–plant signaling functions
from first principles (Baldw in et al., 2006)(Table 1).
5.2. Plant VOCs and responses to abiotic stress
Independent of tissue damage by other organisms, numerous
plants emit VOCs in response to light and temperature changes
or other abiotic stresses, like flooding or drought (Ebel et al.,
1995; Holzinger et al., 2000; Kreuzwieser et al., 2000;
Gouinguene and Turlings, 2002; Teuber et al., 2 008).
Environmental effects on the emission responses can be caused
by temperature-dependent increases in the volatility and
diffusion rates of specific compounds or by the pool size of
specific leaf volatiles (Niinemets et al., 2004). However, the
composition of the herbivore-induced volatiles also strongly
depends on other abiotic factors, such as the availability of
nitrogen and phosphorous (Schmelz et al., 2003), soil salinity
and pH as well as air humidity (Vallat et al., 2005). In fact,
limited water availability can restrict VOC biosynthesis, while
more severe drought reduces emissions (Owen and Penuelas,
2005). Furthermore, the treatment of some plants with heavy
metals (Hg
2+
,Cu
2+
, and Fe
3+
) results in a characteristic blend of
volatiles (Engelberth et al., 2001).
The elevating atmospheric CO
2
concentration results in the
warming of the lower atmosphere, which might lead to a higher
emission of VOCs from plants and other factors, such as
temperature, light and herbivores might conceal the effects of
CO
2
(Scholefield et al., 2004; Vuorinen et al., 2005). However,
VOC emissions that are induced by the leaf-chewing herbivores
are not always influenced by elevated CO
2
concentration
(Vuorinen et al., 2004). Leaf photos ynthetic properties may
confer a valuable basis to model the seasonal variation of VOC
emission capacity; especially in tropical regions where the
environmental conditions vary less than in temperate regions
( Kes selmeier e t al., 200 2; Kuhn et al., 2004). Further
consequences of reduced photosynthetic gas exchange and
maintaining VOC emissions are a very high carbon loss, up to
50%, from VOC emissions related to net CO
2
uptake and a
Fig. 2. The volatilome tree. Branch (A) VOCs are produced by different biochemical pathways. The MEP pathways give rise to the formation of monoterpenes and
diterpenes. The latter are precursors of the homoterpene TMTT and of the caroteoid-derived β-ionone. Isoprene is generated from DMAPP. Branch (B)
sesquiterpenoids are generated by FPP derived from the cytosolic MVA pathway. The homoterpene DMTT derives from the sesquiterpene nerolidol. Branch (C)
oxylipins generate from fatty acids which are cleaved into GLVs and JA derivatives. Branch (D) the volatile indoles generate from anthranilate. Branch (E) aromatic
VOCs such as eugenol derive from phelylpropanoids, whereas MeSA derived from SA generated from benzoic acid. Branch (F) alternatively, MeSA can be formed by
methylation of SA deriving from isochorismate.
620 M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

strong increase in leaf internal isoprene concentrations (Teuber
et al., 2008). It has been demonstrated that transgenic non-
isoprene-emitting poplars show reduced rates of net assimilation
and photosynthetic electron transport during heat stress, but not
in the absence of stress. The decrease in the efficiency of VOCs
has b een inversely correlated with the increase in heat
dissipation o f absorbed light energy, me asured as non-
photochemical quenching (NPQ). Down-regulation of isoprene
emission has been shown to affect thermotolerance of
photosynthesis thus inducing increased energy dissipation by
NPQ pathways (Behnke et al., 2007). It has been hypothesized
that VOCs like isoprene may stabilize thylakoid membranes
and/or may exert antioxidant properties thus increasing plant
tolerance to environmental stresses. The involvement of
isoprene in non-enzymatic plant defense strategy has also been
suggested ( Velikova, 2008). Isoprene appears to act on
photosynthetic membranes to protect against thermal damage
(Singsaas and Sharkey, 2000; Sharkey et al., 2001).
Although the phytotoxic impact of ozone on plants has been
well documented, the effect of O
3
on plant VOC emissions has
received little attention. Chronic exposure to moderately
increased concentrations of ozone on insect induced terpene
Fig. 3. Functional role of plant VOCs. Plants emit a wide array of volatile compounds for pollinator's attraction and in response to biotic and abiotic stress. Flowers
emit compounds belonging to several major classes of VOCs to attract pollinators (Knudsen et al., 2006). Extrafloral nectaries attract both ants and butterlies and their
activation is inducible by insect herbivory (Kost and Heil, 2008). Several beetles, such as Chrysomela menthastri and C. hyperici, feed on aromatic plants despite their
toxic compounds and induce increased VOC plant emissions. Aphids feeding on plants trigger the emission of several monoterpenes and homoterpenes (Sasso et al.,
2007). Sucking herbivore like spider mites induce VOC emissions that attract their predators (Arimura et al., 2000). Chewing herbivores like Spodoptera littoralis
induce the plant emission of several monoterpenes, sesquiterpenes and homoterpenes that attract predatory wasps (Arimura et al., 2000). Oviposition-induced plant
volatiles and contact cues for host and prey location of parasitoids and predators (Hilker and Meiners, 2006). Insect-induced belowground plant signals include the
emission of several sesquiterpenoids which strongly attracts an entomopathogenic nematodes (Rasmann et al., 2005). Plant–bacteria interactions promote plant
synthesis of sesquiterpenoid precursors that are eventually transformed into an array of chemically diverse VOCs (Del Giudice et al., 2008).
621M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

Table 1
Some selected examples of the functional role of plant volatilome.
VOC class Biochemical
pathway
Biosynthetic site
(tissue types)
Defense
compound
name;
Constitutive (C),
Induced (I)
Structure formulae Infochemical interactions Reference
Emiterpene MEP Chloroplast
(mesophyll
cells)
Isoprene (C,I)
Thermotolerance. (Sharkey et al., 2008;
Velikova, 2008)Tolerance of ozone and other
reactive oxygen species.
‘Safety valve’ to get rid of
unwanted metabolites.
Apocarotenoid MEP and
carotenoid
cleavage
products
(CCPs)
Necrotic lesions
of leaf tissues;
flowers
β-ionone (C, I)
Repellent against Phyllotreta
cruciferae.
(Bouvier et al., 2005;
Gruber et al., 2009)
Inhibits mitochondrial
respiration.
Inhibits the sporulation and
growth of the fungus
Peronospora tabacina.
Attracts pollinators.
Homoterpene MEP Herbivore and
microbe wounded
tissues.
4,8,12-
trimethyltrideca-
1,3,7,11-tetraene
(TMTT) (I)
Involved in indirect defence in a
number of plants, such as maize
[Zea mays (L.)], tomato
(Solanum lycopersicum L.),
lima bean (Phaseolus lunatus
L.), and broad bean (Vicia faba L.).
(Arimura et al., 2009;
Moraes et al., 2009)
Induced by treatment with jasmonic
acid, 12-oxo-phytodienoic acid
(OPDA), or linoleic acid.
Monoterpene MEP Glandular
trichomes,
mesophyll
wounded tissues,
chloroplasts
Linalool (C, I)
Repels aphids. (Kleinhentz et al.,
1999; Degenhardt and
Gershenzon, 2000;
Aharoni et al., 2005;
Webster et al., 2008)
Electrophysiologically active
compound.
Alarm pheromone inhibitor.
Increases after attack from
Dioryctria sylvestrella.
Released from maize by Spodoptera
exigua damage.
Monoterpene MEP Glandular
trichomes,
mesophyll
wounded tissues.
Terpinen-4-ol
(C, I)
Causes a significant increase in male
Eupoecilia ambiguella upwind
flying to the pheromone source.
(Tunc and Erler, 2003;
Stamopoulos et al.,
2007; Schmidt-Busser
et al., 2009)Elicits electroantennogram
responses.
Displays toxic effects against
Tribolium confusum fecundity and
egg hatchability.
Monoterpene MEP Glandular
trichomes, resin
ducts, mesophyll
wounded tissues.
α-pinene (C, I)
Repels the spruce beetle
Dendroctonus rufipennis at high
concentrations, but intermediate
concentrations elicit entry and
gallery construction.
(Erbilgin and Raffa,
2001; Bichao et al.,
2003; Wallin and
Raffa, 2004)
Elicits olfactory receptor neurons of
the weevil Pissodes notatus.
Enhances attraction by Thanasimus
dubius, Platysoma cylindrica, and
Corticeus parallelus to the pheromones of
their Ips prey.
Monoterpene MEP Glandular
trichomes,
mesophyll
wounded tissues.
β-ocimene (C, I)
Exposure of Arabidopsis thaliana to
the monoterpene causes increased
abundance of several gene transcripts
and increased plant resistance against
the pathogen Botrytis cinerea.
(Faldt et al., 2003;
Arimura et al., 2004,
2009; Godard et al.,
2008)
Genes of the octadecanoid pathway
and genes known to respond to
octadecanoids are among the most
prevalent within the stress-gene
category up-regulated in Arabidopsis.
The β-ocimene synthase is induced in
622 M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

Table 1 (continued)
VOC class Biochemical
pathway
Biosynthetic site
(tissue types)
Defense
compound
name;
Constitutive (C),
Induced (I)
Structure formulae Infochemical interactions Reference
Lotus japonicus plants infested with
two-spotted spider mites
(Tetranychus urticae).
Monoterpene MEP Glandular
trichomes,
secretory ducts,
mesophyll
wounded tissues.
Limonene (C, I)
Induced oviposition on aphid-free
plants.
(Barnola et al., 1997;
Bichao et al., 2003;
Verheggen et al.,
2008)
Selection of the oviposition site by
predatory hoverflies relies on the
perception of a volatile blend
composed of prey pheromone and
typical plant green leaf volatiles.
Elicits olfactory receptor neurons of
the weevil Pissodes notatus.
Involved in the selective herbivory on
the conifer Pinus caribaea by the leaf-
cutting ant Atta laevigata.
Monoterpene MEP Glandular
trichomes,
mesophyll
wounded tissues
p-cymene (C, I)
Elicits a response of receptors on
Bemisia tabaci (whitefly) antennae as
determined by electroantennography.
(Janmaat et al., 2002;
Park et al., 2003;
Bleeker et al., 2009)
Significantly higher in tomato lines
with a higher repellence level.
Toxic agent for the western flower
thrips (Frankliniella occidentalis).
Repellent against mosquitoes.
Sesquiterpene MVA Glandular
trichomes,
secretory cells,
mesophyll and
root wounded
tissues
β-caryophyllene
(C, I)
Elicits electroantennogram responses. (Barnola et al., 1997;
Bichao et al., 2003;
Del Giudice et al.,
2008; Webster et al.,
2008; Mayer et al.,
2008a,b; Schmidt-
Busser et al., 2009;
Degenhardt et al.,
2009; Abel et al.,
2009)
Involved in insect host location.
Involved in the selective herbivory on
the conifer Pinus caribaea by the leaf-
cutting ant Atta laevigata.
Below ground signal emitted by insect-
damaged maize roots.
Induced by a plant pathogen and
perceived by its vector insect, the
phloem-feeding psyllid Cacopsylla
picta.
Biotransformed by plant-hosted
bacteria.
Released by Arabidopsis upon insect
feeding.
Sesquiterpene MVA Glandular
trichomes,
secretory cells,
mesophyll and
root wounded
tissues
β-farnesene
(C, I)
Common aphid alarm pheromone, the
major example of defence
communication in the insect world.
(Pare and Tumlinson,
1997a; Kunert et al.,
2005; Webster et al.,
2008; Verheggen et al.,
2008; Imbiscuso et al.,
2009)
Produced in response to feeding
Spodoptera littoralis on the fern Pteris
vittata.
Behavioral and electrophysiological
responses of winged Aphis fabae to
volatiles of faba bean.
Biosynthesized de novo following
insect damage.
Sesquiterpene MVA Glandular
trichomes,
secretory cells,
mesophyll and
root wounded
tissues
α-humulene
(C, I)
Produced in high amounts in response
to simultaneous herbivory by the
piercing–sucking insect western flower
thrips Frankliniella occidentalis and the
chewing herbivore Heliothis virescens.
(Delphia et al., 2007;
Abel et al., 2009)
Produced by a recombinant insect-
induced gene (AlCarS) with high
sequence similarity to the florally
expressed (E)-β-caryophyllene
synthase.
(continued on next page)
623M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

Table 1 (continued)
VOC class Biochemical
pathway
Biosynthetic site
(tissue types)
Defense
compound
name;
Constitutive (C),
Induced (I)
Structure formulae Infochemical interactions Reference
Sesquiterpene MVA and
MEP
Glandular
trichomes,
secretory cells,
mesophyll
wounded tissues
E-nerolidol
(C, I)
Precursor of DMNT. (Degenhardt and
Gershenzon, 2000;
Pophof et al., 2005;
Bartram et al., 2006;
Ibrahim et al., 2008)
Released from maize by Spodoptera
exigua damage.
Induced in transgenic Bt (expressing the
cry1Ac endotoxin gene) and
conventional oilseed rape leaves infested
with the third instar larvae of Bt-
susceptible Plutella xylostella.
Induces specific responses in the sensilla
trichodea of the Cactoblastis cactorum
females.
Homoterpene MVA and
MEP
Herbivore and
microbe wounded
tissues.
4,8-
dimethylnona-
l,3,7-triene
(DMNT) (I)
Detected in the headspace of many plant
species after herbivory.
(Degenhardt and
Gershenzon, 2000;
Tscharntke et al.,
2001; Kappers et al.,
2005; Vuorinen et al.,
2007; Carroll et al.,
2008; Mantyla et al.,
2008; Arimura et al.,
2009; Kigathi et al.,
2009; Joo et al., 2010)
Active components in mediating a
possible interplant signal transfer.
Increases in Fagus sylvatica L. in the
presence of the aphid Phyllaphis fagi L.
Emitted by Trifolium pratense (red
clover) after herbivory by Spodoptera
littoralis caterpillars.
Major volatile induced in cowpea by
neonate fall armyworms, Spodoptera
frugiperda, herbivory.
Used by birds to locate insect-rich trees in
the wild.
In birch, leaf fungal pathogen
Marssonina betulae does not induce
emission as in leaves damaged by larvae
of Epirrita autumnata.
Sesquiterpene MVA Root secretory
cells
Vetiverol (C, I)
Produced in root cells upon bacterial
transformation.
(Zhu et al., 2001;
Maffei, 2002; Del
Giudice et al., 2008;
Bhatia et al., 2008)
Toxic to insects and mammals (rats, mice,
rabbits).
Potent skin irritant.
Phototoxic.
Fatty acid
derivatives,
GLV
Oxylipin
pathway
Herbivore and
microbe wounded
tissues.
Hexenyl-acetate
(I)
Induces extrafloral nectar secretion. (Loughrin et al., 1994;
Azuma et al., 1997;
Farag et al., 2005; Heil
et al., 2008)
Increases in response to insect feeding.
Jasmonates Oxylipin
pathway
Secretory tissues,
herbivore
wounded tissues.
Methyl-
jasmonate (C, I)
Released in response to wounding and
herbivore attack.
(Pozo et al., 2004;
Kessler et al., 2006;
Wasternack, 2007;
Katsir et al., 2008)
The potency of MeJA as an exogenous
elicitor of COI1-dependent responses
likely reflects its efficient uptake and in
vivo conversion to bioactive JA–amino
acid conjugates.
The complex interplay with the alarm
signals salicylic acid and ethylene
provides plants with a regulatory
potential that shapes the ultimate outcome of
plant–microbe and plant–insect interactions.
Induces accumulation of proteinase
inhibitor (PIN2).
Induces swelling of mitochondria and
release of cytochrome c.
Indoles Anthranylate
pathway
Wounded tissues Indole (I)
Biosynthesized de novo following insect
damage.
(Pare and Tumlinson,
1997a; Frey et al.,
2000; Gouinguene
and Turlings, 2002)
Triggered by the fatty acid derivative
volicitin in maize.
Is attractive to Cortesia marginiventris,a
624 M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

emissions indicated only very small changes in emissions, but
showed induction of some terpenes, particularly the monoterpene
β-ocimene and the homoterpene DMNT, in response to insect
feeding (Blande et al., 2007). O
3
can affect phytophagous insect
performance and behavior due to changes in the plant physiology
and chemistry and the destruction of olfactory cues, disrupting
insect chemical communication (Pinto et al., 2007a,b). Recent
laboratory studies have shown that exposing Lima bean to ozone
increases the emission of the homoterpenes DMNT and TMTT,
emissions of which are also induced by spider mite (Tetranychus
urticae Koch) feeding (Vuorinen et al., 2004). By using a free-air
ozone concentration enrichment (FACE) it was found that
enhanced O
3
levels activate chemical defenses of some plants,
resulting in altered VOC emission profiles, and that a combination
of abiotic and biotic stress may substantially increase VOC
emission (Blande et al., 2007).
6. Plant VOCs and pollinators' attraction
In order to attract pollinators, plants have evolved the ability
to produce a mind-boggling array of VOCs that have also found
abundant use for humans when collected as essential oils.
Habitat location is generally mediated by long-range cues, such
as plant volatiles or herbivore pheromones perceived by
olfaction, where as cues used in the closer vicinity are mostly
short-range cues of herbi vore products or of the plant surface
often perceived by gustatory receptors (Fatouros et al., 2008).
The role of VOCs produced by flowers as chemical attractants
used to draw in their often highly-specific pollinators has
recently been docum ented, by examining how these compounds
are produced in flowers, detected by potential pollinators, and
how biotechnology can be used to alter their activity (Cseke et
al., 2007). Since floral VOCs are part of pollination syndromes
they represent a very crucial factor to ensure sexual reproduc-
tion (Pichersky and Gershenzon, 2002). Moreover, the ability of
flowers to attract pollinators from a distance is the reason why
VOCs have been retained through natural selection and are
found in floral scents (Caissard et al., 2004).
In general, pollinators respond mainly to olfactory cues and
researchers have focused on pollinator attraction through
combinations of specific floral traits, such as scent and color,
in the form of pollination syndromes (Raguso et al., 2003).
Visual and olfactory cues often function synergistically to
attract pollinators (Majetic et al., 2007) and VOC s are especially
useful at night when visual cues become insufficient. The
potential impact that pollinators, conserved biosynthetic path-
ways, and the genetics of small colonizing po pulations may
have in determining population-specific associations between
floral color and floral scent has been demonstrated (Majetic
et al., 2007).
As pollinator attractants, VOCs are important cues that help
insects locate flowers and signal the presence of food or mates.
The floral scent chemical compositions of hundreds of species
have been enumerated; however, only recently has the
molecular genetic basis of the biosynthesis of these compounds
begun to be elucidated (Barkman, 2003). Although it seems
self-evident that flowers emit scent to attract pollinators, there
has been little experimental work to demonstrate the attractive-
ness of individual scent compo nents to specific pollinators. The
role of individual volatiles in pollinator attraction has been
Table 1 (continued)
VOC class Biochemical
pathway
Biosynthetic site
(tissue types)
Defense
compound
name;
Constitutive (C),
Induced (I)
Structure formulae Infochemical interactions Reference
parasitic wasp that attacks larvae of
several species of Lepidoptera.
Phenyl-
propanoids
Cinnamate
pathway
Glandular
trichomes and
other secretory
structures.
Eugenol (C, I)
Produced by plants as defense compound
against animals and microorganisms and
as floral attractants of pollinators.
(Huang et al., 2002;
Koeduka et al., 2006;
Chaieb et al., 2007; Del
Fabbro and Nazzi,
2008; Kang et al., 2009;
Bhardwaj et al., 2010)
Larvicidal activity against the tobacco
armyworm, Spodoptera litura.
Repellent against female Culex pipiens
pallens adults and against the tick Ixodes
ricinus L.
In addition to its antimicrobial,
antioxidant, antifungal and antiviral
activity, possesses antiinflammatory,
cytotoxic, and anaesthetic properties.
Semiochemical Cinnamate
and
isochorismate
pathway
Wounded tissues Methyl-
salicylate
Required for systemic acquired resistance
signal perception in systemic tissues.
(James and Price, 2004;
Zhu and Park, 2005;
Park et al., 2007;
Webster et al., 2008;
Schmidt-Busser et al.,
2009)
Increase populations of predators and
decreased populations of spider mites in
grape vineyards and hop yards.
In field tests, traps baited with methyl
salicylate were highly attractive to adult
Coccinella septempunctata.
625M.E. Maffei / South African Journal of Botany 76 (2010) 612–631

elegantly tested by genetic manipulation of floral emission
using appropriate mutants and transformants (Pichersky and
Gershenzon, 2002).
In the case of obligate and specific plant–pollinator
relationships, the role of floral signals may be cruci al in
allowing the encounter of the partners. A clear demonstration of
floral scent–insect interaction is found in the fig tree (Ficus
spp.). Because associations between figs and their pollinating
wasps are horizontally transmitted, partner encounter is a
crucial step, and is mediated by the emission by receptive figs of
the volatile compounds that are detected by the pollinator
(Proffit et al., 2008). About 750 Ficus species (Moraceae) are
involved in such interactions, each with a distinct species of
pollinating wasp (Chalcidoidea, Agaonidae). In some cases
pollinators of some species are stimulated by the odor of their
associated fig species and generally not by the odor of another
species (Grison-Pige et al., 2002). In this contex t, the ability to
manipulate floral scent provides a better understanding of
qualitative and quantitative changes in VOCs and of the roles of
individual volatiles in pollinator attraction. This will also enable
to broaden the pollinator attractiveness of important crops that
rely on a lim ited range of insect species for their pollination that
cannot be cultivated outside of their natural habitat without
additional expenses being invested in artificial pollination
techniques. Moreover, customizing floral scent for specialized
pollinators will reduce the chance of pollen loss and
unsuccessful interspecific pollination, thereby increasing plant
reproductive success (Dudareva et al., 2006).
Floral scent headspace samples show the presence of
thousands chemical compounds belonging to seven major
compound classes, of which the aliphatics, the benzenoids and
phenylpropanoids, and, among the terpenes, the mono- and
sesquiterpenes, occur in most orders of seeds plants (Knudsen
et al., 2006)(Fig. 3). The most common single compounds in
floral scent are the monoterpenes limonene, β-ocimene, β-
myrcene, linalool, α-pinene, β-pinene, and the benzenoids
benzaldehyde, MeSA, benzyl alcohol, and 2-phenyl ethanol, the
sesquiterpene β-caryophyllene and the irregular terpene 6-
methyl-5-hepten-2-one (sulcatone ) (Knudsen et al., 2006).
Floral VOCs also provide important guides in the nectar-
seeking behavior of butterflies and compounds may have
evolved as adaptations to attract pollinating butterflies, thus
eliciting a high attractiveness for foraging butterflies (Anders-
son and Dobson, 2003). For example, lilac aldehyde is also
known to elicit strong antennal signals in butterfly species. This
compound is emitted in high amounts, especially in nocturnal
plant species, and it is known to be highly attractive to the
nocturnal moth species Autographa gamma L. and Hadena
bicruris Hufn. (Dotterl et al., 2006). Although electrophysio-
logical techniques have the advantage of onli ne identification of
the electrophysiologically active components of volatile blends,
these compounds are not always behaviorally active to insects
(Bjostad, 1998). Compounds both present in relatively high
abundance in the floral scents and detected exclusively in the
floral parts of the plant, such as linalool, linalool oxide
(furanoid) I and II, oxoisophoroneoxide, and phenylacetalde-
hyde, elicited the strongest insect antennal responses, suggest-
ing that they may reflect adaptations by the plant to attract
butterfly pollinators (Andersson and Dobson, 2003).
7. Concluding remarks
A growing body of evidence indicates that VOCs are
important signaling mol ecules and the deciphering of this
chemical information will be of paramount importance for the
early detection of plant responses to biotic and abiotic stress,
allowing the search for new sustainable methods for pest and
environmental control.
Research on the volatile emission by plants shows that VOCs
are very potent signaling molecules that have evolved to serve
multiple funct ions. As the great majority of cellular signals
origin from membrane proteins within a lipohilic environment,
volatile lipids may be privileged to interact with such processes.
This is shown by the fact that several VOCs are able to
modulate both plant and animal signal transduction pathways.
The production of a highly complex blend of VOCs may have
started with a plant defense strategy to later evolve to also
regulate plant–insect interactions.
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Edited by AM Viljoen
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