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Aphid-plant interactions: a review

a b
Emilio Guerrieri & Maria Cristina Digilio
a
Istituto per la Protezione delle PianteConsiglio Nazionale delle Ricerche, Portici, (NA),
Italy
b
Dipartimento di Entomologia e Zoologia Agraria “Filippo Silvestri”, Università degli
Studi di Napoli “Federico II”, Portici, (NA), Italy

Version of record first published: 19 Nov 2008.

To cite this article: Emilio Guerrieri & Maria Cristina Digilio (2008): Aphid-plant interactions: a review, Journal of Plant
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 Journal of Plant Interactions
Vol. 3, No. 4, December 2008, 223
232

REVIEW ARTICLE
Aphid-plant interactions: a review
Emilio Guerrieria* and Maria Cristina Digiliob

a
Istituto per la Protezione delle Piante, Consiglio Nazionale delle Ricerche, Portici (NA), Italy; bDipartimento di Entomologia e
Zoologia Agraria ‘‘Filippo Silvestri’’, Università degli Studi di Napoli ‘‘Federico II’’, Portici (NA) Italy
(Received 8 July 2008; final version received 20 October 2008)

Aphids are economically important insect pests of agriculture and forest crops. They feed on phloem sap by
extremely efficient mouthparts modified into long and flexible stylets. Adaptation to phytophagy is completed by
an extremely ductile reproduction system that can alternate biparental and parthenogenetic generations. In order
to reach plant phloem, aphids must overcome plant defences, either physically and/or chemically. However,
plants respond to aphid attack by activating defence genes that lead to the production of physical barriers and/or
chemical toxic compounds (direct resistance). In addition, attacked plants can attract the natural enemies of
aphids by releasing specific volatile compounds (indirect resistance). We can take advantage of these different
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types of resistance in order to enhance the sustainable control of these phytophagous insects. In this review we
summarize the main aspects of plant-aphid interactions, focusing on those issues that can have an economic
application.
Keywords: Aphidoidea; phloem-feeder; plant response; multitrophic interactions; natural enemies

Introduction affected by the presence of aboveground and below-

‘Aphid’ is the common name for the insects belonging
to the superfamily Aphidoidea, within the order
Hemiptera. There is virtually no part of terrestrial
plants that is not attacked by an aphid, either above
or below ground; they can even feed on bark. The
reason lies in the amazing biological features that
these tiny insects have evolved to maximize their
performances as phytophagous insects. The combina-
tion between specific feeding and reproductive habits
concurred in making the aphids one of the most
economically important groups of pest in agriculture;
in temperate climates they are considered the most
important insect pest (Minks and Harrewijn 1989),
especially in those cases where their attack is asso-
ciated with the transmission of phytopathogenic
viruses. Aphids may observe any type of host
specificity, from strict monophagy, e.g., the grape
phylloxera, Daktulosphaira vitifoliae Fitch, to poli-
phagy, e.g., the green peach aphid, Myzus persicae
Sulzer, whose summer generations develop on an
exceedingly wide range of host plant species (Dixon
1987).
In this review we will summarize the main
biological features of this group of insects, with
emphasis on those affecting the interactions with
the host plant. Then, we will try to separate the
bottom-up and top-down effects indicating, where
possible, the key points that need attention for
protecting agricultural plants from these insects.
Moreover, we will try to collocate aphids in a
multitrophic context where their performances are
ground organisms. Finally, we will summarize the
current issues in aphid-plant interactions focusing on
the sustainable control of these pests in agricultural
crops. It is the case here to remember that the
interaction between plant and aphid actually is a
tool for plant physiologists, which use stylectomy
performed with a microcautery unit (Pritchard 1996)
or with laser beams (Valle et al. 1998) to recover pure
phloem sap exudating from these natural syringes.
Outline of aphid biology and behavior
In most cases, aphids feed passively on the content of
plant vascular tissues (generally the phloem), by
means of high pressure within the sieve elements
(Figure 1). Their mouth appendages (maxillae and
mandibles) are elongated into a stylet bundle that
pierces the plant tissues to reach the feeding site in the
phloem, while the distal tip of the labium helps stylet
penetration from the outside, acting as a guide.
Aphids produce two different types of saliva (Miles
1999). The first type is dense and proteinaceous, and,
jellifying around the stylets (stylet sheaths), it con-
stitutes an intercellular path towards the phloem for
the piercing stylets, isolating plant tissues from the
mouthparts, thus preventing plant reaction at the site
of feeding (Felton and Eichenseer 1999). When the
stylets have reached the phloem flow, aphids start to
produce the second type of saliva, referred to as
‘watery’, that is injected directly into the vascular
system of the plant, and contains digestive/lytic

*Corresponding author. Email: guerrieri@ipp.cnr.it

ISSN 1742-9145 print/ISSN 1742-9153 online
# 2008 Taylor & Francis
DOI: 10.1080/17429140802567173
http://www.informaworld.com
 224 E. Guerrieri and M.C. Digilio
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Figure 1. Schematic representation of a feeding aphid. e:
epidermis; hd: honeydew droplet; l: labium, not participat-
ing to the piercing activity (brown); p: parenchyma; sb:
stylet bundle (orange); se: sieve elements (blue); ss: stylet
sheaths (black); st: stylet tip.
enzymes. This feeding habit produces but little
mechanical damage if compared to that of chewing
insects (such as caterpillars), which is hardly per-
ceived by the attacked plant. Indeed, we observe that
the expected plant response to sieve tubes puncturing,
leading to the occlusion of the wound, does not
happen, because of the injected salivary proteins that
interact with calcium of plant tissues (Will et al.
2007). Therefore, plant reaction to invading aphids
takes much more time than does plant reaction to a
chewing insect. However, with respect to chewing
insects, the aphid feeding habit is more precise and
selective, allowing them to avoid allelochemicals and
indigestible compounds that are more abundant in
other plant tissues (Schoonhoven et al. 2007).
The selection/identification of a proper host plant
is achieved by subsequent introductions of the stylets
(probes) until the composition of the sap is analyzed/
recognized, therefore stylet tracks originated from
probing behaviour can also be found on non-host
plants. The feeding behavior of aphids is analyzed in
detail by the use of EPG (electrical penetration
graph), a technique proposed by McLean and Kinsey
(1964) and developed by other researchers (Tjallingii
1988, 2006), which allows the monitoring of stylet
insertion, salivation and sap ingestion.
Plant phloem transports the photosynthate; there-
fore, it constitutes a feeding site that theoretically is
very convenient. However, plant sap is an unbalanced
food for aphids, being composed for the most part by
carbohydrates (mainly sucrose) and, as a nitrogen
source, by free amino acids, but is too low in essential
amino acids in respect to animal necessities, and to
account for the high rate of increase of aphids
(Douglas 2006). Studies with artificial diets contain-
ing [14C] sucrose showed that aphids possess the
ability to synthesize amino acids and lipids from
dietary sugars (Febvay et al. 1999). However, to
obtain essential amino acids, they depend on the
bacterial symbiont Buchnera aphidicola Munson Bau-
mann & Kinsey, hosted in the aphid body cavity in
the cytoplasm of specialized cells (bacteriocytes).
Dietary sugars exceeding dietary needs are synthe-
sized into oligosaccharides and excreted by means of
the well-known honeydew, and this lowers the
osmotic pressure of the ingested sap, otherwise lethal
to aphids (Douglas 2006). Honeydew is actively
searched for by ants, which often attend aphid
colonies and protect them from natural enemies
(such as ladybird predators and parasitic wasps),
causing further damage to crops. Nonetheless, honey-
dew is also used by natural enemies and honey bees as
food (Hogervorst et al. 2007).
Most of the aphid populations that are found on
plants during spring and summer are constituted by
females that reproduce by thelytokous parthenogen-
esis associated to viviparity. Each mature female
generates other females, and, in a matrioska-style
organization, the newly laid nymphs already nest
within them developing embryos, hosting on their
turn the developing embryos of the following genera-
tion (telescoping generations). This type of reproduc-
tion does not need any male intervention. This means
that once a single aphid has reached a proper host
plant, it can generate a new population constituted by
clonal individuals in a few days. Among these mainly
apterous females, winged morphs may appear as a
response to crowding or to the complete exploitation
of the host plant, and still are parthenogenic,
thelytokous and viviparous. The specific task of these
winged forms is the migration towards a new unin-
fested plant. In colder climates, aphids present a
unique biological feature, as they are able to alternate
parthenogenesis and biparental reproduction: at the
end of the summer, sexual morphs appear, and the
female, after mating, produces a single overwintering
egg, characterized by cold hardiness. The presence of
a biparental generation once a year means that aphid
populations take advantage of both the benefits of
parthenogenesis (very convenient to exploit short-
lived hosts), and those of the genetic recombination.
Often, the life cycle occurs between different species
of host plants, with a winter host (usually a tree or a
shrub) and a spring-summer host that can be
herbaceous (host alternation).
 Journal of Plant Interactions 225

Bottom-up interactions: aphid response to plant

features
It is certainly difficult to separate the bottom-up
effects from the top-down ones. Indeed, the feeding
habit of aphids establishes a long-term interaction
with the host plant that is made by a wide variety of
induced, reciprocal, responses. However, it is in the
very first phases of plant selection that it is possible to
assess whether a plant is suitable for an aphid species.
The cues a winged aphid use to decide landing are
visual (Doring and Chittka 2007) and chemical
(Pickett et al. 1992). Some of the volatile compounds
that are involved in the long-distance recognition of a
host plant (broad bean) by Aphis fabae (Scopoli) have
been recently identified (Webster et al. 2008).
Upon arrival on the plant, the first feature
affecting the selection behavior of an aphid is the
presence of trichomes. Regardless their structure,
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whether they are simple or glandular, their density

can heavily affect the success of aphid attack (Musetti
and Neal 1997). Indeed, most of the resistant varieties
of cultivated plants as well as many of their wild
relatives are characterized by trichomes that hamper
aphid movements and stylet insertion (Bin 1979)
(Figure 2a). For example, on the wild species of
tomato Lycopersicon pennellii (Corr.) D’Arcy, it is
virtually impossible to have any aphid development
for the contemporary presence of a high density of
simple and glandular trichomes. The latter produce a
toxic exudate that can trap the aphids and eventually
kill them. In addition, the acyl-sugars that exudate
from some of these trichomes (type IV) have been
reported to be highly repellent towards aphids
(Goffreda et al. 1989), and plant breeders have tried Figure 2. Plant resistance to aphid attack. Direct defences.
to transfer this character into cultivated varieties. (a) Macrosiphum euphorbiae entrapped and killed by
The constitutive presence of trichomes, thorns trichomes on a resistant variety of tomato (b) Acyrthosi-
phon pisum (brown colour) killed by cyanogenic glycosides
and thick cell walls all constitute a specific type of
of lima bean (in the bottom left is a live green aphid).
direct resistance that prevents any feeding activity.
Indirect defences. (c) The aphid parasitoid Aphidius ervi
Nonetheless, these mechanical barriers can be pro- attracted by volatiles released by a broad bean plant heavily
duced in response to the feeding activity of an infested by its host, the aphid Acyrthosiphon pisum (Photo:
invading aphid, and in such a case they are referred MC Digilio).
to as direct induced defences.
Constitutive defences are not only mechanical,
but also chemical, as in Solanum berthaultii Hawkes, distance from the plant surface and the dimensions of
whose glandular hairs produce (E)–farnesene, the the sieve elements that must be compatible with
aphid alarm pheromone (Gibson and Pickett 1983), stylets characteristics. Stylets length and thickness at
that prevents the colonization by inducing a ‘dis- their tip appear to be crucial to let the aphid reach the
persal’ behavior in winged aphids. phloem and feed (Will and van Bel 2006).
Antixenotic defences are particularly effective for Complex biochemical interactions happen when a
those aphid species that transmit phytopathogenic plant is probed, that is when the aphid succeeds in
viruses, because there cannot be any virus infection reaching the phloem with its stylets. Aphids and
without the insertion of stylets. On the contrary, virus plants have evolved together and for this reason, if an
transmission can happen even on non-host plants, aphid reaches a host plant, there is an immediate
because a probing stylet insertion is sufficient for recognition of the substrate, that is achieved by
some type of quickly acquired viral infection, and sensorial structures located at the back of the mouth,
salivation occurs on plants resistant to aphid attack, that are able to characterize the plant sap. If the plant
even if feeding does not follow (Will et al. 2007). is a non-host, the aphid retreats the stylets and leaves,
Overall, there are two main constrains that aphids unless the plant produces toxic compounds that
must cope with during the first phases of attack: the poison it (Schoonhoven et al. 2007).
 226 E. Guerrieri and M.C. Digilio
The presence of compounds that are toxic for
insects is a common feature in the plant world and
many plant families exhibit a wide battery of chemical
defences that can be either constitutive and/or
induced by insect attack (Figure 2b). Within agricul-
tural plants key examples are constituted by the
families Brassicaceae and Solanaceae.
The tissues of Brassicaceae are rich in sulphur
derived compounds (glucosynolates) that have de-
fended them from insects until aphids and moths
evolved species able to overcome this kind of
defences. Today, only few insect species are specia-
lized on Brassicaceae, e.g., the cabbage aphid Brevy-
coryne brassicae L. and the cabbage whites Pieris
brassicae L. and P. rapae L., and compounds that are
toxic to generalist plant feeders are used by these
specialized insects as cues for the identification of
their host plants and for their development. More-
over, the production of such compounds is increased
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following insect infestations, with a cascade effect on
the interactions with their specific antagonists (Gols
et al. 2008).
Similarly, tomato and potato are rich in glycosidic
alkaloids (tomatine, solanine) that protect them from
most insects, bacteria and fungi, even though some of
them evolved to overcome this type of defence, as is
the case of the oligophagous aphid species Macro-
siphum euphorbiae (Thomas) and the generalist My-
zus persicae. Nicotiana spp., which belong to the same
plant family as tomato, produce a well-known
insecticidal compound, nicotine, particularly active
towards aphids, that is skipped by feeding aphids
because it is translocated in the xylem.
Once extracted from plants, several plant second-
ary metabolites can act as insecticides, and indeed
pesticide industry has ‘copied’ from plant compounds
as leads for new products. Recently, essential oils of
the aromatic plants of the families Lamiaceae,
Verbenaceae and Apiaceae have shown aphicide
activity (Digilio et al. 2008).
It is interesting to note that the more toxic a
compound is, the more ecological pressure is put on
insect populations. It is not surprising that aphids
have been able to overcome these types of plant
defences because of their complex and effective
reproductive system that includes a genetical varia-
bility confined to the winter generation and a massive
clonal reproduction in the remaining part of the year.
Once a single aphid develops on a resistant plant, its
progeny will eagerly develop into a resistant popula-
tion. Techniques to measure resistance, both in the
field and in the laboratory, are illustrated by Smith
(2005).
The cloning of the gene Mi-1.2, which confers
resistance to tomato towards the root nematode
Meloidogyne incognita (Kofoid & White) and the
aphid M. euphorbiae, has been a milestone in plant
resistance to aphids (Kaloshian et al. 1997; Rossi
et al. 1998; Vos et al. 1998). This gene follows the ‘R
gene mediated resistance’, a type of molecular sur-
veillance system that allows certain genotypes of
plants to recognize and deter pests that can overcome
non-host resistance. Interestingly, it confers resis-
tance also towards psyllids and whiteflies (Nombela
et al. 2003; Casteel et al. 2006), but not in the sister
plant Solanum melongena L. (eggplant) (Goggin et al.
2006). However, as mentioned for highly toxic
compounds, this type of resistance exerts a high
ecological pressure on target species and for this
reason aphid populations have ‘evolved’ a counter
resistance to the Mi 1.2 (Goggin et al. 2001).
So far, other genes have been associated with
aphid resistance. For example the Vat resistance gene
(monogenic, dominant) in melon governs both an
antixenotic reaction to the melon aphid Aphis gossy-
pii Glover and a resistance to non-persistent virus
transmission, restricted to this vector species (Chen et
al. 1997). A single dominant gene named Rag1 is
responsible for the soybean resistance to the aphid
Aphis glycines Matsumura, which is an important
pest of soybean in North America (Li et al. 2007).
Similarly, in the model plant Medicago truncatula
Gaertner, aphid resistance segregates as a single
dominant gene, AKR, named from the bluegreen
aphid Acyrthosiphon kondoi Shinji and Kondo (Klin-
gler et al. 2005). The molecular bases of plant
resistance to aphids have been reviewed by Smith
and Boyko (2007).
Top-down interactions: plant response to aphid attack
Much more complex are the top-down interactions
that occur when aphids develop on a suitable host
plant. A first, major separation can be made between
aphid attack that is or is not associated with virus
transmission.
Plant response to aphid attack not associated with
the transmission of viruses is extremely variable and
can be associated with a wide degree of symptoms
(Miles 1999).
In favorable conditions (spring/summer), aphid
populations are usually extremely abundant, and can
lead to the complete exploitation of herbaceous hosts.
However, in some cases large populations can de-
velop without evident symptoms, as it happens for
Macrosiphum euphorbiae on tomato plants (Guerrieri
2001). More frequently, plant response collocates in
between the above mentioned extremes, and is
associated to the subtraction of plant nutrients,
accompanied by a progressive decline of the plant,
with unpaired growth and enhanced susceptibility to
the attacks of other insects/pathogens. Examples of
this type of response to aphid attack can be observed
following infestation by generalist aphids, e.g., Aphis
fabae (Scopoli), but also by aphids well adapted to
their host, such as specialized Macrosiphum rosae (L.)
(Miles 1989).
Nonetheless, the injection of aphid saliva can be
extremely toxic, leading to localized chlorosis near
 Journal of Plant Interactions
the feeding site and around the stylet tracks, caused
by chloroplast disruption (Miles 1989), and to
localized tissue damage, as induced by Dysaphis
plantaginea (Passerini) on apple fruits. Growth dis-
tortions are common on citrus leaves attacked by
Aphis spiraecola Patch, and leaves of peach trees can
be curled into a cigar by Myzus varians Davidson.
Systemic effects caused by the feeding of Acyrthosi-
phon pisum (Harris) and Therioaphis trifolii (Monell)
are often recognized on alfalfa.
The injection of aphid saliva can even alter the
hormonal balance of the plant, leading to the
formation of galls or tumours (Figure 3). However,
apart from some substances isolated from the gall
induced by Colopha sp. that are responsible for cell
hypertrophy, no cecidogenic compound has, so far,
been identified in aphid saliva that can artificially
induce gall formation in the attacked plant (Otha
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et al. 2000).
The nutrition hypothesis for the adaptive signifi-
cance of insect gall formation postulates that galls
accumulate higher concentrations of nutritive com-
pounds than uninfested plant tissue, resulting in a
higher performance of the gall former. This has been
demonstrated in the plant Sorbus commixta Hedl,
where the amount of amino acids exuding from cut
galled leaves induced by Rhopalosiphum insertum
(Walker) was five-fold that in ungalled leaves; how-
Figure 3. Plant response to gall-forming aphids. (a) Pem-
phigus spyrothecae. (b) Pemphigus immunis. (c) Pemphigus
vesicarius (Photo: B Espinosa).
227
ever, there was no significant difference in the amino
acid composition (Koyama et al. 2004). Gall forma-
tion is also considered as an ecological adaptation
that guarantees favorable microclimatic conditions to
the aphid, and it may as well protect them from
natural enemies and insecticides. There is a great deal
of specialization, biological complexity and even
variation in the interaction between host plant and
a gall-forming aphid (Wool 2004).
Regardless of the types of direct damage, aphids
produce a huge quantity of honeydew whose crystals
accumulate on leaves surface. During sunny days,
these crystals act as a magnifying lens burning the
plant tissues. More commonly, on honeydew strati-
fies a black layer of saprophytic fungi that blocks the
stomata causing a fall of the leaves and impairs
photosynthesis. In many cases these indirect damages
are by far worse than the simple subtraction of plant
sap.
A completely different situation occurs when
aphids transmit phytopathogenic viruses. There are
many theories about the association between aphids
and viruses, even though many researchers consider it
a symbiosis with mutual benefits. From the aphid
perspective, most virus-infected plants assume a
yellowish coloration that is extremely attractive to
the aphid winged morphs. Moreover, in virus-in-
fected plants, the titre of free amino acids in the sap is
higher with respect to virus-free plants and this
positively affects aphid development and reproduc-
tion. Finally, plant viruses have an indirect beneficial
effect on aphid fitness, by downregulating plant
defence response. From virus perspective, aphids
represent a phenomenal mean of dispersion/injection
and in some cases a favourable host for replication.
However, often viruses circulate throughout the
aphid without replication. Both circulative and re-
plicative viruses make the aphid infective for the rest
of its life, with disastrous consequences for agricul-
tural crops. Following the crowding induced by the
better nutritional conditions of a virus-infected plant,
aphids differentiate winged morphs that migrate to
colonize new uninfected plants, thus actively partici-
pating to disperse the virus.
In the case of virus-transmission, pathogenic
symptoms add to those caused by aphid attack.
There is no cure for aphid-transmitted phytopatho-
genic viruses other than the prevention of aphid
probing.
Different aphid species can coexist on the same
plant. For example, on citrus leaves, it is common to
find colonies of Toxoptera aurantii (Boyer de Fon-
scolombe), A. spiraecola, M. euphorbiae, A. gossypii
living without any manifest interference. Conversely,
it has been demonstrated that previous infestation by
both heterospecific and co-specific aphids enhances
food acceptance by M. persicae on potato, but only at
the feeding site and not systemically (Dugravot et al.
2007).
 228 E. Guerrieri and M.C. Digilio
In some cases, species belonging to the same genus
are able to share the same host plant by developing at
different feeding sites. For example, different species
of Pemphigus spp. attack different tissues of poplar
tree (leaf vein, leaf petiole, leaf blade, branch), each
producing a specific type of gall (Wool 2004) (Figure
3).
More recently other types of plant responses have
been characterized. In detail it has been demonstrated
that both biotic and abiotic stresses alter the compo-
sition of the volatile compounds that a plant releases.
Aphids are no exception and it has been shown that
this change in volatile profiles can regulate the
interactions between aphids and their natural enemies
(see below).
Aphids in a multitrophic context
Aphids appear in many food chains (Kennedy 2003).
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However, it is interesting to note that a key role in
the regulation of aphid populations is played by
other insects (Van Veen et al. 2008), especially those
feeding exclusively on aphid species, i.e., predators,
such as ladybirds (e.g., Coccinella septempunctata L.
and Adalia bipunctata L.) and midges (Aphidoletes
aphidimyza
Rondani-) and parasitoids (e.g., Hyme-
noptera Braconidae Aphidiinae: Aphidius spp. Praon
spp. Tryoxis spp.; Diaeretiella spp.; Hymenoptera
Chalcidoidea Aphelinidae: Aphelinus spp.). The
complex of insects acting as aphid antagonists is
completed by generic predators such as myrids
(Hemiptera), chrysopids (Neuroptera) and syrphids
(Diptera). Not always aphid antagonists have been
perceived as tremendously efficient control instru-
ments, because their action may be delayed in
respect to the build-up of aphid colonies (aphid
populations start to develop in spring), but, when
their action has started, the result is a crash of aphid
colonies that can be observed especially in organic
crops (Tremblay 1973).
During the last 15 years, the key role of the plant
in the recruitment of aphid antagonists has been
recorded in a number of tritrophic systems (Guerrieri
et al. 1993; Reed et al. 1995; Han and Chen 2002;
Girling et al. 2006; Blande et al. 2007; López Pérez et
al. 2007; Pareja et al. 2007; Sasso et al. 2007). With
only one exception (López Pérez et al. 2007), in all
these studies it has been shown that the volatile
compounds released by an aphid infested plant
selectively attract aphid predators and parasitoids
towards their preys/hosts. This feature is referred to
as indirect defence, to stress the fact that the plant
defends itself from herbivore insects through the
intervention of their specific natural enemies (Dicke
et al. 2003).
For example, broad bean plants infested by the
pea aphid Acyrthosiphon pisum are six times more
attractive than uninfested plants towards the para-
sitoid Aphidius ervi Haliday (Guerrieri et al. 1993). In
this system, it has been shown that the changes in
plant volatile emissions that account for this increase
of attractiveness are systemic, thus occurring also in
the undamaged parts of the plant (Guerrieri et al.
1999). Moreover, these changes are produced only
after a prolonged feeding activity by a consistent
aphid population (Guerrieri et al. 2002). The ex-
tended time needed by the plant to ‘realize’ the
presence of an aphid population is strictly linked to
the minimum mechanical damage that is caused by
stylets penetration if compared, for example, to the
destruction of plant tissues performed by chewing
caterpillars.
Aphids (and phloem feeders in general) are
perceived by the plant as they were intermediate
between pathogens and herbivores (Kaloshian and
Walling 2005), thus eliciting a metabolic response
that involves both the salicylic and the jasmonic
acid pathways (Du et al. 1998; Stout et al. 1998,
1999; Sasso et al. 2007; Smith and Boyko 2007;
Girling et al. 2008). These two main metabolic
pathways are known to be mainly activated in
response to phytopathogens and to herbivore
chewers (and to mechanical damage), respectively
(see Agrawal et al. 1999). More recently it has been
reported that plant response to aphids is completed
by the activation of the other known minor path-
ways of ethylene, abscissic acid, giberellic acid,
nitric oxide and auxine (see Smith and Boyko
2007 and references therein).
In many plant-aphid systems, among the identi-
fied compounds whose release is increased by aphid
infestation, methyl-salycilate appears to be a key one.
This compound can be rightly considered the very
end of the salicylic acid pathway and has been shown
to be attractive towards both aphid parasitoids (Sasso
et al. 2007) and predators (James 2003; Zhu and Park
2007). However, the volatile blend released by aphid
infested plants is completed by several terpenes
deriving from the jasmonic acid pathway that is
regulated by the COI gene (Girling et al. 2008), and
by a series of alcohols known to be linked to general
biotic stresses (Sasso et al. 2007).
The deep intimacy of aphid plant interactions is
sometimes demonstrated by the specificity of plant
volatiles released in response to different aphid
species. For example, the changes in volatile emis-
sions released by broad bean plants infested by the
black aphid Aphis fabae do not affect the flight
behavior of A. ervi, as conversely do those induced
by the green aphid Acyrthosiphon pisum (Du et al.
1996, 1998). It is important to note that A. fabae is
not a host for A. ervi and thus the parasitoid wasp is
able to detect the subtle differences in the ‘odors’
induced by these two aphid species feeding on the
same plant and to forage only on those infested by its
natural host A. pisum. In contrast, no significant
preference in orientation behavior by the aphid
parasitoid Diaeretiella rapae (McIntosh) was ob-
served in response to the volatile chemicals produced
 Journal of Plant Interactions
by turnip (Brassica rapa L. var rapifera) exposed to
either Lipaphis erysimi (Kaltenbach) (a specialist on
Brassicaceae) or Myzus persicae (a true generalist)
(Blande et al. 2008). There are at least two main
differences that can be noted in respect to the broad
bean case. First of all, both L. erysimi and M.
persicae can be attacked by D. rapae and thus there
is no advantage for the parasitoid in discriminating
between volatiles induced by the two aphid species.
Moreover, regardless the herbivore species involved,
the volatile profile of infested Brassica is dominated
by isothiocyanates that are highly attractive towards
D. rapae.
The possibility of using plant attractiveness to
enhance the natural control of aphid pests has
prompted a series of studies aiming at indicating
possible ways of eliciting it in uninfested plants.
Aboveground, exogenous applications of a com-
pound derived from jasmonic acid, namely (Z)-
Downloaded by [University of Guelph] at 05:52 04 October 2012
jasmone, resulted in a significant change in the
emission of volatile compounds from uninfested
broad bean plants, making them as attractive
towards A. ervi as the plants infested by A. pisum
(Birkett et al. 2000). More recently, these findings
were confirmed for the model plant Arabidopsis
thaliana (L.), with differences noted in the behavior
of a specialist aphid versus a generalist one on
induced plants (Bruce et al. 2008). However, a
deterrent effect towards aphids was also noted
following treatment with (Z)-jasmone (Birkett et al.
2000; Pickett et al. 2007). Belowground, plant
responses are regulated by a myriad of interactions
that include the soil microfauna as well as neighbor-
ing plants, either conspecific or not, that can affect
indirect and direct defences. For example, root
exudates from A. pisum-infested plants were able
to induce a dramatic increase of attractiveness
towards aphid parasitoids in a nearby uninfested
broad bean plant (Guerrieri et al. 2002). Also weeds
can play a role in the aphid-plant interaction, as
demonstrated for barley plants. Indeed, following
exposure to root allelochemicals from the aggressive
weed couch-grass, Agropyron repens (L.), barley
plants were less accepted by the bird cherry-oat
aphid, Rhopalosiphum padi (L.), and became repel-
lent for the aphids in olfactometer bioassay (Glin-
wood et al. 2003).
Much more complex is the response of a plant to
aphid attack in presence of soil symbionts. For
example, the presence of an arbuscular mycorrhizal
fungus, Glomus mossae (Nicol and Gerd), is able to
induce an increase on both direct and indirect
defences in tomato plants (Guerrieri et al. 2004). In
other words, a drastic reduction in the reproductive
rate of Macrosiphum euphorbiae and a significant
increase of attractiveness towards the parasitoid A.
ervi has been recorded on mycorrhizal tomato plants
in respect to non mycorrhizal ones (Guerrieri et al.
2004). However, there seems to be a species-specifi-
229
city effect of plant-arbuscular mycorrhizal fungus
associations in terms of the final output of these
complex interactions. On a completely different
system, including different plant, fungal symbiont
and aphid species, mycorrhizal symbiosis seemed to
have a positive effect on the fitness of a generalist
aphid (Gange et al. 1999).
Although contrasting, these findings stressed how
belowground interactions could shape the above-
ground insect pest populations through plant media-
tion (Guerrieri and Digilio 2008).
Current issues in aphid-plant interactions and
conclusions
There is probably one main issue that can be
considered pivotal in aphid-plant interactions: plant
resistance. As mentioned above, aphids can be serious
pests of agricultural crops, especially when they are
able to transmit phytopathogenic viruses. In these
cases there is virtually no tolerance to their attack,
and chemical treatments are required to save the
yield.
We are just starting to understand the molecular
basis of the varied plant response to aphid attack, and
resistance sources are actively searched in order to
introduce resistance traits in crops (Goggin 2007).
Now tomato plants commonly cultivated are Mi-
1.2, i.e., resistant to root nematode Meloidogyne
incognita and to aphid Macrosiphum euphorbiae
(Kaloshian et al. 1995, 1998; Rossi et al. 1998).
However, this feature can be even enhanced by
applications of foliar inducers such as the jasmonic
acid and the salicylic acid analog, benzothiadiazole
(BTH) (Cooper et al. 2004).
A decade has passed since this discovery, and just
recently there are a few indications of genes that can
be responsible for aphid resistance. A great help in
this topic has been given by the use of the model
plants Arabidopsis thaliana, whose genome has been
completely sequenced, and Medicago truncatula. In
the characterization of aphid
plant interactions it is
of extreme help the use of both mutants, with known
genes overexpressed or silenced (Girling et al. 2008),
and of near-isogenic lines (NILs) (Gao et al. 2007).
This is true both for direct resistance, which directly
hampers aphid development and reproduction, and
for indirect defence, which is based on the production
of volatile compounds attractive towards the natural
enemies of aphids. For species like tomato, these
features can be also investigated by using wild species
that are highly resistant to phloem feeders, such as
Solanum pennellii and Solanum habrochaites Knapp
and Spooner, whose entire genome has been intro-
gressed into a cultivated variety leading to a series of
introgression lines (ILs) that are available for biolo-
gical tests.
In the absence of viral transmission, the augmen-
tation of the attractiveness of cultivated plants can be
considered as a profitable strategy, inducing no
 230 E. Guerrieri and M.C. Digilio
ecological pressure on aphid populations being linked
to their feeding activity. For example, a cultivar
screening within the most important cultivated spe-
cies can be advisable for assessing which are the best
ones in defending themselves by aphid attack. The
modern techniques can be of great help in reducing
the time needed to transfer the genes involved in
direct and indirect defence against aphids, in respect
to traditional breeding methods. In this view, geneti-
cally modified plants can also integrate the knowl-
edge about the most promising resistance genes in
economically important plant species, such as to-
mato. For example, it has been recently demonstrated
that the overexpression of a gene regulating the
production of systemin, a hormone induced in
tomato by insect chewers and mechanical damage,
is also responsible for a significant increase of the
attractiveness towards an aphid parasitoid through a
quantitative alteration of the volatile compounds
Downloaded by [University of Guelph] at 05:52 04 October 2012
released (Corrado et al. 2007).
Almost unexplored remains the importance of
belowground interactions on the development of
aphid populations and on the attractiveness towards
their natural enemies. With the exception of a few
records there remains a large group of root symbionts
whose presence can have a significant impact on
aboveground aphids and antagonists. For example,
the known positive effects of plant growth promoting
rhizobacteria (PGPR) and of non mycorrhizal fungi
such as Trichoderma spp. on plant performances can
possibly extend to aphid resistance, either direct or
indirect. However, no experimental data are available
for these multilevel interactions. The modern techni-
ques can be of great help in unravelling the intimate
relationship that exists between aphids and plants
and in exploiting plant resistance for the control of
these pests in agriculture. However, this requires a
multidisciplinary approach realized through a thor-
ough collaboration between researchers with different
expertise, such as plant physiologists, geneticists,
entomologists, ethologists, chemists and ecologists,
each one giving a contribution in adding a little piece
of knowledge to the puzzle of aphid-plant interac-
tions.
Acknowledgements
The authors are deeply grateful to Prof. E. Tremblay for his
continuous and invaluable guide in approaching and
understanding plant-insect interactions. The authors also
thank the anonymous referees for their useful comments
and suggestions.
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