Терпени

Available online at www.sciencedirect.com
Protective perfumes: the role of vegetative volatiles in plant
defense against herbivores
Sybille B Unsicker, Grit Kunert and Jonathan Gershenzon
Herbivore damage to leaves and other vegetative tissues often
stimulates the emission of volatile compounds, suggesting that
these substances have a role in plant defense. In fact, ample
evidence has accumulated in the last few years indicating that
volatiles from vegetative plant parts can directly repel
herbivores, such as ovipositing butterflies and host-seeking
aphids. Volatiles have also been demonstrated to protect
plants by attracting herbivore enemies, such as parasitic
wasps, predatory arthropods and possibly even insectivorous
birds. Even below ground herbivory results in the release of
volatiles that attract herbivore enemies. However, plant
volatiles are also known to attract enemies of plants. Hence, to
determine the true value of these substances in defense, more
research is needed especially in natural communities with non-
agricultural species.
Addresses
Department of Biochemistry, Max Planck Institute for Chemical Ecology,
Hans-Kno¨ll-Strasse 8, D-07745 Jena, Germany
Corresponding author: Gershenzon, Jonathan (gershenzon@ice.mpg.de)
Current Opinion in Plant Biology2009,12:479–485
This review comes from a themed issue on
Biotic Interactions
Edited by Xinnian Dong and Regine Kahmann
Available online 19th May 2009
1369-5266/$ – see front matter
#2009 Elsevier Ltd. All rights reserved.
DOI10.1016/j.pbi.2009.04.001
Introduction
Among the huge variety of chemical compounds pro-
duced by plants, some are released into the surrounding
atmosphere. In addition to carbon dioxide, oxygen, water
vapor and the gaseous hormone ethylene, plants have
been shown to emit a variety of other organic compounds.
Volatiles are released not only from floral organs but also
from vegetative parts, especially after herbivore damage.
The two most common constituents of these volatile
blends are terpenes (C
10monoterpenes and C15sesqui-
terpenes) and green leaf volatiles (C
6aldehydes, alcohols
and esters derived from lipoxygenase cleavage of fatty
acids that embody the typical odor of damaged leaves).
The close association of volatile release with herbivory
has long suggested that these substances act in plant
defense, and some fascinating lines of research provide
support for this notion. Here we review recent findings on
the role of vegetative volatiles in anti-herbivore defense.
We summarize studies on both the direct action of vola-
tiles against invertebrate herbivores and the role of vola-
tiles in attracting herbivore enemies, discuss why volatile
emission might not always be advantageous to plants and
suggest what further work is necessary to demonstrate the
defensive function of vegetative volatiles in nature.
Vegetative volatiles play other intriguing roles in plants
that are not covered here, including defense against
pathogens, protection against heat and oxidative stress
[1], signaling among plant organs [2], inter-plant com-
munication [3] and allelopathy (Figure 1). In addition,
volatile emission from herbivore-damaged plants or plant
parts may not immediately trigger defense responses, but
instead prepare the metabolic machinery for subsequent
defense production upon further herbivore attack, a
phenomenon known as priming [4]. These functions
and other aspects of plant volatiles were also treated
recently in an excellent general review [5].
Vegetative volatiles deter herbivory
Evidence that vegetative volatile compounds function to
directly repel herbivores has begun to accumulate in the
last decade [6,7]. For example, the monoterpene volatiles
ofChrysanthemum morifoliumwere recently reported to
repel ovipositing females of the diamondback moth (Plu-
tella xylostella). This lepidopteran does not normally lay
eggs onC. morifolium, and the repellence of the mono-
terpene volatiles may help explain why [8]. However,
diamondback moth females that had prior experience
with these volatiles were not necessarily repelled. Vola-
tiles may not only chase away adult lepidopterans but also
deter caterpillars from feeding. The common C
5volatile,
isoprene (Figure 2), previously implicated in plant pro-
tection against temperature and oxidative stress [1], was
shown surprisingly to deter tobacco hornworm (Manduca
sexta) caterpillars from feeding on isoprene-releasing
transgenic tobacco lines and on isoprene-emitting artifi-
cial diet [9

].
Vegetative volatiles have also been shown to repel other
insect groups, such as aphids [10–12]. In one instance, this
appears to result from outright deception. The sesqui-
terpene, (E)-b-farnesene (Figure 2) is a common aphid
alarm pheromone that is released by attacked aphids and
causes other aphids in the vicinity to stop feeding and
move away. The same compound is also present in some
www.sciencedirect.com Current Opinion in Plant Biology2009,12:479–485

plant volatile mixtures. Volatiles fromArabidopsis thaliana
engineered to emit (E)-b-farnesene repelled the green
peach aphid (Myzus persicae) in comparison to volatiles
from non-emitting control lines [13]. However, volatile
blends containing mixtures of (E)-b-farnesene and other
sesquiterpenes are not necessarily repellent [14], so the
ability of this sesquiterpene to function as a natural aphid
repellent requires further investigation. In addition to
aphids, another piercing-sucking insect, the western
flower thrips (Frankliniella occidentalis), was repelled from
oviposition by volatile nicotine (Figure 2)[15

].
In the marine environment, volatile plant defenses have
also been recently documented. The brown alga,Dictyota
dichotoma, releases trimethylamine and dimethylsulfide
(Figure 2) after wounding, which in combination with a
non-volatile compound, acrylate, inhibited feeding by a
marine amphipod [16

]. Dimethylsulfide and acrylate are
derived upon wounding from dimethylsulfoniopropio-
nate, a compound found in a variety of algal species
[17]. Interestingly, other sulfur volatiles, dimethyldisul-
fide and dimethyltrisulfide, were emitted from the roots
ofBrassica nigraupon feeding by the cabbage root fly
(Delia radicum)[18

]. These substances were previously
described as insect neurotoxins [19] and so could also act
in direct defense.
To date, little information is available on how plant
volatiles might actually cause herbivore repulsion or
inhibit feeding. One may speculate that volatiles could
function as good markers of a species identity and so repel
herbivores from non-hosts. Additionally, herbivore-
induced volatiles may serve as reliable signals to other
herbivores regarding the presence of competitors or the
danger of herbivore enemies. These compounds could
also indicate that a prospective host has increased its
defenses due to prior herbivore attack. Furthermore,
volatiles could have direct toxic action on herbivores,
480Biotic Interactions
Figure 1
Volatiles play many diverse roles in the lives of plants. This review focuses on their role in anti-herbivore defense.
Current Opinion in Plant Biology2009,12:479–485 www.sciencedirect.com

but this possibility needs to be tested under biologically
realistic conditions with appropriate concentrations of
chemical compounds, which are mostly emitted at rates
of nanograms or micrograms per hour per gram of leaf
tissue.
Vegetative volatiles attract herbivore enemies
Since the earliest studies on herbivore-induced volatiles
by Dicke, Turlings and others [20,21], researchers have
been captivated by the idea that volatiles could attract
arthropod predators and parasitoids of herbivores and thus
reduce plant damage [22]. This phenomenon, which is
known as indirect defense, has been extended recently to
vertebrate predators of herbivores. WhenBetula pubescens
trees were heavily infested with caterpillars of the autum-
nal moth (Epirrita autumnata), artificial caterpillars
attached to branches were more frequently attacked by
passerine birds than artificial caterpillars on trees without
autumnal moth infestation. The amount of bird attacks
was directly correlated to the emission of several ter-
penes, including (E)-b-ocimene (Figure 2), linalool and
DMNT, indicating that these volatiles could attract birds
to herbivore-infested trees [23

].
The vast majority of studies investigating the role of
volatiles in attracting herbivore enemies have been per-
formed with a very restricted group of plant species of
agronomic importance (e.g. [24–28]). These species
belong principally to four plant families, the Poaceae
(maize, wheat), the Fabaceae (lima bean, cowpea, soy-
bean), the Brassicaceae (cabbage, black mustard) and the
Solanaceae (tomato, potato). In contrast, the number of
contributions where non-crop-species have been investi-
gated for volatile-based indirect defense is comparatively
small (e.g. [29,30]). A study by Kessler and Baldwin [7]on
the wild tobacco species,Nicotiana attenuata, in the desert
of the southwestern United States was the first to demon-
strate that herbivore-induced volatiles attract herbivore
enemies in a natural community. More recently, some
remarkable field studies by Heil and Kost on wild lima
bean growing in Mexico showed that plant volatiles
primed plants to increase their production of extrafloral
nectar, which functions as a reward for carnivorous arthro-
pods, such as ants, that attack herbivores [31,32].
Volatile attraction of herbivore enemies is not restricted
to the aerial parts of plants. Rasmannet al.[33] discovered
that insect-induced (E)-b-caryophyllene (Figure 2) emis-
sion from maize roots attracts nematodes that prey on the
attacking insect larvae. Subsequent studies have inves-
tigated the combined effects of above and below ground
herbivory, and demonstrated that herbivory in both
locations reduces volatile emissions and predator and
parasitoid attraction in maize and other species
[18

,34,35

]. For example, the parasitic waspCotesia
glomeratawas attracted preferentially to caterpillars of
the large cabbage white butterfly (Pieris brassicae) feeding
on black mustard with undamaged roots as compared to
cabbage white caterpillars feeding on plants whose roots
were simultaneously infested by the cabbage root fly
[18

].
The extension of studies on plant volatiles, herbivores
and herbivore enemies to include multiple herbivores is a
welcome development since this may more closely reflect
natural conditions. Plants face a diversity of biotic and
abiotic stresses in their natural environments that could
Protective perfumesUnsicker, Kunert and Gershenzon 481
Figure 2
Chemical structures of selected vegetative volatiles that function in
repelling herbivores and attracting herbivore enemies. Although most
vegetative volatiles identified to date are either terpenes or green leaf
volatiles, some of the latest studies report the involvement of alkaloids,
sulfur compounds or amines in repelling herbivores.
www.sciencedirect.com Current Opinion in Plant Biology2009,12:479–485

modify volatile emission and indirect defense [36]. Con-
cerning abiotic stresses, the increasing attention to global
climate change has prompted some researchers to inves-
tigate whether increases in ambient levels of CO
2or
ozone in the atmosphere have any influence on the
attraction of herbivore enemies. Some herbivore-induced
volatile compounds are highly reactive with ozone, and
elevated ozone concentrations were found to degrade
most of the terpenes and green leaf volatiles emitted
from bothBrassica oleraceaandPhaseolus lunatusafter
herbivore damage [37,38]. Nevertheless, herbivore ene-
mies still oriented towards damaged plants after ozone
treatment suggesting that ozone-stable volatile com-
pounds, such as methyl salicylate and benzyl cyanide,
might serve as sufficient signals for the enemies investi-
gated in this study, the predatory mitePhytoseiulus persi-
milisand the parasitic waspCotesia plutella[37].
A hallmark of herbivore-induced v