Journal of Experimental Botany, Vol. 66, No. 2 pp.

455–465, 2015
doi:10.1093/jxb/eru391 Advance Access publication 30 September, 2014

Review Paper

Interplay between insects and plants: dynamic and complex

interactions that have coevolved over millions of years but
act in milliseconds
Toby J. A. Bruce*
Rothamsted Research, Harpenden, Herts AL5 2JQ, UK

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* To whom correspondence should be addressed. E-mail: tobyjabruce@gmail.com

Received 19 May 2014; Revised 26 August 2014; Accepted 28 August 2014

Abstract
In an environment with changing availability and quality of host plants, phytophagous insects are under selection pres-
sure to find quality hosts. They need to maximize their fitness by locating suitable plants and avoiding unsuitable ones.
Thus, they have evolved a finely tuned sensory system, for detection of host cues, and a nervous system, capable of
integrating inputs from sensory neurons with a high level of spatio-temporal resolution. Insect responses to cues are
not fixed but depend on the context in which they are perceived, the physiological state of the insect, and prior learning
experiences. However, there are examples of insects making ‘mistakes’ and being attracted to poor quality hosts. While
insects have evolved ways of finding hosts, plants have been under selection pressure to do precisely the opposite and
evade detection or defend themselves when attacked. Once on the plant, insect-associated molecules may trigger or
suppress defence depending on whether the plant or the insect is ahead in evolutionary terms. Plant volatile emission
is influenced by defence responses induced by insect feeding or oviposition which can attract natural enemies but
repel herbivores. Conversely, plant reproductive fitness is increased by attraction of pollinators. Interactions can be
altered by other organisms associated with the plant such as other insects, plant pathogens, or mycorrhizal fungi. Plant
phenotype is plastic and can be changed by epigenetic factors in adaptation to periods of biotic stress. Space and time
play crucial roles in influencing the outcome of interactions between insects and plants.

Key words: Chemical ecology, coevolution, herbivores, insect–plant interactions, pollinators, spatio-temporal dynamics.

Introduction
The purpose of this review is to consider the important role the insects (non-host plants). Thus, in an environment with
played by time and space in insect–plant interactions. Great changing availability and quality of host plants, phytopha-
advances are being made in understanding the mechanistic gous insects are under selection pressure to find quality hosts
basis by which insects interact with their host plants (reviewed (Bruce et al., 2005). To maximize their fitness they need to
by Hogenhout and Bos, 2011; Mithoefer and Boland 2012; locate suitable plants and avoid unsuitable hosts (Bruce and
Smith and Clement, 2012). The ecological and evolutionary Pickett, 2011). Thus, they have evolved a finely tuned sensory
context of these interactions requires consideration because system for detection of host cues and a nervous system capable
they are dynamic and what occurs at one point in time may of integrating inputs from sensory neurons with a high level
not occur at another. Insects are programmed to recognize of spatio-temporal resolution (Martin et al., 2011). Time and
and rapidly respond to patterns of host cues. Particularly space also influence plant responses to insects; for example, a
specialist insect species have to find specific plant species on history of pre-exposure can prime plant defence responses so
which they can feed and reproduce (host plants) among plant that plants respond more quickly and strongly when they are
species that do not support feeding and/or reproduction of attacked again (Ton et al., 2007, Jinwon et al., 2011).

© The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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456 | Bruce

The phytophagous insects that exist today and the plants their beneficial animal pollinators (Yuan et al., 2013). The
they feed on are the product of a coevolutionary process that fossil record shows that pollination originated 250 million
has been ongoing for 400 million years (Labandeira, 2013) years ago (Labandeira, 2013). Some plants have evolved with
(Fig. 1). However, insect responses to host plant cues from their pollinators and produce olfactory messages which make
their external environment can be very quick because they them unique for their specific pollinators (Grajales-Conesa
have a sophisticated system for sensing their external envi- et al., 2011). For example, certain orchid flowers mimic aphid
ronment and processing the sensory input (Martin et al., alarm pheromones to attract hoverflies for pollination (Stoekl
2011). In particular, decisions made during flight, such as et al., 2011).
which plant to land on, are exceedingly rapid and made in Furthermore, insect herbivores can drive real-time eco-
a timescale of tens to hundreds of milliseconds (Cardé and logical and evolutionary change in plant populations. Recent
Willis, 2008; Baker, 2009; Bruce and Pickett, 2011). This is studies provide evidence for rapid evolution of plant traits
because odour plumes are patchy in structure and insects that confer resistance to herbivores when herbivores are pre-
encounter pockets of host odour only for fractions of a sec- sent but for the evolution of traits that confer increased com-
ond. Moreover, insect responses are sensitive to combina- petitive ability when herbivores are absent (Agrawal et al.,
tions of host cues because exposure to plant volatiles as a 2012; Hare, 2012; Züst et al., 2012). While phytophagous
blend can elicit an entirely different response from individual insects have been adapting to exploit their hosts, the plants

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compounds (Riffell et al., 2009; Webster et al., 2010). By have simultaneously been evolving defensive systems to coun-
being sensitive to combinations of cues, insects can maxi- teract herbivore attack (Anderson and Mitchell-Olds, 2011;
mize the information they gather from their environment. Johnson, 2011).
Consequently this means that the context of cues can be very Studies of fossil plant–insect associations suggest that
important in influencing the behaviour elicited. Responses insects have been feeding on plants for 400 million years
can also change with learning behaviour, such as if a par- (Labandeira, 2013). Coevolution between insects and plants
ticular cue or set of cues is associated with a reward (e.g. was drawn attention to in the classic review by Erhlich and
Hartleib et al., 1999). Raven (1964). Thus, the phenotypic traits and interactions
There is much interest in phytophagous insects due to we see today are the legacy of a long history of associa-
their role as pests in agricultural ecosystems and the negative tion between the organisms and reciprocal adaptations that
effect this has on food security for humanity (Bruce, 2010). provide fitness advantages (Gomez et al., 2010). There is a
However, other types of insect–plant interactions exist. trend for phytophagous insects to become more specialized
Insects play very important roles as pollinators and the nat- in host plant use over time, although some important agri-
ural enemies of the herbivore insects are also beneficial. At cultural pest species are polyphagous. Ecological specializa-
the other extreme there are carnivorous plants that consume tion involves subtle and complex interplay between species
insects (Renner and Specht, 2013). For nature conservation and is not limited to the plant and the herbivore but can
in wild habitats, insect–plant interactions are very interesting also be influenced by multitrophic interactions (Forister
because the coevolutionary forces can drive speciation and et al., 2012). There can also be bidirectionality in transi-
increase biodiversity. tions between generalist and specialist lineages and Janz
and Nylin (2008) have proposed an oscillation hypothesis
in which periods of host range expansion are followed by
Coevolution periods of specialization, as seen in the leaf-mining fly genus
Phytomyza.
The huge number species of flowering plants on our planet
Divergent selection exerted on ecological traits may
(approximately 275 000) is thought to be the result of adap-
result in adaptive population differentiation and reproduc-
tive radiation driven by the coevolution between plants and
tive isolation, and affect differentially the level of genetic
divergence along the genome (Jaquiery et al., 2012). The
4. induced defence pea aphid (Acyrthosiphon pisum) genome has provided
hours
some insight into candidate genes that allow insect adapta-
tion to host plants because it is a species complex of diver-
3. settlement/colonisation
gent host races. Differences between races were found in
olfactory receptor genes and three genes encoding salivary
minutes
proteins (Jaquiery et al., 2012), although it is not known
2. host plant decisions made in flight (land
or not?) at which point in speciation these gene changes occurred
or if they definitely played a causal role in the speciation
milliseconds process. Drosophila sechellia, which has evolved to special-
1. coevolution of plants and insects
ize on Morinda citrifolia fruit, provides another interest-
400 million years ing example: compared to Drosophila melanogaster it has
higher expression levels of neurons ab3 and ab3B, sensi-
Fig. 1. The different timescales associated with insect–plant interactions.
The timescale over which mechanisms have evolved is very long tive to hexanoate esters and 2-heptanone, respectively, thus
whereas the actual mechanisms themselves operate over much shorter making it better able to recognize Morinda fruit odours
periods. (Ibba et al., 2010).
 Dynamic interplay between insects and plants | 457

Host/non-host odour recognition the components of a synthetic host volatile blend of grape
odours (comprising (E)- and (Z)-linalool oxides, nonanal,
The way in which insects use plant volatiles to recognize their decanal, (E)-caryophyllene, and germacrene-D), while keep-
host plants (Fig. 2), which usually involves blends of com- ing the concentration of the other compounds constant, sig-
monly occurring volatiles in specific combinations or ratios, nificantly reduced female attraction in a wind-tunnel study
has been reviewed previously (Bruce et al., 2005; Bruce and with grape berry moth (Paralobesia viteana).
Pickett, 2011) and will not be described at length here. The
time dimension is of major significance because whether or
not odours arrive simultaneously at the antenna can change How insect responses change over time
the type of behavioural response elicited in the insect. Blend
combinations play a crucial role as evidenced by a study with Insects have a nervous system and the capacity to learn
host odours of the black bean aphid, Aphis fabae, in which which has consequences for their responses to plant volatiles
odours presented individually in an olfactometer were repel- (Cunningham et al., 2004; Bruce and Pickett, 2011; Webster
lent but when put together as a blend became attractive et al., 2013). Learning behaviour, such as when an odour is
(Webster et al., 2010). This, although an extreme example, associated with a reward, can affect the strength or even the
demonstrates that the behavioural response does not only type of response to plant stimuli. For example, hawkmoths
depend on the molecular structure of the plant volatile but (Manduca sexta) are innately attracted to blends of particu-

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also on the context in which it is perceived. lar night-blooming flowers, but, when there are not enough
In 2005, I suggested that insects use a ‘coincidence detec- of these hawkmoth-adapted flowers in the habitat, moths
tion’ mechanism in which high spatio-temporal resolution of learn to associate the odours of bat-pollinated Agave palm-
odours allows them to recognize host odour blends and dis- eri flowers which have a completely different smell (Riffell
tinguish them from combinations of non-host odours. A com- et al., 2013). Thus, processing of stimuli through two olfac-
bination of olfactory and visual cues can further enhance tory channels, one involving an innate bias and the other a
attraction (e.g. Han et al., 2012). There is also active avoid- learned association, allows the moths to exist within a chang-
ance of non-host odours (Bruce and Pickett, 2011). Early ing environment.
evidence for this came from the finding of olfactory recep- A more extreme example occurred in a laboratory study
tor neurones (ORNs) tuned to specific non-host compounds, where Spodoptera littoralis moths were trained to extend their
3-butenyl isothiocyanate and 4-pentenyl isothiocyanate, in proboscis (a feeding response) in response to (Z,E)-9,11-
the black bean aphid (Nottingham et al., 1991). When these tetradecadienyl acetate, which is a sex pheromone that usu-
isothiocynates were tested in an olfactometer bioassay, they ally elicits sexual behaviours (Hartlieb et al., 1999). However,
were found to be repellent. it has been shown that some odours are learnt better than
Ratios can also be important; for example, Cha et al. others in particular insect–plant interactions; for example,
(2011) found that doubling the concentration of any one of honey bees learn linalool and 2-phenylethanol better than

host odour blend

H

non-host odour blend

herbivore
induced
plant
volatiles
(HIPVs)

below-ground organisms or
abiotic stress can change
above-ground volatile emission

Fig. 2. The challenge of host recognition: not only do herbivorous insects need to discriminate between host and non-host but they also have to select
good quality hosts. Hosts already attacked by other insects may have defences induced and be lower quality. Other biotic and abiotic stresses that
change plant quality can also change the profile of volatiles emitted thus providing further information to foraging insects. This figure is available in colour
at JXB online.
458 | Bruce

other oilseed rape volatiles (Pham-Delegue et al., 1993). This induced defence against pathogens and the jasmonic acid
suggests that there is a hierarchy and an innate preference for (JA) pathway with defence against herbivores (Ballare, 2011).
certain odours (Bruce and Pickett, 2011). Natural enemies However, numerous studies have shown a more complex pic-
can also learn. It appears that generalist egg and larval para- ture, with varying involvement of both pathways in different
sitoids respond innately to herbivore-induced plant volatiles pathogen and herbivore interactions depending on the species
(HIPVs) whereas specialists rely more on associative learning involved (Stout et al., 2006; Bruce and Pickett 2007; Diezel
(Peñaflor et al., 2011a). et al., 2009).
Innate responses allow insects to respond rapidly to reli- Plant secondary metabolism also provides indirect
able cues that occur in favourable situations, such as γ– defence by attracting natural enemies of pests (Turlings
octalactone, the Oriental fruit fly oviposition stimulant et al., 1990; De Moraes et al., 1998; Dicke and van Loon,
(Damodaram et al., 2014) or, conversely, to avoid detrimental 2000; Heil, 2008). Studies with mutants have revealed that
situations. An example of the latter is geosmin, a compound herbivore-induced plant volatile (HIPV) release requires
associated with harmful toxic microbes, that is repellent to the jasmonate-signalling pathway in Arabidopsis exposed to
D. melanogaster (Stensmyr et al., 2012). They have a dedi- aphids (Girling et al., 2008; de Vos and Jander, 2009) and
cated olfactory circuit with sensory neurons expressing the in tomato exposed to hawkmoth larvae (Degenhardt et al.,
olfactory receptor Or56a that target the DA2 glomerulus 2010) but other systems could be different. The homoterpe-

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and connect to projection neurons that respond exclusively nes 4,8-dimethylnona-1,3,7-triene (DMNT) and 4,8,12-tri-
to geosmin. methyltrideca-1,3,7,11-tetraene (TMTT) are among the
The physiological condition of an insect has long been most widespread HIPVs produced by angiosperms and the
known to influence insect–plant interactions (Dethier, 1982). metabolic pathway and biosynthetic pathway underpinning
When the insect is satiated it will be less motivated to respond their production has been elucidated in Arabidopsis (Tholl
to food odours; for example, the response of D. melanogaster et al., 2011). Recently it has been shown that HIPVs can
to vinegar is modulated by hunger (Ruebenbauer et al., 2008; increase plant fitness; evidence for this was provided by a
Becher et al., 2010). Similarly, when a female insect has field study (Schuman et al., 2012) in which HIPV-emitting
already laid eggs she will be less attracted to oviposition cues. Nicotiana attenuata plants produced twice as many buds
Female insects are influenced by mating which can induce and flowers as HIPV-silenced plants. Predators (Geocoris
profound physiological changes. After mating, S. littoralis spp.) reduced herbivore loads by 50% on HIPV-emitters.
switches its behavioural response to olfactory cues from food- There is variation in responsiveness to insects between dif-
associated ones to oviposition-associated ones (Saveer et al., ferent genetic lines of plants. This is particularly apparent
2012). Unmated females are strongly attracted to lilac flow- in maize where some lines produce a clear HIPV signature
ers but, after mating, attraction to floral odour is abolished following attack by larvae (Degen et al., 2004; Degen et al.,
and they fly instead to the green-leaf odour of the larval host 2012) or oviposition (Tamiru et al., 2011) while others show
plant cotton (Gossypium hirsutum). little or no response. This suggests that some lines are better
able to recognize insect elicitors (see How Plants Recognize
Insects section below).
As well as influencing their natural enemies, HIPV emission
Plant defence
can also affect the herbivores themselves by repelling further
Plants have had to defend themselves against insect attack. colonization (de Moraes et al., 2001; Kessler and Baldwin,
Being rooted to the ground they are unable to flee from attack- 2001; Bruce et al., 2010). An elegant study by Signoretti
ing herbivores. They have evolved a wide range of sophis- et al. (2012) showed that female Spodoptera frugiperda moths
ticated defence systems to protect their tissues (De Moraes respond strongly to maize HIPVs. Females preferred vola-
et al., 2001; Kessler and Baldwin, 2001; Ballare, 2011). These tiles released by undamaged plants to those from herbivore-
include toxic or anti-feedant secondary metabolites that induced plants but the timing of events was important and
represent a major barrier to herbivory (Harborne, 1993; the effect was not seen with freshly damaged maize odours
Mithoefer and Boland, 2012), and physical defences such as (0–1 h) but only 5–6 h after attack. Preference for undamaged
lignin (Franceschi et al., 2005). These provide direct defence plants makes ecological and evolutionary sense because it
via toxic, anti-nutritive or repellent effects on herbivores. provides an adaptive strategy to avoid competitors and natu-
Examples of defensive secondary metabolites include ral enemies for offspring. Plants are also sensitive to HIPV
protease inhibitors in wild relatives of pigeonpea that are emission from their damaged neighbours (Baldwin et al.,
effective against the cotton bollworm, Helicoverpa armig- 2006). Responses to HIPVs and other stress-associated vol-
era (Parde et al., 2012), threonine deaminase in tomato that atiles appear to occur over relatively short distances (Frost
degrades threonine in the insect gut (Gonzales-Vigil et al., et al., 2008). This may be an adaptive mechanism to avoid
2011), 7-epizingiberene in the glandular trichomes of wild responding unless concentrations are high enough to indicate
tomato (Bleeker et al., 2012), and O-acyl sugars in the glan- a real threat.
dular trichomes of tomato and other plants in the Solanaceae Not only do plants respond to insect feeding damage
(Schilmiller et al., 2012). Some chemical defences are con- but they have also been shown to be responsive to insect
stitutive while others are induced after attack. The salicylic egg laying, the very earliest stage of insect attack (Hilker
acid (SA) pathway is often, but not always, associated with and Meiners, 2006). This is of considerable adaptive value
 Dynamic interplay between insects and plants | 459

because it allows the plant to prepare defences even before the wounding or application of herbivore oral secretions unlike
damaging feeding stages of the insect life cycle have started. mechanical wounding (Maffei et al. 2004). Recent evidence
Thus, certain plants emit HIPVs following insect oviposition suggests that depolarization plays a role in the systemic spread
which attracts natural enemies (Tamiru et al., 2011; Fatouros of herbivore-induced defence through a plant (Mousavi
et al., 2012) or increase direct defences so that insect growth et al., 2013). Longer term changes can also occur after stress
rates are reduced on plants that are exposed to eggs (Beyaert and increased resistance may even be observed in subsequent
et al., 2012; JinWon et al., 2012; Geiselhardt et al., 2013). In generations due to epigenetic imprinting (Bruce et al., 2007;
some interaction systems oviposition actually leads to a sup- Luna et al., 2012, Rasmann et al., 2012).
pression of plant volatile emission and a change in the ratio The biological role of plant defence chemicals can change
of compounds, something which natural enemies may (Bruce over time. Although many plant secondary metabolites
et al., 2010) or may not (Peñaflor et al., 2011b) be tuned into. have evolved as plant defence, insects may overcome the
A highly interesting study by Gouhier-Darimont et al. defences by coevolving adaptations such as cytochrome
(2013) showed that treatment of Arabidopsis with cabbage P450 monooxygenases (P450s) that metabolize plant toxins
white butterfly (Pieris brassicae) egg extract caused a rapid (Schuler and Berenbaum, 2013). For example, cotton boll-
induction of early PAMP-responsive genes. Expression of worm (Helicoverpa armigera) uses a P450, CYP6AE14, to
the defence gene PR-1 required EDS1, SID2, and, partially, detoxify gossypol (Mao et al., 2007); hawkmoth can feed on

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NPR1, thus implicating the SA pathway downstream of egg O-acyl-sugar-producing N. attenuata (Weinhold and Baldwin,
recognition. Then in a search for putative receptors of the 2011); and many Brassica specialists have evolved adapta-
egg-derived elicitors, a receptor-like kinase mutant, lecRK- tions to thrive on glucosinolate-producing plants (Winde and
I.8, was identified which displayed a much reduced induction Wittstock, 2011; Bruce, 2014). Specialist insects may even use
of PR-1 in response to egg extract treatment. This discovery the plant secondary metabolites to defend themselves against
of a putative plant receptor suggests that molecular recogni- their own attackers at the third trophic level (Boppré, 1978).
tion processes exist in plants that allow them to detect mol- The molecular basis of resistance to toxic cardenolides has
ecules associated with insects. been well defined (Dobler et al., 2012) and involves an amino
acid change on the transmembrane sodium channel, which is
the target site of the toxin. There has been convergent evolu-
tion with several insect species evolving the same amino acid
How plant responses change over time
change (Dobler et al., 2012). Insights into the evolutionary
Plant defences are orchestrated both in time and space by process have been obtained from studies of the recent host
highly complex regulatory networks that themselves are fur- shift to tobacco (Nicotiana tabacum) by the peach-potato
ther modulated by interactions with other signalling pathways aphid, Myzus persicae. Tobacco-adapted aphid races were
(Maffei et al., 2007). Defences can be constitutive or induced. found to overexpress a cytochrome P450 enzyme (CYP6CY3)
Time is of crucial importance where defences are induced or that allows them to detoxify nicotine (Bass et al., 2013).
primed (Conrath et al., 2006; Ton et al., 2007; Bruce et al.,
2007). Primed plants respond more quickly and strongly
when they are attacked again (Ton et al., 2007; Jinwon et al.,
Insect effectors
2011). Metabolites and energy can, thus, be more efficiently
allocated to defensive activities when there is a mechanism Insect oral secretions contain specific proteins and chemicals
for recognizing the herbivore challenge and triggering precise that are likely to have evolved as effectors to inhibit plant
timing of the adaptive modulation of the plant’s metabolism defences but, with time, some plants have adapted to recog-
(Mithoefer and Boland, 2012). nize some of these substances so that they may even trigger
Plants have evolved ways to adjust their phenotype in defence responses (Hogenhout and Bos, 2011). Salivary pro-
terms of defence gene expression levels according to the level tein C002 was shown by Mutti et al. (2006) to play a cru-
of threat they face. Induced resistance represents a contin- cial role in pea aphid survival and, when knocked down by
uum of phenotypes that is determined by the plant’s ability RNAi, reduced time spent by aphids in contact with phloem
to integrate multiple signals of plant and herbivore origin sap when feeding on broad bean, Vicia faba (Mutti et al.,
(Jinwon et al., 2011). Early events in induced defence such as 2008). Candidate effectors were identified from the aphid
accumulation of reactive oxygen species (ROS) and calcium Myzus persicae by Bos et al. (2010) and of these Mp10 and
signalling are very rapid and occur in the first few minutes of Mp42 reduced aphid fecundity whereas MpC002 enhanced
contact between the insect and the plant (Maffei et al., 2007). aphid fecundity when overexpressed in Nicotiana benthami-
Herbivores (and pathogens) induce Ca2+ influx by opening ana. Although there may be differences when these proteins
calcium channels and this triggers a series of cascade events, are expressed by the aphid instead of being continuously
including ROS production. It is likely that these channels expressed in the plant it appears that Mp10 and Mp42 benefit
are associated with plant receptors tuned to insect elicitors. the plant rather than the aphid. It is possible that N. bentha-
A rapid increase in ROS concentration can also occur after miana has receptors that detect Mp10 and Mp42 and trigger
tissue damage caused by both biotic and abiotic injuries. defence metabolism. Phloem-feeding insects need to over-
Herbivore wounding is different from mechanical wounding; come plant physical defence mechanisms based on plugging
Ca2+ influx and depolarization is maintained after herbivore the sieve tubes with callose or proteins (Will et al., 2013) and
460 | Bruce

require effectors for this. With the increasing availability of damaged-self compounds produced after insect attack (Heil
aphid genome and transcriptome sequence data, aphid effec- et al., 2012). miRNAs have also been implicated in insect–
tor biology is an expanding area of research (Rodriguez and plant interactions (Pandey and Baldwin, 2007; Kettles et al.,
Bos, 2013). 2013). Sattar et al. (2012) found that Aphis gossypii miRNAs
Oral secretions are likely to be a major factor in limiting were differentially regulated during resistant and susceptible
the host range of herbivorous insect species and biotypes, interactions with different melon lines, some possessing the
particularly aphids (Elzinga and Jander, 2013). Insect oral Vat resistance gene and others not.
secretions include salivary enzymes such as glucose oxidase Recognizing the herbivore challenge to allow precise tim-
and β-glucosidase, peptides like inceptin, and fatty acid con- ing of appropriate plant metabolic responses is important
jugates (FACs) like volicitin that can trigger plant defence so that metabolites and energy are efficiently allocated and
responses (Wu and Baldwin, 2009) but also suppress defence correctly timed (Mithoefer and Boland, 2012). However, for
(Eichenseer et al., 2010; Consales et al., 2012) depending on most insect–plant interactions, relatively little is currently
whether the plant or the insect is ahead in the evolutionary known about the molecular basis of insect perception by
game. Aphid honeydew has also been shown to suppress plants, the signalling mechanisms directly associated with this
induced plant defence (Schwartzberg and Tumlinson, 2013). perception, or how plants differentially discriminate between
Highly polyphagous species, like Helicoverpa zea, are more different species of attacking insects (Bonaventure, 2012).

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likely to possess relatively high levels of salivary glucose oxi- Plant–pathogen interactions have been better defined in this
dase (GOX) for suppression of plant defences, compared respect and effector-based models of insect–plant interac-
to species with a more limited host range (Eichenseer et al., tions are now being put forward (Hogenhout and Bos, 2011).
2010). However, plants can adapt; for example, recognition The chemical ecology literature has many examples of plants
of H. zea GOX in tomato may represent a case for effector- responding to volatiles such as HIPVs and other chemi-
triggered immunity (Tian et al., 2012). Intricate adaptations cals that activate defence (reviewed by Baldwin et al., 2006;
have evolved with specialist herbivores; for example, velvet- Arimura et al., 2009). Thus plants not only respond directly
bean caterpillar (Anticarsia gemmatalis) evades detection by to molecules from attacking organisms but can also respond
cowpea by converting fragments of chloroplastic ATP syn- to volatiles released by other plants which are under attack
thase gamma-subunit proteins, termed inceptin-related pep- (Arimura et al., 2009).
tides, that usually function as an elicitor of plant defence into Putative receptors are known but their ligands have not yet
an antagonist effector (Schmelz et al., 2012). been identified. For example, three genes conferring resist-
ance to insects have been identified in plants and are all mem-
bers of the NB-LRR family: the Mi-1 gene in tomato confers
How plants recognize insects resistance to Macrosiphum euphorbiae (Rossi et al., 1998), the
Bph14 gene in rice confers resistance to Nilaparvata lugens
All living organisms face the shared challenge of detecting (Du et al., 2009), and the Vat gene in melon provides resist-
and responding to chemical stimuli from their external envi- ance to A. gossypii (Boissot, 2010). The mechanism of resist-
ronment. Detection of molecules associated with attacking ance is thought to involve the putative receptors binding to
organisms is crucial for eliciting behavioural, physiological, as yet unidentified insect effectors. The pests involved are all
and biochemical responses to ensure survival. Being unable in the insect order Hemiptera, which are stealthy herbivores
to flee from attack, plants have had to evolve sophisticated with a sucking mode of feeding, and it seems likely that the
ways of detecting attackers and it is becoming increasingly HAMP is a small molecule or protein contained in the insect’s
clear that they can detect and respond to a wide range of saliva.
molecules. Pattern recognition is a fundamental process in It is possible that the detergent-like properties of fatty acid
the immune responses of both plants and animals (Boller conjugates could disrupt plasma membranes and cause influx
and Felix, 2009) and there is much biomedical literature of Ca2+ thus triggering responses. However, radiolabelled
relating to this subject (reviewed by Akira et al., 2006). It is volicitin has been shown to bind rapidly, reversibly, and satu-
becoming increasingly clear that molecular recognition via ratably to plasma membranes (Truitt et al., 2004) suggesting
ligand–receptor binding phenomena plays important roles in that there is an interaction with a receptor. HAMPs have also
plants (Boller and Felix, 2009; Monaghan and Zipfel, 2012; been identified from insect egg ovipositional fluid (Hilker and
Erb et al., 2012) and that this plays a role in insect–plant Meiners, 2006; Tamiru et al., 2011). The chemical structures
interactions (Prince et al., 2014; Chaudhary et al., 2014). The of these have been identified as bruchins for the pea wee-
identification of receptors and ligands is crucial to under- vil, Bruchus pisorum (Doss et al., 2000), and benzyl cyanide
stand specificity in plant immunity to herbivores (Erb et al., for P. brassicae (Fatouros et al., 2008). Systemic changes in
2012). Plants possess surveillance systems that are able to defence gene expression can also occur, such as when insect
detect highly specific herbivore-associated cues as well as eggs are deposited on one leaf, other egg-free leaves also have
general patterns of cellular damage, thus allowing them to induced volatile emission (Tamiru et al., 2011).
mount defences. Molecular recognition mechanisms under- A highly interesting study by Gouhier-Darimont et al.
pin this process with receptors tuned to herbivore-associ- (2013) showed that treatment of Arabidopsis with P. bras-
ated molecular patterns (HAMPs; Mithofer and Boland, sicae egg extract caused a rapid induction of early PAMP-
2008; Hogenhout and Bos, 2011; Bonaventure, 2012) or responsive genes. Expression of the defence gene PR-1
 Dynamic interplay between insects and plants | 461

required EDS1, SID2, and, partially, NPR1, thus implicat- beetles can secrete symbiotic bacteria into wounded plants
ing the SA pathway downstream of egg recognition. Then in that elicit SA-regulated defences (Chung et al., 2013). Due
a search for putative receptors of the egg-derived elicitors, a to negative crosstalk with jasmonate-regulated defences this
receptor-like kinase mutant, lecRK-I.8, was identified which makes plants more suitable for the chewing herbivore. The
displayed a much reduced induction of PR-1 in response traditional plant–herbivore concept needs to be updated to
to egg extract treatment. This discovery of a putative plant include the role of micro-organisms in insect–plant interac-
receptor suggests that molecular recognition processes exist tions; for example, yeast, not fruit volatiles, stimulate D. mel-
in plants that allow them to detect molecules associated with anogaster attraction, oviposition, and development (Becher
insects. et al., 2010). Sugio et al. (2011) showed that phytoplasma
protein effector SAP11 enhances insect vector reproduction
by manipulating plant development and defence hormone
Interactions between insects and other biosynthesis.
organisms associated with plants By sharing the same host plant above-ground and below-
ground insects can influence each other even though they are
Although biologists often study individual interactions of not in direct contact (Bruce and Pickett, 2007). For exam-
one species of insect with one species of plant, the reality in ple, Robert et al. (2012) found that Diabrotica virgifera lar-

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nature is more complicated because plants are exposed to mul- vae showed stronger growth on roots previously attacked by
tiple attacking and beneficial organisms (Bruce and Pickett, conspecific larvae, but performed more poorly on roots of
2007; Lucas-Barbosa et al., 2011). Much less is known about plants whose leaves had been attacked by larvae of the moth
the effect of multiple, co-occurring stress factors than indi- S. littoralis.
vidual biotic and abiotic stresses, despite the fact that mul-
tiple stresses are probably the rule under natural conditions
(Holopainen and Gershenzon, 2010). Conclusions
Negative crosstalk between plant defence pathways means
Ecological interactions between insects and plants are
that time can have an impact on these multi-species interac-
complicated and dynamic. What occurs in one system at
tions due to differences in the sequence in which plants are
one snapshot in time may not occur again at another snap-
exposed to different organisms. Thus, the chronological order
shot at a different time and each insect–plant system has
in which attackers arrive at a plant matters: later arrivals will
its own unique features. Both the insect and the plant can
perform better or worse according to the types of defence
change over time: the insect changes because of learning
that have been induced or primed by the earlier arrivals. Soler
behaviour in the short term and by gene mutations in the
et al. (2013) proposed that the outcome of intra-feeding guild
longer term; the plant changes due to induced defence pro-
interactions is generally negative due to induction of simi-
cesses in the short term, epigenetic changes in the medium
lar phytohormonal pathways, whereas between-guild inter-
term, and gene mutations in the longer term. There is vari-
actions are often positive due to negative signal crosstalk.
ation between different strains of both insects and plants.
However, each interaction should be considered individu-
The genetic and temporal variability of biological material
ally because it also depends whether the previous attacker
allows survival in an environment which is also dynamic and
managed to suppress plant defences against it or whether it
not entirely predictable. Interactions are complicated even
activated them.
further because the history of exposure to other associated
Interactions with the third trophic level can also change the
insects can change the suitability of a plant to the insect
outcome of insect–plant interactions. For example, Wilson
being considered.
and Leather (2012) found that cereal aphids preferred larvi-
Agricultural environments are often simplified with less
positing on nutritionally superior wheat cultivars, but in the
habitat diversity than natural ecosystems. Furthermore, many
presence of the harlequin ladybird, Harmonia axyridis, they
of the natural resistance traits that exist in wild plants may
changed their preference to nutritionally inferior cultivars
have inadvertently been lost while selecting for crop yield and
apparently because the risk of predation was lower on these.
quality in a pesticide-treated background. To reduce pesticide
HIPVs are important in tritrophic interactions. Although this
dependency, agriculturalists are faced with the challenge of
review has focussed mainly on plant–herbivore interactions,
bringing the resistance mechanisms found in wild plants back
we should remember that any negative effects of HIPVs on
into the elite crop cultivars (Bruce, 2012) and improving bio-
pollinator visitation rates are likely also to exert selection pres-
control by natural enemies of pests. Reducing the losses to
sure on HIPV emission (Lucas-Barbosa et al., 2011). Another
global harvests caused by pests, which remain high even with
consideration is that attraction of natural enemies may be
pesticide use, could provide a tangible way of producing more
compromised if their hyperparasisoids are also attracted to
‘crop per drop’ or unit area of land.
the HIPVs (Poelman et al., 2012).
Microbial mutualists may be more important ‘hidden play-
ers’ in insect–plant interactions than is currently realized
Funding
(Frago et al., 2012). A very interesting interaction between
organisms is the use of symbiotic bacteria by Colorado potato Rothamsted Research receives grant-aided support from the
beetle to evade antiherbivore defences of its host. These Biotechnology and Biological Sciences Research Council.
462 | Bruce

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