Abiotic stresses and induced BVOCs

Abstract

Plants produce a wide spectrum of biogenic volatile organic compounds (BVOCs) in various tissues above and below ground to communicate with other plants and organisms. However, BVOCs also have various functions in biotic and abiotic stresses. For example abiotic stresses enhance BVOCs emission rates and patterns, altering the communication with other organisms and the photochemical cycles. Recent new insights on biosynthesis and eco-physiological control of constitutive or induced BVOCs have led to formulation of hypotheses on their functions which are presented in this review. Specifically, oxidative and thermal stresses are relieved in the presence of volatile terpenes. Terpenes, C6 compounds, and methyl salicylate are thought to promote direct and indirect defence by modulating the signalling that biochemically activate defence pathways.

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Special Issue: Induced biogenic volatile organic compounds from plants
Abiotic stresses and induced BVOCs
Francesco Loreto
1
and Jo¨ rg-Peter Schnitzler
2
1
Consiglio Nazionale delle Ricerche (CNR), Istituto per la Protezione delle Piante (IPP), Via Madonna del Piano 10, 50019 Sesto
Fiorentino, Firenze, Italy
2
Karlsruhe Institute of Technology (KIT), Institute of Meteorology and Climate Research (IMK-IFU), Kreuzeckbahnstraße 19,
82467 Garmisch-Partenkirchen, Germany
Plants produce a wide spectrum of biogenic volatile
organic compounds (BVOCs) in various tissues above
and below ground to communicate with other plants
and organisms. However, BVOCs also have various func-
tions in biotic and abiotic stresses. For example abiotic
stresses enhance BVOCs emission rates and patterns,
altering the communication with other organisms and
the photochemical cycles. Recent new insights on bio-
synthesis and eco-physiological control of constitutive
or induced BVOCs have led to formulation of hypotheses
on their functions which are presented in this review.
Specifically, oxidative and thermal stresses are relieved
in the presence of volatile terpenes. Terpenes, C6 com-
pounds, and methyl salicylate are thought to promote
direct and indirect defence by modulating the signalling
that biochemically activate defence pathways.
The emission of BVOCs: few biochemical pathways but
many compounds emitted
Biosynthesis of the main BVOCs
Plants produce a wide spectrum of BVOCs in various
tissues above and below ground. Most BVOCs are largely
lipophilic and have enough vapour pressure to be released
into the atmosphere in significant amounts. The availabil-
ity of new methods of head-space sampling (such as solid
phase micro-extraction) in combination with gas chroma-
tography–mass spectroscopy and new techniques for on-
line analysis (proton transfer reaction-mass spectrometry)
[1] has led, in the last 15 years, to a significant expansion of
our knowledge on the occurrence and temporal and spatial
distribution of BVOCs emissions. At present, about 1700
substances have been found to be emitted from plants [2].
Nearly all organs from vegetative parts, as well as flowers
[3] and roots [4] emit these compounds. Many BVOCs are
emitted constitutively and the emissions can be observed
throughout the life cycle of the plant or, more often, at
specific developmental stages (e.g. leaf and needle matu-
ration, senescence, flowering, and fruit ripening). The
emission is biosynthetically controlled by abiotic factors
such as light and/or temperature, atmospheric CO
2
con-
centration, or nutrition. Other BVOCs are induced after
wounding and herbivore feeding or after environmental
stresses. Stresses may induce change of constitutive
BVOCs, either stimulating or quenching the emissions
(e.g. [5]) or may induce de novo synthesis and emission
of BVOCs. Induced emissions may occur in a systemic way,
i.e. away from the site of damage [6].
The biosynthesis of most BVOCs can be assigned to the
following three major pathways: terpenes (= isoprenoids),
oxylipins, and shikimate and benzoic acid [7,8]. Low mol-
ecular weight, C1 and C2, compounds, such as methanol,
ethanol, formaldehyde, and acetaldehyde can be synthes-
ized via other biosynthetic routes [9]. Two other BVOCs are
methane and ethylene. Emission of non-microbial methane
by vegetation has been discovered recently [10] and
research on this important topic is still in its infancy.
Recent isotope labelling studies provided evidence that
methane can be generated from methoxyl groups deriving
from breakdown of plant pectins [11].
In this review of the impact of abiotic factors on the
induction of BVOCs emissions, we will mostly concentrate
on volatile terpenes which are the most important com-
pounds for plant biology [12] and atmospheric chemistry
[13] because of their role in plant protection (e.g. in the
protection of photosynthesis against thermal and oxidative
stresses, and in direct and indirect defence against herbi-
vores), as well as in the chemical properties of the atmos-
phere (e.g. entering the cycle of photochemical production/
destruction of ozone, aerosols, and particles). The emission
of volatile terpenes is estimated to account for more than
half of the total emission of BVOCs [14] and is constitu-
tively ten times higher than other emissions, as heavy
emitters can release isoprene at rates of 50–100 nmol
m
2
s
1
, representing up to 2–5% of the photosynthetic
net carbon uptake in tree species. Volatile terpene emis-
sions are far more sustained than the emission of other
induced volatiles, for which emissions are transient by
nature and limited to specific periods after stress, depend-
ing on the damage experienced and on the activation of the
biosynthetic pathways producing the volatiles.
Biosynthesis of volatile terpenes
Terpenes are constitutively formed in some plant families
that store them in massive amounts in internal or external
structures (e.g. the resin ducts of conifers or the glandular
cells of Lamiaceae leaves). They may also be induced in
response to wounding or herbivory attack. The emission of
terpenes from storage structures is generally uncoupled
from photosynthesis as it may occur, for example, at night
[15].
Direct emission of isoprene or monoterpenes from the
mesophyll is common in some tree species (Figure 1), in
Review
Corresponding author: Loreto, F. (francesco.loreto@ipp.cnr.it).
154 1360-1385/$ –see front matter ß2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2009.12.006 Available online 4 February 2010

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particular from the Fagaceae and Salicaceae (oaks and
poplars) [16,17]. These emissions are light-dependent
[18,19] and are closely linked to the availability of photo-
synthetic intermediates [19,20]. The investigation of
volatile terpene biosynthesis is a very active area of plant
research, especially since the discovery and complete elu-
cidation of the methylerythritol (MEP) pathway, respon-
sible for the formation of the basic C5 units isopentenyl
diphosphate (IDP) and dimethylallyl diphosphate
(DMADP) in many bacteria and in the plastids of all
organisms from phototrophic phyla [21].
In plants, IDP and DMADP are formed via two alterna-
tive pathways: (i) in the cytosolic mevalonic acid (MVA)
pathway from acetyl-CoA, and (ii) in the plastidic MEP
pathway from pyruvate and glyceraldehyde-3-phosphate
[22]. Generally, the MEP pathway provides IDP and
DMADP for hemiterpene and monoterpene biosynthesis,
while the MVA pathway provides the C5 units for sesqui-
terpene formation. However, a very recent report has
revealed that the MEP pathway also contributes to sesqui-
terpene formation [23]. In addition, some metabolic
crosstalk between both biosynthetic routes is possible
[24] particularly (via IDP) in the direction from chloro-
plasts to the cytosol [25].
Prenyl transferases catalyze the condensation of IDP
and DMADP to form geranyl diphosphate (GDP) and
farnesyl diphosphate (FDP) [26]. Finally, the conversion
of DMADP, GDP, and FDP, into volatile hemi-, mono-, and
sesquiterpenes, respectively, is catalyzed by terpene
synthases (TPS), a large family of enzymes, encoded by
closely related genes [27]. Isolation and characterization of
prenyl transferase [28] and terpene synthase genes [29] is
now giving new insights into the evolutionary origin
[30,31] and genetic and biochemical regulation of terpene
biosynthesis.
Isoprene and 2-methyl-3-buten-2-ol (MBO), a hemiter-
pene common only in American western pines, [32] are
biochemically synthesized in chloroplasts by isoprene [33]
and MBO synthase [34] from DMADP. Due to the import-
ance of isoprene for atmospheric processes and plant func-
tions, isoprene synthase (ISPS) became one of the best
studied TPS [35]. A positive correlation between ISPS
activity and basal standard emission capacity was found
in different isoprene-emitting species [36,37].Uptonow,
five ISPS genes from different poplar (Populus) species or
poplar hybrids have been described [35]. The only ISPS gene
cloned so far from another genus, Pueraria montana (kudzu)
[38], shows only 52% identity with the poplar protein
sequences, although the structure of poplar and kudzu genes
are similar (six introns and seven exons) [38].AllISPS genes
belong to the subgroup b of the class 1 plant TPS-family
which includes monomeric mono-, sesqui-, and diterpene
synthases, grouped in six subgroups (Tspa–TspfTpsa–Tpsf?)
[27]. All known ISPS enzymes have a 10–100-fold higher
Michaelis constant (k
M
) for its substrate DMADP (in the
millimolar range) than monoterpene synthases for GDP [39]
or prenyltransferases for DMADP [40]. The low k
M
of pre-
nyltransferases may control the metabolic flux within the
MEP pathway because downstream reactions leading to
monoterpene and non-volatile terpene biosynthesis are
favoured over isoprene biosynthesis. Based on this finding,
it was suggested that isoprene emission occurs only when
plants’ need for ‘essential’, higher terpenes (hormones, e.g.
ABA and gibberellins; tocopherol; phytosterols; and photo-
synthetic pigments) are satisfied [41].
Interest in genetic regulation and biochemical proper-
ties of TPS other than ISPS mostly focused on those TPS
involved in the formation in storage structures (e.g. in
gymnosperms and Lamiaceae) of those terpenes with
defensive or attractive functions [42] (see Dicke and Bald-
win, this issue).
In light-dependent monoterpene emitters, the infor-
mation about TPS regulation is scant. Differences in mono-
terpene emission pattern of chemotypes and oak hybrids
[43], the seasonal development of monoterpene emission
[44,45], and the dependence of monoterpene emission on
atmospheric CO
2
[46] all appear to be controlled by TPS
activities. However, our knowledge about the underlying
genes is scarce; in oak, only two mono-TPS genes, a b-
myrcene synthase [47] and a multiproduct a-pinene
synthase [48] have been isolated and functionally charac-
terized up to now.
Figure 1. Origin of volatile terpene emissions from different leaf types. In
deciduous leaves of many tree species (e.g. oaks and poplars) with no specific
storage structures for terpenes, isoprene and monoterpene, BVOCs emissions
originate from mesophyll cells in a light- and temperature-dependent manner. In
conifer needles (e.g. Picea abies - Norway spruce) light-dependent terpene
emission stems from photosynthetic tissue and is superposed by a temperature-
dependent volatilization of terpenes from resin ducts. Lamiaceae (e.g. Ocimum
basilicum basil) leaves release temperature-dependent volatile terpenes from
external glandular cells. Confocal laser scanning microscopic images were taken
from cross-sections of Quercus robur (top), Picea abies (middle) and leaf surface of
Ocimum basilicum (bottom).
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The commonly used model plant Arabidopsis thaliana
(Arabidopsis) is a good example of how modern technol-
ogies can improve knowledge of BVOCs biosynthesis and
functions. In the past classified as ‘non-emitting’ species,
analysis of the Arabidopsis genome revealed the existence
of over 30 putative genes belonging to the multigene family
of TPS [49,50]. Most of these genes are almost exclusively
expressed in flowers [50,51], but low constitutive terpene
emissions from leaves and siliques [50,52] and even emis-
sions from roots (namely 1,8-cineole, [4]) could be detected.
Isoprene synthase overexpression in Arabidopsis allowed
verification of a ‘thermo-protective’ activity of isoprene
[53,54], see below, and indicated an ecological function
of this hemiterpene in plant–insect interactions as a repel-
ling cue [55]. The expression of b-caryophyllene was also
successfully engineered in this plant (J. Gershenzon,
personal communication) and may help assess functions
and fate of sesquiterpenes. Sesquiterpenes are not emitted
in large amounts constitutively, but their biosynthesis can
be induced by biotic stresses, and may be important as an
indirect defence mechanism (see Dicke and Baldwin, this
issue). Even at low concentrations sesquiterpenes are also
important as nucleation factors, eventually leading to
particle formation in the atmosphere [56].
Poplar is another seminal model system to study regu-
lation and function of plant volatiles. Besides ISPS [35],
only one TPS gene [()-germacrene-D synthase] [57] is
characterized. However, full length cDNAs [58], cDNA
microarrays [59,60], and a largely sequenced genome of
Populus trichocarpa [61] are now available, and these tools
will certainly allow for quick progress in the understanding
of BVOCs formation in a near future.
Biosynthesis of C1 and C2 oxygenated compounds
Volatile terpenes are certainly the family of compounds
that contributes the majority of BVOCs [14]. However,
short-chained oxygenated compounds (especially methanol
and acetaldehyde) are important components of constitu-
tive and induced emissions of many plants [5] with a large
presence globally [62].
Methanol is predominantly emitted because of degra-
dation and formation of cell wall pectins, e.g. (i) during cell
expansion in all types of plant tissue and seeds, and (ii)
during leaf abscission, senescence, and seed maturation
(Figure 2). The formation of methanol is catalyzed by
pectin methylesterases (PME) which, among the other
functions, demethoxylates pectin [63,64]. To a minor
extent, methanol emissions originate from protein meth-
yltransferase and protein repair reactions [65], or from
tetrahydrofolate metabolism [66]. Emission of methanol
can be induced by mechanical wounding [67] or herbivore
feeding, due to an upregulation of PME expression. This
finding has stimulated a discussion about whether metha-
nol might act as a signal in plant–plant communication
[68].
The metabolic origin of acetaldehyde emitted by forest
trees is still a matter of debate [69,70]. This compound
seems to be predominantly induced by stresses. It is known
that acetaldehyde emission correlates with root flooding
[71,72] and with xylem sap ethanol concentrations [73,74].
Ethanol formed under anoxic conditions in roots is trans-
ported to leaves by the transpiration stream, where it is
oxidized to acetaldehyde by alcohol dehydrogenase (ADH).
However, only a small portion of acetaldehyde is emitted
while the bulk is further metabolized by aldehyde dehydro-
genase (ALDH) to acetate and acetyl-CoA.
In some tree species, strong transient acetaldehyde
bursts during light–dark transitions have been reported
[70,72,75]. These acetaldehyde bursts are thought to be the
result of a ‘pyruvate overflow mechanism’ [75]. In the
proposed mechanism pyruvate decarboxylase (PDC) acts
as a metabolic regulator converting excess cytosolic pyr-
uvate into acetaldehyde, which is subsequently oxidized to
acetate. Such an excess of cytosolic pyruvate may be the
result of transiently decreased transport rates of pyruvate
equivalents [i.e. phosphoenolpyruvate (PEP)] into orga-
nelles, or reduced pyruvate utilization in leaf cells immedi-
ately after darkening [75]. However, emission of
acetaldehyde may also derive from cleavage of moieties
of C6 aldehydes, which emissions are also transiently
stimulated during light–dark transitions [70]. In this case,
acetaldehyde emission is independent of cytosolic pyruvate
and is part of the leaf response to wounding that also
includes biosynthesis of C6 compounds (see below).
Biosynthesis of C6 aldehydes and alcohols
Wounding induces the release of ‘green leaf volatiles’
(GLV) as can be easily sensed in the odour of fresh hay.
In most wounded plants GLV are C6 aldehydes, C6 alco-
hols, and their derivatives, often collectively called C6- or
LOX-products [76]. Physiologically these compounds have
Figure 2. Simplified scheme of the subcellular origin and biosynthesis of volatile
organic compounds upon abiotic stress. Abbreviations: CH
4
, methane; DMADP,
dimethylallyl diphosphate; DXS, 1-deoxy-D-xylulose 5-phosphate synthase (EC
4.1.3.37); FDP, farnesyl diphosphate; GDP, geranyl diphosphate; HMGR, 3-hydroxy-
3-methylglutaryl-CoA reductase (EC 1.1.1.34); 13-HPOT, 13S-hydroperoxy-
9(Z),11(E),15(Z)-octadecatrienoic acid; IDP, isopentenyl diphosphate; ISPS,
isoprene synthase (EC 4.2.3.27); a-LeA, a-linolenic acid; 13-LOX, 13-lipoxygenase
(EC 1.13.11.12); MeOH, methanol; MTS, monoterpene synthase (e.g. myrcene EC
4.2.3.14); PDC, pyruvate decarboxylase (EC 4.1.1.1); PEP, phosphoenolpyruvate;
PME, pectine methylesterase (EC 3.1.1.11); PYR, pyruvate; STS, sesquiterpene
synthase (e.g. epi-aristolochene EC 4.2.3.9); 13-HPL, 13-hydroxyperoxide lyase (not
listed in enzyme classification); TP, triose phosphate. The broken arrow indicates a
proposed, yet unidentified acetaldehyde emission path from chloroplasts.
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antibiotic properties inhibiting the invasion of damaged
tissue [77], and can serve a signalling function within
plants to induce or prime defence [78].
GLV are derived from oxidized polyenoic fatty acids
(PUFA), collectively called oxylipins. The initial formation
is catalyzed by lipoxygenases (LOX), a large gene family of
non-haeme iron containing fatty acid dioxygenases [8]
(Figure 2). LOXs (13-LOX, classified with respect to their
positional specificity of oxidation at carbon-13 of the fatty
acid hydrocarbon backbone) initiate the octadecanoic
pathway by adding O
2
stereospecifically to unsaturated
fatty acids [e.g. linoleic acid (18:2) and a-linolenic acid
(18:3)] generating 13-(S)-hydroperoxides. Subsequently,
13-(S)-hydroperoxide lyase (HPL) catalyzes the cleavage
between C12 and C13 releasing n-hexanal (from linoleic
acid) and (Z)-3-hexenal (from a-linolenic acid) which are
the parent compounds for all other aldehydes and alcohols,
and enzymatically acetylated compounds such as hexyl
acetate and (Z)-3-hexenyl acetate [76].AnalysisofC6
compounds is complicated by their chemical instability
and the transient nature of their formation after wound-
ing. Thanks to modern on-line techniques like proton
transfer reaction mass spectrometry (PTR-MS) that avoid
pre-concentration of the samples on adsorbent phases, the
rapid and transient emission of C6 upon various stimuli,
such as physical damage [79], light–dark transitions, her-
bivory, or senescence processes, can be easily monitored
[70,79].
Plants and abiotic stresses: how stresses affect BVOCs
biosynthesis and emissions
Abiotic stresses affect primary and secondary metabolism
in different ways. Stresses generally inhibit photosyn-
thesis by reducing CO
2
uptake and diffusion inside leaves
to the site of fixation into carbohydrates or by altering the
photochemical or biochemical reactions of the photosyn-
thetic cycle [80]. The impact of stresses on the secondary
metabolisms that produces BVOCs is more controversial,
as some of the pathways may be elicited by stresses. In the
case of volatile terpenes, the uncoupling of photosynthesis
and BVOCs emission is surprising, because of the well-
known high requirement of photosynthetic carbon for ter-
pene biosynthesis [81]. The stimulation of terpene pro-
duction is made possible by the activation of sources of
carbon which are alternatives to freshly fixed photo-
synthates and not yet fully identified. Some labelling
studies have provided evidence that isoprene may also
be formed from xylem-transported glucose and chloroplas-
tic starch [82]. However, under stress conditions, other
13
C
labelling studies point out that, because of starch
depletion, extra-chloroplastic sources of carbon may be
activated and feed carbon to volatile terpenes [83]. Stresses
may also induce damage that elicits or induces the syn-
thesis of other volatiles with important consequences for
plant protection, directly against the environmental con-
straint [12] or indirectly, against possible, associated
bursts of pathogens and herbivores (see Dicke and Bald-
win, this issue). The impact of the main environmental
factors of stress on the biosynthesis and emission of vola-
tiles will be reviewed in the following sections (see also
Figure 3).
Temperature
BVOCs partition between the gas and liquid phase in the
plants according to their Henry’s law constant (k
H
), which
is generally very high (e.g. k
H
7500 Pa m
3
mol
1
at 25 8C
for isoprene) [84]. The equilibrium between gas and aqu-
eous phases is indeed determined by the temperature and
therefore it is expected that more BVOCs enter the gas
phase and are emitted at rising temperatures. This direct
effect of temperature on BVOCs emission is, however,
modulated by diffusion resistances encountered from the
sites of synthesis inside the leaf to the atmosphere. BVOCs
that are stored in specialized structures (ducts or glands)
reach very high concentrations and are tightly separated
by the surrounding cells by an impermeable cell layer,
generally made by sub-cuticular cells [85]. This is because
high concentrations of BVOCs, which have probably
important ecological functions as deterrents of herbivores
and as anti-bacterial and anti-mycotic substances, could be
auto-toxic for plant cells [86]. Temperature affects the
evaporation and release of a minimal part of the pools of
BVOCs that leaks out the impermeable cell layer. Indeed
plants with large storage pools are moderate emitters
[15,17] unless the pools are opened up, e.g. by herbivory
[87], strong winds, or forest fires [88]. High humidity may
also lead to a swelling and to the consequent explosion of
the structures containing the pools. In this case strong
emissions of terpenes may even be sensed, e.g. walking on a
pine forest at sunrise.
On the other hand, plants that do not store BVOCs into
specialized structures have small temporary pools in the
leaf mesophyll that freely diffuse out of the leaf driven by a
concentration gradient. The only important constraint to
this diffusion is at the stomatal conductance to gas
Figure 3. Schematic overview of long-term and short-term regulation of terpene
emissions upon various abiotic stresses. Long-term adaptation of volatile terpene
emission (predisposition and/or priming) relates to differential gene expression
resulting in upregulation (green circles) and/or downregulation (red circles) of
specific enzymes and changed emission pattern and emission rates. Short-term
regulation reflects rapid changes in metabolic fluxes and enzyme kinetic properties
(e.g. temperature, pH and ion shifts, and redox/energy status) due to abiotic factors
like atmospheric CO
2
concentration, light and temperature. Orientation of arrows
in the green and red circles indicate strength of upregulation and downregulation.
Abbreviations: h, hours; min, minutes; s, seconds.
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exchange. High temperatures often affect stomatal beha-
viour, either per se or because this stress is generally
associated with a drought stress. Stomatal opening under
transient heat stress is an important mechanism to dis-
sipate latent heat through transpiration of water and to
uncouple the leaf temperature from air temperature. On
the other hand, stomatal closure improves instantaneous
water use efficiency (the ratio between net CO
2
assimila-
tion and transpiration) and avoids excessive loss of water
driven by increasing transpiration. Stomatal movements
do not affect the steady-state diffusion rates of gases with
high k
H
, such as isoprene and monoterpenes [84]. In the
case of stomatal closure, these compounds build up tran-
siently significant partial pressures inside leaves that
compensate for the increasing resistance at stomatal level
[89,90]. However, diffusion of gases that are mainly parti-
tioned into liquid phase, such as oxygenated VOCs (metha-
nol, C6 aldehydes, and alcohols) might be strongly
restrained by stomatal closure [87].
Temperature has a strong and immediate influence on
the activity of the enzymes that catalyze the synthesis of
many BVOCs. Emissions of volatile terpenes typically
have a Q10 = 2–4, at temperatures variable between 20
and 40 8C[91]. Thus the main effect of rising temperature
is a direct increment of the terpenes formed through
enzymatic reactions. However, when a heat stress occurs
with temperature above the optimal enzyme temperature
(around 40–45 8C for enzymes in the MEP pathway and
most TPS), then a very rapid inhibition of terpene emission
is observed [5]. This is probably due to downregulation or
impairment of primary metabolism and to the con-
sequently insufficient supply of photosynthetic metabolites
into the MEP pathway [92,93]. However, there are cases in
which the emission is not rapidly re-established upon heat
stress removal, and in these cases a heat-induced dena-
turation of the TPS is also likely to occur [5].
Interestingly, when the heat-induced inhibition of
volatile terpenes occurs, then the emission of other BVOCs
is highly enhanced [5]. This is particularly evident in the
case of methanol and C6 compounds, pinpointing that the
inhibition of volatile terpene emission coincides with the
occurrence of damage to cell walls and membranes,
respectively [5]. The emission of C6 compounds is sus-
tained for the whole period of heat stress and may continue
for a long time after temperatures go back to physiological
levels [5]. Significant fluxes of methyl-butenol, ethanol,
and acetaldehyde were found in North American conifers
exposed to high temperature [94], and methanol and
acetone emissions were also observed from bare agricul-
tural soils following a heat wave episode [95]. Thus soil
microorganisms may also contribute to the temperature-
dependent emission of oxygenated BVOCs.
Finally, temperature seems to have an important role in
determining emissions of methyl salicylate (MeSA), a sig-
nalling molecule whose induction is frequent in response to
biotic stresses [74,96]. One study [97] reported induction of
MeSA only after spraying plants with jasmonic acid,
another important signalling molecule activating the
induction of genes involved in hypersensitive responses,
both after biotic and abiotic stresses. In another study a
significant induction of MeSA, with fluxes comparable to
those of monoterpenes was observed in plants exposed to
night chilling temperatures [98] and the induction of this
compound correlated to the difference in temperature
between day and night that was experienced by walnut
(Juglans californica Juglans regia) plants.
Drought and salt
The impact of drought and salt on BVOCs emission is
surprising. These abiotic stresses directly affect stomatal
conductance and produce diffusive and biochemical limita-
tions of photosynthesis [79]. Both the reduction of photo-
synthesis and the stomatal closure are expected to
negatively impact on BVOCs emission by altering the
carbon supply into the MEP pathway and by increasing
resistance to their emission.
In fact, the emission of volatile terpenes is resistant to
these stresses and is often elicited by stress occurrence.
The original observation that isoprene is not reduced by
increasing drought stress until the stress becomes heavy
and almost completely inhibits photosynthesis [99] has
been repeatedly made, also with experiments in which
the drought stress has been controlled differently, e.g.
[90,100]. The sustained emission of isoprene to salt and
drought [101,102] is made possible by the induction of
carbon sources alternative to photosynthesis, possibly
related to respiration [103] or starch breakdown [82].
Labelling experiments with
13
CO
2
[35,83] demonstrate
clearly the preference of ‘old’ unlabeled (
12
C) carbon
skeletons over recently fixed,
13
C enriched photosynthetic
intermediates when photosynthesis (which is heavily
reduced by drought and salt stress) [83,101] and isoprene
biosynthesis become uncoupled. This may also explain why
in some instances re-establishment of photosynthetic
metabolism, by re-watering plants, results in a burst of
isoprene emission [99]. However, it has been shown [83]
that the alternative carbon sources rapidly cease to feed
carbon into the MEP pathway once the water status of
plants is reintegrated. A recent observation indicates that
in plants exposed to severe drought stress and in those
recovering from drought stress the temperature depen-
dency of isoprene emission is lost for at least several weeks,
if not permanently [100]. The mechanism behind this
observation is still unknown, but it is likely that the ISPS
protein is slowly or incompletely re-synthesized after the
stress [100]. Climate-change impact on isoprene emission
has been mainly attributed to positive long-term (enzy-
matic) and short-term (substrate) feedback of rising
temperature [104,105], implying that future emissions of
isoprene will also increase [106]. However, as drought is
often associated with heat waves and summer climate, the
finding that drought suppresses temperature-dependency
of isoprene emission may have consequences for trees’
thermal and ozone tolerance in regions (e.g. the Mediter-
ranean basin) which will be plagued by climate-change-
induced droughts associated with rising temperatures.
Laboratory measurements of the impact of drought on
monoterpene emissions are missing, but in field exper-
iments monoterpene emissions are inhibited by drought
stress [46,107,108]. Interestingly, the inhibition is particu-
larly evident only when drought stress is severe (e.g. the
water potential is less than –2 MPa) again suggesting that
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biosynthesis of volatile terpenes is resistant to mild
drought stress [109]. It is unclear whether alternative
carbon sources can be used to generate monoterpenes
under these conditions. As for temperature, heavily
drought-stressed oak plants lose the capacity to respond
to other environmental factors that are known to modulate
the emission, such as CO
2
(see below) [46].
Drought seems to have a different effect on pools of
monoterpenes stored in specialized structures or non-
stored in the mesophyll. In conifers, if the drought event
occurs in winter, when the biosynthesis of terpenes is
restrained by temperature, the pools appear to be nega-
tively affected. However, summer droughts can further
enrich the monoterpene pools. In non-storing species,
summer drought depletes the pools of terpenes in the
mesophyll which are under direct control of photosynthetic
carbon via the MEP pathway [110].
As described above, the emission of oxygenated BVOCs
depends on stomatal opening [84]. Stomatal closure in
response to drought and salt stress is therefore expected
to reduce particularly the emission of these compounds.
However, morning peaks of acetone and methanol emis-
sions may be very high in drought-stressed leaves, because
the temporary opening of stomata during times of higher
humidity allows the release of large pools of oxygenated
BVOCs that were built inside the leaf mesophyll [111,112].
Thus, drought stress does not inhibit per se the biosyn-
thesis of oxygenated BVOCs. Moreover, if the stress
reaches levels that are able to damage membranes and
cell walls, further increments of the emission of C6 com-
pounds and methanol must be expected. However, emis-
sion of these compounds has not been reported generally in
response to drought and salt [101]. Indeed, C6 emissions
occur in bursts, immediately after the damage to cellular
structures has occurred [5,113]. A recent experiment has
established a correlation between the emission of C6 vola-
tiles and the damage to membranes, as assessed by the ion
leakage, under a developing drought [114].
Ozone and other oxidants
In the atmosphere, volatile terpenes perform a dual action,
depending on the presence of anthropogenic pollutants.
When these compounds are absent, volatile terpenes
cleanse the atmosphere of ozone. In the presence of NO
x
,
however, these BVOCs initiate reactions leading to
increased ozone formation [13]. The chemical reactivity
of terpenes in the atmosphere led to the idea that volatile
terpenes play a similar dual action inside the leaves, before
they are released into the atmosphere [115,116].
In general, terpenes have been demonstrated to reduce
ozone damage and to quench ozone and reactive oxygen
species (ROS) [115–118]. The mechanism(s) by which this
protective effect occurs is still under investigation and the
prevalent theories will be discussed below. Here we con-
centrate on the impact of oxidative stresses on the emission
of BVOCs. If isoprene reacts with ozone and other oxidative
species then it is expected that it disappears, concurrently
with the appearance of its reaction products. In the atmos-
phere, these products are mainly methyl-vinyl-ketone and
methacrolein, two compounds that are indeed found in
chamber studies in which isoprene-emitting trees were
fumigated with ozone [119]. In plants exposed to ozone
either a reduction [113,120] or a stimulation of isoprene
and monoterpene emissions is observed. The stimulation of
the emission is more evident in response to acute and
heavy doses of ozone [121–123] (e.g. 150–300 ppb) whereas
it is often absent when plants are exposed to low doses of
ozone above background [122,124]. Ozone-enhanced emis-
sion of isoprene is due to a higher expression of the ISPS
mRNA which probably upregulates the protein and the
activity of the enzyme [123]. Interestingly, such an upre-
gulation is more evident in leaves that develop under
enriched ozone and that build up a better resistance to
pollutants, as well as in new leaves that develop above
those that have been ozonated [123]. Evidently, impair-
ment of photosynthetic activities prevents older ozonated
leaves from enhancing the secondary metabolism, leading
to volatile terpene formation.
When plants are exposed to low or moderate and chronic
doses of ozone, such an induction of the volatile terpene
pathway is absent, and the expression of ISPS mRNA and
the level of ISPS protein may even be reduced [120,124].
Clearly, the signals that activate the biochemistry of ter-
pene formation, and which are unknown at present, are not
released under these conditions. It has been hypothesized
[125] that the induction of volatile terpenes in response to
ozone follows a hormetic dose–response relationship, i.e.
that the volatile terpenes are increasingly induced at low
but growing doses of ozone until an ozone threshold is
reached after which the biosynthesis of terpenes is
repressed. The experiments, however, reveal a more com-
plex picture, with biosynthesis of volatile terpenes being
induced only when ozone dose overcomes a threshold that
marks cellular damage but at which photosynthesis is not
yet so heavily suppressed to be unable to supply enough
substrate for volatile terpenes. On the basis of these find-
ings a long-term induction of isoprene biosynthesis, and
the consequent evolutionary hypothesis that high terpene
emitters will be favoured in a future more oxidative atmos-
phere [126] may not hold true.
Ozone is a very damaging pollutant for plant cells, and
one of the first recognized ozone effects is the denaturation
of the lipids in cellular membranes [127]. It is therefore
expected that volatiles that are associated with lipid per-
oxidation are also more emitted in ozone-stressed leaves.
Accordingly, bursts of C6 compound emissions were
observed in ozone-stressed leaves and the lag time with
which these compounds were emitted was proportional to
the ozone dose absorbed by the leaves [128] and to the
ozone-induced injuries [113]. These experiments clearly
show that C6 compounds are in vivo indicators of mem-
brane denaturation and damage as already indicated also
in response to drought [114]. In addition, these studies
[113,128] also revealed transient pulses of methanol and
MeSA. While methanol emission has been mainly attrib-
uted to demethylation of cell wall pectins, and is therefore
likely to be another indicator of ozone damage, the induc-
tion of MeSA is more intriguing. MeSA emissions showed a
weak association with high levels of ozone recorded in non-
manipulative field experiments [98], but acute exposures
to ozone and UV light are apparently also able to induce
bursts of this compound (Velikova et al., personal com-
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munication). Emissions of MeSA induced by oxidative and
other environmental stresses may further contribute to
biogenic secondary organic aerosols [129,130] and may
alter the network of plant communication with other
organisms which is mediated by chemical messengers [98].
Other climate change factors: UV-B radiation
Studies of the effect of UV-B radiation (wavebands of 290–
320 nm) on BVOCs emissions are rare, despite the fact that
UV-B radiation is known (i) in moderate doses (environ-
mentally relevant) as a priming abiotic agent, triggering
the formation of UV screening pigments and modulating
plant growth; and (ii) in higher doses (e.g. as a result of the
stratospheric ‘ozone hole’ and indeed transiently present in
certain regions surrounding the South Pole) as an agent
causing severe damage to the photosynthetic machinery,
nucleic acids, and proteins [127].
The impact of UV-B radiation on terpenes seems to
indicate a stimulation of their biosynthesis and emission.
In one study with European oak [131] the higher emission
of isoprene under UV-B radiation was attributed to a
higher biomass density rather than to a higher instan-
taneous photosynthetic rate. A more recent study [132]
again showed increased isoprene emission rates of sub-
arctic peatlands when irradiated with increasing levels of
UV-B radiation, and explained the rising emission as a
consequence of oxidative damage to membranes and to the
induction of the terpene defensive antioxidant pathway
[133].
UV damage to cellular structure may also induce emis-
sion of other BVOCs. Emission of methane under aerobic
conditions originating from plant material [10] is a con-
troversial topic in recent plant and atmospheric research,
e.g. [134,135]. Plant-mediated transport of methane
originating from methanogenic soil microorganisms
through the aerenchyma and out of the leaves of wetland
plants, e.g. rice [136] has been known from many years.
However, there is growing evidence that UV radiation can
mediate non-microbial methane release from cell wall
material, in particular pectin. In the initial work [10] it
was suggested that the methoxyl groups of pectin can be
one, albeit not the only, source of aerobic methane, e.g.
[137,138]. It was recently demonstrated [137–139] that the
release of methane from structural cell wall components of
fresh and dried leaf tissue was UV-B dependent. In line
with this observation, the authors [139] also showed that
the removal of methoxyl groups interrupted methane emis-
sion from UV-irradiated pectin. Very recently it was
demonstrated [140] that the emission of methane from cell
wall material is mediated by UV-generated ROS [hydroxyl
radicals (

OH) and singlet oxygen; but not hydrogen per-
oxide or superoxide radicals].
Environmental stresses as well as cellular signalling
processes involve the formation of ROS. Therefore it might
be speculated that aerobic methane formation is a com-
mon, yet overlooked part of plant stress responses com-
plementing the transient burst of BVOCs, i.e. methanol,
acetaldehyde, and C6 alcohols and aldehydes [67,79], and
the long-lasting stimulation of terpene biosynthesis. Sup-
port for this assumption is given by recent work demon-
strating increased emissions of methane upon bacterial
infection, chemical generation of ROS [139] or physical
injury [141].
Other climate change factors: atmospheric CO
2
Rising CO
2
concentration at global level is dramatically
affecting plant life. The primary effect is the increased
availability of substrate for Rubisco, and the consequent
enhancement of photosynthesis [142]. However, CO
2
is one
more factor that uncouples terpene metabolism and emis-
sions from photosynthesis.
As early as 1964, G. Sanadze [143] demonstrated that at
low CO
2
concentration photosynthesis is reduced, but iso-
prene emission increases. In a more recent laboratory
study the highest emission of isoprene was detected at
an intercellular CO
2
concentration (C
i
) of around 150–200
ppmv, not far from the C
i
experienced in nature by leaves of
tree species [18], and then progressively decreased at
higher C
i
. Since then, many studies on different plant
species have shown an inhibition of isoprene biosynthesis
under higher than ambient CO
2
concentrations [144–148].
For example elevated CO
2
in a natural CO
2
spring reduces
ISPS activity and isoprene emission from common reed
(Phragmites australis)[37]. Compared to isoprene, less is
known about the influence of CO
2
on light-dependent
monoterpene emission. A study on holm oak (Quercus ilex)
growing under CO
2
concentration double than ambient in
open top chambers [46] showed a parallel downregulation
of mono-TPS activities and monoterpene emission. How-
ever, studies conducted in holm oak plants growing for
their entire life in natural CO
2
springs under very high but
not steady CO
2
levels did not reveal substantial inhibition
of the emitted monoterpenes [149], probably because the
treatment was also associated with recurrent drought
stress episodes that could also affect the emission (see
above).
While a downregulation of ISPS and mono-TPS is gener-
ally associated with lower emission of isoprene and mono-
terpenes grown under elevated CO
2
[145], the enzyme
properties are not necessarily the factors controlling the
emissions. This control may be exerted primarily by
reduced substrate availability (DMADP and GDP) result-
ing from a downregulation of the MEP pathway. Although
this assumption has no direct support from the literature, a
simultaneous decrease in isoprene emission and DMADP
content was observed [145]. This reduction in isoprene
(and also monoterpene) emission under elevated CO
2
might result from enforced higher consumption rates of
cytosolic PEP (phosphoenolpyruvate) through PEP
carboxylase activity, thus lowering the rates of PEP trans-
port into the chloroplast, where PEP, in its dephosphory-
lated form (pyruvate) feeds into the MEP pathway. Based
on this work [145] and earlier suggestions by G. Sanadze
[143,150] a double carboxylation hypothesis was proposed
[148,151] for C3 plants (to which all of isoprene emitters
belong) with cytosolic PEP carboxylase and plastidic RuBP
carboxylase as antithetic precursors controlling the flow of
carbon to plastidic terpene metabolism (as well as to the
shikimic acid pathway and fatty acid biosynthesis) in
response to changes in CO
2
concentration. This idea gets
support from a study [152] showing an inverse relationship
of isoprene biosynthesis and PEP carboxylase activity
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when cottonwoods (Populus deltoides) were grown on high
nitrate concentration, a condition favouring cytosolic
organic acids synthesis. In line with this scheme, mito-
chondrial respiration can constitute a growing sink for
cytosolic PEP under rising CO
2
, thus competing with the
import of this substrate in the chloroplast for terpene
biosynthesis [145]. Recent experiments with Free Air
CO
2
Enhancement (FACE) facilities, however, indicated
that the inverse relationship between isoprene and respir-
ation was not straightforward under elevated CO
2
, and
that competition occurs only when oxaloacetate production
from PEP for anabolic support of respiration is strong, such
as in young, expanding leaves [153]. A positive CO
2
effect
on isoprene [144] and monoterpene [154] emissions may be
occasionally observed. Moreover, no effect on isoprene and
monoterpenes was reported on poplar [125,153] or on Scots
pine (Pinus sylvestris)[155].
Currently we do not know whether the CO
2
impact on
light-dependent isoprene and monoterpene emission is a
general effect and which fundamental biochemical mech-
anisms are responsible. If the biosynthesis of volatile
terpenes is ubiquitously enhanced at CO
2
lower than
ambient, then stress conditions in which a lower intercel-
lular CO
2
concentration is set by increasing resistances to
CO
2
diffusion can generically lead to higher emissions.
Why is emission of volatile terpenes induced by
abiotic stress?
Whereas oxygenated BVOCs are mainly catabolic products
of the denaturation of cellular walls and membranes, iso-
prene and monoterpenes are produced through a dedicated
metabolic pathway that is stimulated by several abiotic
stresses (see above). This tightly regulated terpene biosyn-
thesis and the observation that emission of volatile ter-
penes represents a significant loss of photosynthetic
carbon, led to the proposition that these compounds play
important physiological and ecological roles in the protec-
tion of plants from environmental constraints. However,
the debate is still ongoing whether one or more ecological
actions should be attributed to volatile terpenes, and which
are the physiological mechanisms that allow terpenes to
exert their protective action. Two ‘metabolic’ hypotheses
suggest that isoprene acts as a kind of ‘safety valve’ which
allows quenching energy or metabolites (Figure 4). In
particular, one study [150] considers isoprene biosynthesis
as a pathway for dissipation of excess photosynthetic
energy, whereas a more recent one [145] postulates that
isoprene biosynthesis prevents the overflow of chloroplas-
tic DMADP. We consider as a ‘metabolic’ hypothesis also
the ‘opportunistic hypothesis’ [41] which suggests that
volatile terpenes are somehow alternative to ‘essential’
terpenes (such as carotenoids, also formed through the
MEP pathway, and for which an important antioxidant
role is clearly established). The same pool of carbon may
generate volatile and/or essential terpenes according to the
need to face different constraints. This may be true also
within the class of volatile terpenes, as it was recently
demonstrated that isoprene decreases when monoterpenes
are synthesized in poplar leaves attacked by beetles [156].
A second group of hypotheses establishes a more
distinctive functional role for volatile terpenes in plant
protection against abiotic stressors (Figure 4). The main
hypothesis is that isoprene, as well as monoterpenes, are
thermoprotective molecules, able to stabilize chloroplast
membranes during high temperature events [157] there-
fore protecting the photosynthetic apparatus. There is
ample experimental support for this idea. In brief: (i)
experiments in which plants have been fumigated with
terpenes or in which the biosynthesis of these compounds
have been chemically blocked have shown that the photo-
synthetic apparatus of isoprene-emitting plants is better
protected against heat stress [158–160] and in particular
against rapid temperature changes [161]. The interesting
idea behind the latter observation is that isoprene acts as a
rapid mechanism of protection before plants can synthes-
ize more complex molecules (including non-volatile ter-
penes) that improve thermal stabilization. (ii) An in
silico experiment has demonstrated that isoprene may
indeed partition into the phospho-lipid bilayer of mem-
branes and maintain their stability, in particular during
exposure to high temperature [162]. (iii) Transgenic plants
that have been engineered to emit isoprene or monoter-
penes, or in which isoprene biosynthesis has been
repressed are now available. Isoprene-emitting transgenic
plants are more resistant to heat stress than wild types
[53,54,163].
Volatile terpenes also appear to have a relevant anti-
oxidant action. Again several lines of evidence support this
hypothesis: (i) isoprene and monoterpenes have been
shown to reduce the damage caused by ozone [115,122]
and ROS [117,133,164]. (ii) Evidence of the reaction be-
tween isoprene and monoterpenes and ozone or other ROS
has been produced by observing the appearance of the
reaction products and the disappearance of the reagents
[120,165]. In plants exposed to oxidative stresses isoprene
has also been shown to quench nitrogen reactive species
(namely NO) that can also have an important role as
messenger molecules of the hypersensitive response to
stress [166,167]. (iii) Transgenic tobacco (Nicotiana taba-
cum) plants that have been engineered to emit isoprene are
more resistant to ozone toxicity than non-emitting wild
types [168], and the ozone sensitivity of poplar clones is
inversely related to their capacity to emit isoprene [169].
However, both functions of isoprene have been chal-
lenged by studies in which the authors were not able to
reproduce improved resistance to the stresses, especially
when using artificial systems or transgenic plants. For
instance, photosynthesis analysis showed that transgenic
Arabidopsis plants do not benefit from isoprene when a
transient heat stress occurs [53]. In transgenic, isoprene-
emitting tobacco plants, tolerance of photosynthesis
against transient high-temperature episodes could only
be observed in lines emitting high levels of isoprene. More-
over, this effect was very mild and could only be identified
over repetitive stress events [168]. Finally, grey poplar
(Populus canescens) plants in which isoprene emission
was efficiently repressed were not more sensible to oxi-
dative stresses [113]. There may be good reasons that
explain why the protection offered by volatile terpenes is
not observed in specific cases: (i) the protection offered by
these molecules may not be achieved when photosynthesis
is already heavily impaired by prolonged or acute stresses,
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or when the stresses are too mild to affect photosynthesis.
Probably a window of stress exists in which these mol-
ecules substantially protect the photosynthetic apparatus.
(ii) In some transgenic plants, especially Arabidopsis
[53,54], the achieved emission of isoprene may be too
low to induce any significant physiological effect. (iii)
Downregulation or repression of the emission of isoprene
in natural emitters may cause a large induction of other
antioxidant molecules (e.g. ascorbate and tocopherol
[113]). This is actually another strong indication that
compensatory mechanisms are operated to replace the
antioxidant action of volatile terpenes.
The observation that volatile terpene emission is resist-
ant and is often induced by stress conditions, including
stress other than heat and strong oxidants (e.g. drought
[100] and salt [102]), has led to the hypothesis that a
unique mechanism, mostly related to the antioxidant
capacity of volatile terpenes, exists [12]. As for higher
terpenes which are known for their antioxidant function
(i.e. tocopherols, carotenoids, and sesquiterpenes), the
antioxidant action of volatile terpenes may be due to the
presence of conjugated double bounds [12]. Indeed, it might
be that the role of isoprene and monoterpenes in thermal
protection also comes from their antioxidant properties.
Hydrogen peroxide may also be produced by enhanced
photorespiration under moderately high temperatures.
The generation of ROS under heat stress has been reported
often [170,171]; however, there are many heat-tolerance
mechanisms in plants [172]. Probably, ROS scavenging
would not be sufficient to protect leaves from heavy heat
stress which directly affects thylakoid structure and the
functions associated with thylakoid intactness, namely
photochemical reactions. Thylakoid functionality would
be explained better by a mechanism counteracting thyla-
koid leakiness and the consequent increase of cyclic elec-
tron flow around photosystem I. Xanthophylls, a group of
non-volatile terpenes also originating from the MEP path-
way, may indeed render the thylakoid membranes more
resistant to heat [173], and this function may also be
carried out by volatile terpenes. The localization of ISPS
in the stromal side of thylakoidal membranes [35,174] and
the hydrophobic nature of isoprene are expected to assist
with its partition into photosynthetic membranes [162].
Lipophilic isoprene partitioned into membranes can also
prevent the formation of water channels responsible for the
membrane leakiness at high temperature [158,175]. Iso-
prene could also enhance hydrophobic interactions within
thylakoids and thereby stabilize interactions between
lipids and/or membrane proteins during episodes of
heat-shock or high temperature stress conditions [176].
Figure 4. Schematic overview of the proposed physiological functions of volatile terpenes: (a) In the ‘Metabolic overflow’ hypothesis cytosolic PEPC activity plays a central
role dividing the PEP pool into fractions (red line indicates the negative impact of PEPC activity on isoprene emission) available for isoprene biosynthesis and mitochondrial
metabolism or carbon metabolism (e.g. amino acid biosynthesis) (cellular scheme adapted from [152]) explaining the downregulation of isoprene emission under enhanced
CO
2
[145].(b) The thermoprotective function of isoprene is evident when comparing the net CO
2
assimilation in wild type and non-isoprene emitting poplars [163] when
short periods of heat were applied. (c) The property of isoprene to quench NO accumulation and ozone injury is demonstrated with transgenic tobacco leaves modified in
isoprene emission potential [168].(d) Interactions of isoprene with biomembranes are indicated by an in silico model study postulating a stabilizing effect of isoprene under
high temperature [162]. (Microscopic images of NO staining are provided by V. Velikova; photos from ozone-stressed tobacco leaves are provided by V. Velikova and C.
Vickers).
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Preliminary research using circular dichroism spec-
troscopy, a valuable tool for probing the molecular archi-
tecture of the complexes and supercomplexes and their
macro-organization in the membrane system [177]
confirms that a higher thermal stability of thylakoid mem-
branes is induced in transgenic plants that are able to emit
isoprene (Fortunati et al., personal communication).
Conclusions and future directions
We have seen that abiotic stresses may induce the emission
of multiple BVOCs. Many of the emitted compounds are
synthesized from the degradation of cellular structures
and may be used as reliable indicators of cell wall degra-
dation (methanol and methane) or membrane denatura-
tion (C6 volatiles). In the case of volatile terpenes the
induced emissions reflect the elicitation of the MEP path-
way, revealing important function(s) of these compounds in
the protection against stresses. The physiological and
ecological functions of volatile terpenes are well estab-
lished; however, more studies are needed to reveal the
molecular and biochemical mechanisms that oversee the
protective role of volatile terpenes. Induction or alteration
of these BVOCs emissions by abiotic stresses and other
climate change factors may also contribute to modify the
communication of plants with other organisms, namely
herbivores and carnivores that use BVOCs emissions as
olfactory cues to retrieve hosts suitable both as food and
shelter. Technical advances have made it possible to detect
induced emissions of MeSA not only in response to biotic
stresses but also in plants subjected to abiotic stresses.
This volatile is therefore emerging as a central molecule for
the signalling of stresses and for the consequent activation
of systemic acquired resistance and hypersensitive
responses.
Acknowledgments
We thank I. Zimmer for critical reading of the manuscript and C. Vickers
and V. Velikova for providing us with tobacco images. The work was
supported by the ESF Project Volatile Organic Compounds in the
Biosphere-Atmosphere System (VOCBAS). The German Research
Foundation (DFG; SCHN653/4 to J.-P.S.) supported the research within
the German joint research group ‘Poplar –a model to address tree-specific
questions’.
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