Biochemical Systematics and Ecology 29 (2001) 1103–1113
Chemical information transfer between wounded
and unwounded plants: backing up the future
Jan Bruina,*, Marcel Dickeb
a
Section Population Biology, University of Amsterdam, Institute of Biodiversity and Ecosystem Dynamics,
PO Box 94084, 1090 GB Amsterdam, Netherlands
b
Wageningen University, Laboratory of Entomology, PO Box 8031, 6700 EH Wageningen, Netherlands
Received 9 April 2001; accepted 19 April 2001
Abstract
This special issue on ‘‘Chemical information transfer between wounded and unwounded
plants’’ provides an overview of past and ongoing experiments on plant-to-plant communication. Since the studies on plant responses to single gaseous compounds were not
particularly emphasised, the actual number of studies relevant to the subject is underestimated. All in all, we think the amount of data on damage-induced plant-to-plant
information transfer makes that the phenomenon can no longer be denied and deserves
intensified attention by the scientific community. In this epilogue we highlight a couple of
issues which received little attention and present some speculative ideas. First we concentrate
on functional aspects of plant-plant communication we stress the concept of damage-induced
signalling as an ecological cost to the signal-sending plant and we discuss the theoretical
development on interplant signalling, which is still in its infancy. With respect to mechanisms,
we compare above- to belowground signalling, discuss potential cues and stress the possibility
that responses in signal-exposed plants may be hidden. Finally, we address some future
prospects which may help in the further development of the still underexposed phenomenon of
damage-induced plant-to-plant information transfer. r 2001 Elsevier Science Ltd. All rights
reserved.
1. Introduction
Like the study of life on Mars, the study of plant–plant communication is an easy
subject to attract public attention with. In recent years the study of information
transfer between wounded and neighbouring unwounded plants is receiving
*Corresponding author. Tel.: +31-20-525-7623; fax: +31-20-525-7754.
E-mail address: [email protected] (J. Bruin).
0305-1978/01/$ - see front matter r 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 3 0 5 - 1 9 7 8 ( 0 1 ) 0 0 0 5 3 - 9
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J. Bruin, M. Dicke / Biochemical Systematics and Ecology 29 (2001) 1103–1113
increasing attention from the scientific community as well. In the introduction to this
issue we listed the published studies showing positive evidence for plant–plant
information transfer (Dicke and Bruin, 2001). Taking into account that only those
studies were listed that were published prior to this special issue and that used plant
material as signal-sender, the amount of work relevant to the subject is actually
much bigger. Think e.g. of all the studies in which defensive responses were studied
in plants exposed to single compounds (e.g. Avdiushko et al., 1997; Baldwin, 1998;
Bate and Rothstein, 1998; Zeringue, 2001; Birkett et al., 2000), or the studies which
reported negative evidence (e.g., Fowler and Lawton, 1985; Preston et al., 1999).
Although most publications report on laboratory experiments, the recent studies by
Karban and colleagues (Karban et al., 2000; Karban, 2001; Preston et al., 2001) and
by the group of Tscharntke (Dolch and Tscharntke, 2000; Tscharntke et al., 2001)
present intriguing field evidence. All in all, there is an undeniable pile of experimental
data, which may be explained by damage-induced plant-to-plant information
transfer. In this paper we highlight some issues which received little attention so far
and present some speculative ideas.
2. Evolutionary ecology of plant signalling
2.1. Ecological costs of damage-related signalling
Many ecologists take volatile production by (damaged) plants for granted and start
to ask interesting questions from thereon. It may be helpful, however, to ask why
plants produce volatiles in the first place, in other words to question the function of
volatile production. One important advantage of voltatile production may be the
attraction of natural enemies of the plant’s antagonists (e.g. Price et al., 1980; Dicke
and Sabelis, 1989). A plant individual that manages to increase the effectiveness of
these natural enemies through the production of volatile compounds that inform them
on the presence of their prey/host will suffer relatively little damage, and thus is likely
to gain an advantage through natural selection (e.g. Sabelis et al., 1999; Van Loon
et al., 2000). The magnitude of this advantage depends on the costs involved. These
costs are not only physiological (metabolic), but also ecologicalFa volatile-producing
plant may e.g. attract extra herbivores or ineffective, but competitively superior,
predators (e.g. Dicke and Sabelis, 1989). A third possible ecological cost would be the
tapping of the information by downwind neighbouring plants (Bruin et al., 1995;
Shonle and Bergelson, 1995; Dicke and Vet, 1999; Sabelis et al., 1999; Dicke and Van
Loon, 2000). Since neighbouring plants are likely to compete for limiting resources
(e.g. Stoll and Weiner, 1999), it is probably safest to view damage-related interplant
information transfer as ‘unintended’ by the signal-sender: eavesdropping neighbours
are likely to reduce the sender’s fitness, thus conferring an ecological cost.
2.2. Theoretical development
Defensive action by the signal-receiving plants could also be advantageous to the
damaged signal-sending plant. If signal-sending and receiving plants are sufficiently
J. Bruin, M. Dicke / Biochemical Systematics and Ecology 29 (2001) 1103–1113
1105
close kin, informing the receiving plants may benefit the sender as it increases its
inclusive fitness (cf. Grafen, 1984). But relatedness between sender and receiver plants
is not a prerequisite for advantageFwhenever the combined effort of all plants would
result in a higher number of natural enemies locally and, consequently, in less
herbivore damage, natural selection is expected to favour such plant behaviour. In
situations like these, benefits to the information senders are highly dependent on
the actions of the information receivers. In other words: these systems are vulnerable
to the invasion of ‘cheaters’, i.e. plants that take advantage from the freely
available information around but do not add to a communal defensive activity.
This can be concluded from theoretical studies on polymorphic plant populations
in which plant individuals have fixed defence strategies, and plants may benefit
from their neighbours via, for example, the attraction of natural enemies of
shared herbivores, or via competition for shared resources (Sabelis and De Jong,
1988; Augner et al., 1991; Augner, 1994). Cheating plants save energy and are
likely to be stronger competitors after the herbivores are gone (cf. Van Dam and
Baldwin, 1998).
Verbal tracking of the consequences of the various roles plants may play soon
becomes impossible, as these games between damaged and undamaged plants
become very complicated. Mathematical models are then required to predict possible
outcomes and to yield (quantitative) hypotheses, which can subsequently be tested
experimentally. Recently, Nowak and co-workers have started to develop an
evolutionary approach to the study of communication and the progress of language
(a.o. Nowak and Krakauer, 1999). Although their (ESS-) models aim to understand
the evolution of language among humans, there is no a priori reason why the results
would not also (at least partly) apply to plants. Thus far, Nowak and colleagues have
assumed shared interests for signal-sender and signal-receiver. Van Baalen and
Jansen (unpublished manuscript) release this assumption and explore the evolution
of communication strategies when the interests of sender and receiver are not
overlapping. In (ESS-) models with an explicit spatial structure (‘‘contact
networks’’), Krakauer and Pagel (1995) already concluded that communication
systems may be vulnerable to the invasion of cheaters. Van Baalen and Jansen
extend this model by allowing multiple signals to evolve. Their analysis indicates that
at certain levels of the ‘temptation to cheat’ the communication system no longer
functions, and then it pays to develop ‘coded information’ (dialects). Initially the
individuals who understand these codes are rare and safe. But the more they spread,
the higher the risk of cracking the code by cheaters, which subsequently start to
spread. Thus, information is expected to become more and more idiosyncratic. Thus
far, Van Baalen and Jansen have assumed that (physiological) costs involved in
signalling are negligible. However, this assumption may be difficult to hold, since
cheap information may easily lead to loss of meaning, as shown by Godfray (1995) in
a model study on signalling between plants and the natural enemies of herbivores.
Thus far, the models of Van Baalen and Jansen are on the evolution of
communication between undefined organisms. They intend, however, to explore
the evolution of communication between plants, herbivores and natural enemies of
herbivores in tritrophic systems, and subsequently to incorporate plant-to-plant
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J. Bruin, M. Dicke / Biochemical Systematics and Ecology 29 (2001) 1103–1113
communication (M. van Baalen, personal communication). Their first results may
already provide an argument for the evolution of specificity (i.e. idiosyncratic
information) in plant–plant information transfer.
3. Mechanisms of plant–plant information transfer
3.1. Aboveground versus belowground
Two of the studies in this issue presented evidence for belowground transfer of
information between damaged and undamaged plants. Chamberlain et al. (2001)
showed that undamaged broad bean (Vicia fabae) plants became attractive to
parasitoids (Aphidius ervi), after the plants had been in soil together with pea aphid
(Acyrthosiphon pisum)-infested broad bean plants for five days. A similar response in
the parasitoids was found when undamaged broad bean plants stood in a
hydroponic solution where pea aphid-infested plants had been standing for 3 days.
In an analogous study, Dicke and Dijkman (2001) showed that uninfested lima bean
(Phaseolus lunatus) plants became attractive to predatory mites (Phytoseiulus
persimilis), after the plants had been incubated in water in which spider mite
(Tetranychus urticae)-infested lima bean plants had been standing before. In both
studies it was ensured that volatiles could not have caused the effect. Hence, these
studies suggest that the infested plants give off a water-soluble soil-borne cue that
may influence nearby uninfested plants.
Findings like these stimulate to consider the differences between aboveground and
belowground information transfer. One obvious factor that comes to mind is the
absence of wind in the soil. Airborne signals travel in a linear fashion, they go
wherever the wind blows them, but soilborne signals probably travel radially via
diffusion. This implies that soilborne information may also reach upwind plants. By
giving off both airborne and soilborne information, a damaged plant may thus
enlarge the group of neighbouring plants that will be reached. If the group of signalexposed plants somehow adds to, for example, the luring of natural enemies of
herbivores, then the size of the group may be related to the number of natural
enemies attracted, and thus to the benefit of the damaged plant. In other words, it
may pay a damaged plant to reach more neighbours.
On the other hand, by giving off soilborne signals only, a damaged plant may
rather limit the number of plants that are being exposed to their information. If the
number of protagonists attracted is related to the group size of signalling plants, then
the production of only soilborne cues can be seen as a cost. At the same time,
however, it could be a way to minimise the risk of eavesdropping by other plants. If,
for example, kinship among plants would decline with increasing distance to a focal
plantFand this seems to be the case for many plants, since ‘‘plants exchange pollen
over very limited distances, even in wind-pollinated species [...], and most seeds fall in
the immediate vicinity of their maternal parents’’ (Crawley, 1997)Fthen the
production of only soilborne signals could even be a mechanism via which plants
could evolve ‘neighbourhood support’. The different consequences of soilborne and
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1107
airborne signals for the emitting plant raise the question to what extent plants can
control the nature of damage-related information.
The evidence presented by Chamberlain et al. and by Dicke and Dijkman relates
to water-soluble signals, which are probably exuded in the soil. However,
belowground plants may be interconnected by means of direct root–root contacts
or via fungal (ectomycorrhizal) bridges. There is increasing evidence that compounds
are being transferred between plant individuals via such underground networks (e.g.
Wu et al., 2001). There is no evidence that damage-related information is being
transferred in this way, but the possibility is intriguing. Also the transport of
information via such networks could allow a damaged plant to reduce the risk of
being tapped by its competitors (as opposed to aboveground, where picking up
volatile signals seems hard to avoid...).
3.2. Damage-related cues
Preston et al. (2001) mention several criteria for successful signals, referring to a
note by Firn and Jones (1995). They state that a volatile can only function as a
damage-related plant–plant airborne cue if it is (1) received at physiologically active
levels, and (2) given off at significantly larger quantity if also produced by
undamaged plants, or in modified mixtures. To investigate the first criterion, dose–
response studies should be performed. The second criterion refers to the so-called
‘signal-to-noise problem’Fa signal has to contrast its surroundings in order to be
notable. Subsequently, Preston and colleagues build a strong case for their
hypothesis that (cis)-methyl jasmonate potentially is a meaningful signal in the
interaction between sagebrush and wild tobacco. We fully agree that these criteria
make sense. However, we would like to add one straightforward possibility for
getting around the signal-to-noise-problem (see also Firn et al., at http://wwwusers.york.ac.uk/Bdrfl/tt.htm). It is known that the production of plant volatiles
follows diurnal rhythms (Loughrin et al., 1994; Turlings et al., 1995; De Moraes
et al., 2001). Such patterns are highly predictable, not just for investigators, also for
neighbouring plants. Meaningful damage-related information could thus simply be
created by changing the timing of production of a single compoundFthe compound
itself does not have to be different, nor its level; by shifting its production relative to
other compounds its surrounding noise changes, hence the signal-to-noise ratio. (At
daytime, city traffic is full of cars honking and few pay attention, at night however
honking is alarming.) We are not aware of evidence for such shifts in timing, and for
a meaningful assessment of its feasibility more knowledge of the mechanisms
underlying the rhythmicity of volatile production is needed.
To date, almost all attention has been given to volatiles as damage-related
cues between plants (apart from the root-released cues mentioned by Dicke and
Dijkman (2001) and Chamberlain et al. (2001)). However, it would be interesting
to investigate the role of other information carriers. For instance, several studies
have shown that visual cues may play a role in plant–plant resource competition
(review in Ballar!e, 1999). Since often infestation with herbivores or pathogens
is associated with colour changes, light may also mediate the induction of
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defensive responses in undamaged plants. Needless to say, there is not a shred of
evidence.
3.3. Assaying changes in signal-receiving plants and silent responses
When studying the influence of damage-related plant information on undamaged
plants, the information-receiving plants can be assayed in various ways. Bioassays
will provide information on effects of possible changes in the plant on organismsF
either antagonistic (herbivores, pathogens) or protagonistic (natural enemies of the
herbivores). This type of assays can be said to provide ‘ultimate’ information on
effects. Usually very little is learned on mechanisms, but one does obtain an
impression of the biological meaning of effects. If no effect is found in a bioassay, this
may mean that (1) there is no change in the signal-receiving plant, or (2) there is a
change, but it does not affect the organism under investigation. The latter, of course,
may imply that an effect could have been found if another organism had been tested.
For this reason, the finding of no effect in a bioassay is not very informative.
To know for sure whether there is a change in the signal-receiving plant, more
sensitive assays have to be done, such as chemical or molecular-biological assays.
The disadvantage of the latter types of assay is that they may be too sensitive, and
will always indicate differences. To differentiate between relevant and irrelevant
changes, bioassays are indispensable. Hence, the combination of bioassays and
chemical or molecular-biological assays is most rewarding.
Any type of assay aiming at external signs of a plant response to volatile
exposureFsuch as behavioural assays with predators or parasitoids, or chemical
headspace analysesFmay result in recording no effect. Still, it remains possible that
the plants’ response is ‘silent’ (see also Bruin and Sabelis, 2001). For example, in
response to damage-related volatiles, undamaged plants could somehow become
alertedFthe exposure to the volatiles informs them on potential danger nearby. Since
there is always the possibility that the plants will not actually become damaged, it
could pay to postpone expensive defensive measures until they are actually needed.
This state of alertness, involving preparations for an immediate response when
damaged, could be less costly than the induction of direct or indirect defences. This
concept of alertness is reminiscent of the (immunological) ‘memory’ in inducible
defences, both in animals (e.g. Harvell, 1990) and plants (Karban and Niiho, 1995;
Baldwin and Schmelz, 1996). Hidden or silent responses by exposed plants may easily
go unnoticed when only the outside of a plant is assayed. This is yet another
argument for assaying behaviour, chemistry and molecular biology in combination.
It is of course tempting to perform small-scale laboratory experiments with (very
young) plantsFor parts of themFin small glass enclosures, in which the effect of
exposure to a volatile compound is measured. Such experiments quickly yield results
and they are easily replicated. It should be kept in mind, however, that the relevance
of their results for phenomena in whole plants or in the field may be limited. There
are several reasons for this. (1) The amount of carbon dioxide may rapidly be
depleted and plants are forced to photosynthesise below their CO2 compensation
point, which may induce stress responses (Nilsen and Orcutt, 1996; Zobayed et al.,
J. Bruin, M. Dicke / Biochemical Systematics and Ecology 29 (2001) 1103–1113
1109
1999). Although control plants will experience a similar shortage of CO2, a possible
interaction effect of stress and the factor under study is usually not controlled for. (2)
Plant parts may display responses, which are quite different from those of intact
plants (e.g. Risch, 1985; Stamp and Bowers, 1994). (3) Similarly, responses by
seedlings may differ considerably from responses by older plants.
The results from this type of experiments should be treated as stepping stones,
rather than end resultsFthey should be repeated in laboratory set-ups with intact
plants, in much bigger air volumes and/or wind rather than still air, and finally they
should be repeated in the field. Increasing the experimental complexity in this way
may make it more difficult to obtain clear and repeatable results, but the
simultaneous increase in ecological relevance of the results is ultimately rewarding.
4. Future prospects
4.1. Pairing ecology and molecular biology
Much may be expected from the (further) integration of ecological and molecular
approaches (as also pointed out by Hunter (2000a, b) and Paul et al. (2000). This
integration will provide answers, based on sensitive assays of tiny tissue
sections, to questions of population biologists or community ecologists on
(groups of) whole organisms. One of the major advantages of this integration will
be to sample high numbers of plant individuals during large-scale field
experimentsFsince high numbers of samples are generally manageable in molecular
biology, levels of variability in the field can be assessed. Also, since often tiny
tissue samples suffice, repetitive sampling of the same plant individuals may be
feasible.
The application of molecular tools to studies on plant–herbivore interactions
will help to elucidate signalling pathways in defense reponses in plants (e.g.
Halitschke et al., 2001; Hermsmeier et al., 2001; Schittko et al., 2001). Also the use of
signal-mutants and/or genetically modified plants will be instrumental in this respect.
The pairing of this approach to bioassays with intact plants and herbivores, may
help in the selection of relevant plant variables, which subsequently can be assayed in
larger-scale experiments. Much of the most recent work is being done on the
interaction between plants and herbivores and pathogens. But a similar approach
will also provide insight in the study of plant–plant interactions (e.g. Arimura et al.,
2000a, b).
4.2. Mechanisms of information perception by plants
There is extensive information on signal-transduction in induced plant responses
(e.g., Karban and Baldwin, 1997; Chadwick and Goode, 1999; Agrawal et al., 1999;
Pieterse and Van Loon, 1999). This relates to internal plant processes in response to
herbivore or pathogen damage. Whether these signal-transduction processes also
mediate plant responses to chemical information from damaged neighbours, may be
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elucidated by physiological, biochemical and molecular analyses. However, so
far virtually nothing is known on the perception of chemical cues related to attackers
before the attack occurs. Yet, there is ample knowledge on the perception by
plants of environmental cues such as light (Ballar!e, 1999). How do plants perceive
chemical information from damaged neighbours? Is this perception dependent
on open stomataFalthough many small volatile organic compounds may
diffuse straight through the apolar waxy surface, into a receiving plantFand are
the receptors present on cell surfaces in intercellular space? Knowledge on
the receptors with which plants perceive chemical information from damaged
neighbours will provide an important step forward (compare e.g. to the identification
of a systemin-receptor in the plasmamembranes and surface of suspension
cultured cells (Ryan, 2000)). It will not only ultimately solve the question ‘do plants
perceive chemical information from damaged neighbours’ but more interestingly,
it will allow a direct analysis of information perception by plants, analogous to
studies on information perception by animals. This mechanistic knowledge will
be important for functional studies that aim to understand the strategies of
plants that are based on chemical information from their damaged neighbours (cf.
Dukas, 1998).
Acknowledgements
We thank Minus van Baalen and Maurice Sabelis for constructive comments on
(parts of) the manuscript.
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