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Aphid-plant interactions: A review

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DOI: 10.1080/17429140802567173

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

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
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(such as ladybird predators and parasitic wasps),

causing further damage to crops. Nonetheless, honey-
Figure 1. Schematic representation of a feeding aphid. e: dew is also used by natural enemies and honey bees as
epidermis; hd: honeydew droplet; l: labium, not participat-
food (Hogervorst et al. 2007).
ing to the piercing activity (brown); p: parenchyma; sb:
Most of the aphid populations that are found on
stylet bundle (orange); se: sieve elements (blue); ss: stylet
sheaths (black); st: stylet tip. plants during spring and summer are constituted by
females that reproduce by thelytokous parthenogen-
enzymes. This feeding habit produces but little esis associated to viviparity. Each mature female
mechanical damage if compared to that of chewing generates other females, and, in a matrioska-style
insects (such as caterpillars), which is hardly per- organization, the newly laid nymphs already nest
ceived by the attacked plant. Indeed, we observe that within them developing embryos, hosting on their
the expected plant response to sieve tubes puncturing, turn the developing embryos of the following genera-
leading to the occlusion of the wound, does not tion (telescoping generations). This type of reproduc-
happen, because of the injected salivary proteins that tion does not need any male intervention. This means
interact with calcium of plant tissues (Will et al. that once a single aphid has reached a proper host
2007). Therefore, plant reaction to invading aphids plant, it can generate a new population constituted by
takes much more time than does plant reaction to a clonal individuals in a few days. Among these mainly
chewing insect. However, with respect to chewing apterous females, winged morphs may appear as a
insects, the aphid feeding habit is more precise and response to crowding or to the complete exploitation
selective, allowing them to avoid allelochemicals and of the host plant, and still are parthenogenic,
indigestible compounds that are more abundant in thelytokous and viviparous. The specific task of these
other plant tissues (Schoonhoven et al. 2007). winged forms is the migration towards a new unin-
The selection/identification of a proper host plant fested plant. In colder climates, aphids present a
is achieved by subsequent introductions of the stylets unique biological feature, as they are able to alternate
(probes) until the composition of the sap is analyzed/ parthenogenesis and biparental reproduction: at the
recognized, therefore stylet tracks originated from end of the summer, sexual morphs appear, and the
probing behaviour can also be found on non-host female, after mating, produces a single overwintering
plants. The feeding behavior of aphids is analyzed in egg, characterized by cold hardiness. The presence of
detail by the use of EPG (electrical penetration a biparental generation once a year means that aphid
graph), a technique proposed by McLean and Kinsey populations take advantage of both the benefits of
(1964) and developed by other researchers (Tjallingii parthenogenesis (very convenient to exploit short-
1988, 2006), which allows the monitoring of stylet lived hosts), and those of the genetic recombination.
insertion, salivation and sap ingestion. Often, the life cycle occurs between different species
Plant phloem transports the photosynthate; there- of host plants, with a winter host (usually a tree or a
fore, it constitutes a feeding site that theoretically is shrub) and a spring-summer host that can be
very convenient. However, plant sap is an unbalanced 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,
whether they are simple or glandular, their density
can heavily affect the success of aphid attack (Musetti
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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 gene mediated resistance’, a type of molecular sur-
insects is a common feature in the plant world and veillance system that allows certain genotypes of
many plant families exhibit a wide battery of chemical plants to recognize and deter pests that can overcome
defences that can be either constitutive and/or non-host resistance. Interestingly, it confers resis-
induced by insect attack (Figure 2b). Within agricul- tance also towards psyllids and whiteflies (Nombela
tural plants key examples are constituted by the et al. 2003; Casteel et al. 2006), but not in the sister
families Brassicaceae and Solanaceae. plant Solanum melongena L. (eggplant) (Goggin et al.
The tissues of Brassicaceae are rich in sulphur 2006). However, as mentioned for highly toxic
derived compounds (glucosynolates) that have de- compounds, this type of resistance exerts a high
fended them from insects until aphids and moths ecological pressure on target species and for this
evolved species able to overcome this kind of reason aphid populations have ‘evolved’ a counter
defences. Today, only few insect species are specia- resistance to the Mi 1.2 (Goggin et al. 2001).
lized on Brassicaceae, e.g., the cabbage aphid Brevy- So far, other genes have been associated with
coryne brassicae L. and the cabbage whites Pieris aphid resistance. For example the Vat resistance gene
brassicae L. and P. rapae L., and compounds that are (monogenic, dominant) in melon governs both an
toxic to generalist plant feeders are used by these antixenotic reaction to the melon aphid Aphis gossy-
specialized insects as cues for the identification of pii Glover and a resistance to non-persistent virus
their host plants and for their development. More- transmission, restricted to this vector species (Chen et
over, the production of such compounds is increased al. 1997). A single dominant gene named Rag1 is
following insect infestations, with a cascade effect on responsible for the soybean resistance to the aphid
the interactions with their specific antagonists (Gols Aphis glycines Matsumura, which is an important
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et al. 2008). pest of soybean in North America (Li et al. 2007).

Similarly, tomato and potato are rich in glycosidic Similarly, in the model plant Medicago truncatula
alkaloids (tomatine, solanine) that protect them from Gaertner, aphid resistance segregates as a single
most insects, bacteria and fungi, even though some of dominant gene, AKR, named from the bluegreen
them evolved to overcome this type of defence, as is aphid Acyrthosiphon kondoi Shinji and Kondo (Klin-
the case of the oligophagous aphid species Macro- gler et al. 2005). The molecular bases of plant
resistance to aphids have been reviewed by Smith
siphum euphorbiae (Thomas) and the generalist My-
and Boyko (2007).
zus persicae. Nicotiana spp., which belong to the same
plant family as tomato, produce a well-known
insecticidal compound, nicotine, particularly active Top-down interactions: plant response to aphid attack
towards aphids, that is skipped by feeding aphids
Much more complex are the top-down interactions
because it is translocated in the xylem. that occur when aphids develop on a suitable host
Once extracted from plants, several plant second- plant. A first, major separation can be made between
ary metabolites can act as insecticides, and indeed aphid attack that is or is not associated with virus
pesticide industry has ‘copied’ from plant compounds transmission.
as leads for new products. Recently, essential oils of Plant response to aphid attack not associated with
the aromatic plants of the families Lamiaceae, the transmission of viruses is extremely variable and
Verbenaceae and Apiaceae have shown aphicide can be associated with a wide degree of symptoms
activity (Digilio et al. 2008). (Miles 1999).
It is interesting to note that the more toxic a In favorable conditions (spring/summer), aphid
compound is, the more ecological pressure is put on populations are usually extremely abundant, and can
insect populations. It is not surprising that aphids lead to the complete exploitation of herbaceous hosts.
have been able to overcome these types of plant However, in some cases large populations can de-
defences because of their complex and effective velop without evident symptoms, as it happens for
reproductive system that includes a genetical varia- Macrosiphum euphorbiae on tomato plants (Guerrieri
bility confined to the winter generation and a massive 2001). More frequently, plant response collocates in
clonal reproduction in the remaining part of the year. between the above mentioned extremes, and is
Once a single aphid develops on a resistant plant, its associated to the subtraction of plant nutrients,
progeny will eagerly develop into a resistant popula- accompanied by a progressive decline of the plant,
tion. Techniques to measure resistance, both in the with unpaired growth and enhanced susceptibility to
field and in the laboratory, are illustrated by Smith the attacks of other insects/pathogens. Examples of
(2005). this type of response to aphid attack can be observed
The cloning of the gene Mi-1.2, which confers following infestation by generalist aphids, e.g., Aphis
resistance to tomato towards the root nematode fabae (Scopoli), but also by aphids well adapted to
Meloidogyne incognita (Kofoid & White) and the their host, such as specialized Macrosiphum rosae (L.)
aphid M. euphorbiae, has been a milestone in plant (Miles 1989).
resistance to aphids (Kaloshian et al. 1997; Rossi Nonetheless, the injection of aphid saliva can be
et al. 1998; Vos et al. 1998). This gene follows the ‘R extremely toxic, leading to localized chlorosis near
 Journal of Plant Interactions 227

the feeding site and around the stylet tracks, caused ever, there was no significant difference in the amino
by chloroplast disruption (Miles 1989), and to acid composition (Koyama et al. 2004). Gall forma-
localized tissue damage, as induced by Dysaphis tion is also considered as an ecological adaptation
plantaginea (Passerini) on apple fruits. Growth dis- that guarantees favorable microclimatic conditions to
tortions are common on citrus leaves attacked by the aphid, and it may as well protect them from
Aphis spiraecola Patch, and leaves of peach trees can natural enemies and insecticides. There is a great deal
be curled into a cigar by Myzus varians Davidson. of specialization, biological complexity and even
Systemic effects caused by the feeding of Acyrthosi- variation in the interaction between host plant and
phon pisum (Harris) and Therioaphis trifolii (Monell) a gall-forming aphid (Wool 2004).
are often recognized on alfalfa. Regardless of the types of direct damage, aphids
The injection of aphid saliva can even alter the produce a huge quantity of honeydew whose crystals
hormonal balance of the plant, leading to the accumulate on leaves surface. During sunny days,
formation of galls or tumours (Figure 3). However, these crystals act as a magnifying lens burning the
apart from some substances isolated from the gall plant tissues. More commonly, on honeydew strati-
induced by Colopha sp. that are responsible for cell fies a black layer of saprophytic fungi that blocks the
hypertrophy, no cecidogenic compound has, so far, stomata causing a fall of the leaves and impairs
been identified in aphid saliva that can artificially photosynthesis. In many cases these indirect damages
induce gall formation in the attacked plant (Otha are by far worse than the simple subtraction of plant
et al. 2000). sap.
The nutrition hypothesis for the adaptive signifi- A completely different situation occurs when
aphids transmit phytopathogenic viruses. There are
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cance of insect gall formation postulates that galls

accumulate higher concentrations of nutritive com- many theories about the association between aphids
pounds than uninfested plant tissue, resulting in a and viruses, even though many researchers consider it
higher performance of the gall former. This has been a symbiosis with mutual benefits. From the aphid
demonstrated in the plant Sorbus commixta Hedl, perspective, most virus-infected plants assume a
yellowish coloration that is extremely attractive to
where the amount of amino acids exuding from cut
the aphid winged morphs. Moreover, in virus-in-
galled leaves induced by Rhopalosiphum insertum
fected plants, the titre of free amino acids in the sap is
(Walker) was five-fold that in ungalled leaves; how-
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
Figure 3. Plant response to gall-forming aphids. (a) Pem- food acceptance by M. persicae on potato, but only at
phigus spyrothecae. (b) Pemphigus immunis. (c) Pemphigus the feeding site and not systemically (Dugravot et al.
vesicarius (Photo: B Espinosa). 2007).
 228 E. Guerrieri and M.C. Digilio

In some cases, species belonging to the same genus plant volatile emissions that account for this increase
are able to share the same host plant by developing at of attractiveness are systemic, thus occurring also in
different feeding sites. For example, different species the undamaged parts of the plant (Guerrieri et al.
of Pemphigus spp. attack different tissues of poplar 1999). Moreover, these changes are produced only
tree (leaf vein, leaf petiole, leaf blade, branch), each after a prolonged feeding activity by a consistent
producing a specific type of gall (Wool 2004) (Figure aphid population (Guerrieri et al. 2002). The ex-
3). tended time needed by the plant to ‘realize’ the
More recently other types of plant responses have presence of an aphid population is strictly linked to
been characterized. In detail it has been demonstrated the minimum mechanical damage that is caused by
that both biotic and abiotic stresses alter the compo- stylets penetration if compared, for example, to the
sition of the volatile compounds that a plant releases. destruction of plant tissues performed by chewing
Aphids are no exception and it has been shown that caterpillars.
this change in volatile profiles can regulate the Aphids (and phloem feeders in general) are
interactions between aphids and their natural enemies perceived by the plant as they were intermediate
(see below). between pathogens and herbivores (Kaloshian and
Walling 2005), thus eliciting a metabolic response
Aphids in a multitrophic context that involves both the salicylic and the jasmonic
acid pathways (Du et al. 1998; Stout et al. 1998,
Aphids appear in many food chains (Kennedy 2003). 1999; Sasso et al. 2007; Smith and Boyko 2007;
However, it is interesting to note that a key role in Girling et al. 2008). These two main metabolic
the regulation of aphid populations is played by pathways are known to be mainly activated in
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other insects (Van Veen et al. 2008), especially those

response to phytopathogens and to herbivore
feeding exclusively on aphid species, i.e., predators,
chewers (and to mechanical damage), respectively
such as ladybirds (e.g., Coccinella septempunctata L.
(see Agrawal et al. 1999). More recently it has been
and Adalia bipunctata L.) and midges (Aphidoletes
reported that plant response to aphids is completed
aphidimyza
Rondani-) and parasitoids (e.g., Hyme-
by the activation of the other known minor path-
noptera Braconidae Aphidiinae: Aphidius spp. Praon
ways of ethylene, abscissic acid, giberellic acid,
spp. Tryoxis spp.; Diaeretiella spp.; Hymenoptera
nitric oxide and auxine (see Smith and Boyko
Chalcidoidea Aphelinidae: Aphelinus spp.). The
2007 and references therein).
complex of insects acting as aphid antagonists is
In many plant-aphid systems, among the identi-
completed by generic predators such as myrids
fied compounds whose release is increased by aphid
(Hemiptera), chrysopids (Neuroptera) and syrphids
infestation, methyl-salycilate appears to be a key one.
(Diptera). Not always aphid antagonists have been
This compound can be rightly considered the very
perceived as tremendously efficient control instru-
ments, because their action may be delayed in end of the salicylic acid pathway and has been shown
respect to the build-up of aphid colonies (aphid to be attractive towards both aphid parasitoids (Sasso
populations start to develop in spring), but, when et al. 2007) and predators (James 2003; Zhu and Park
their action has started, the result is a crash of aphid 2007). However, the volatile blend released by aphid
colonies that can be observed especially in organic infested plants is completed by several terpenes
crops (Tremblay 1973). deriving from the jasmonic acid pathway that is
During the last 15 years, the key role of the plant regulated by the COI gene (Girling et al. 2008), and
in the recruitment of aphid antagonists has been by a series of alcohols known to be linked to general
recorded in a number of tritrophic systems (Guerrieri biotic stresses (Sasso et al. 2007).
et al. 1993; Reed et al. 1995; Han and Chen 2002; The deep intimacy of aphid plant interactions is
Girling et al. 2006; Blande et al. 2007; López Pérez et sometimes demonstrated by the specificity of plant
al. 2007; Pareja et al. 2007; Sasso et al. 2007). With volatiles released in response to different aphid
only one exception (López Pérez et al. 2007), in all species. For example, the changes in volatile emis-
these studies it has been shown that the volatile sions released by broad bean plants infested by the
compounds released by an aphid infested plant black aphid Aphis fabae do not affect the flight
selectively attract aphid predators and parasitoids behavior of A. ervi, as conversely do those induced
towards their preys/hosts. This feature is referred to by the green aphid Acyrthosiphon pisum (Du et al.
as indirect defence, to stress the fact that the plant 1996, 1998). It is important to note that A. fabae is
defends itself from herbivore insects through the not a host for A. ervi and thus the parasitoid wasp is
intervention of their specific natural enemies (Dicke able to detect the subtle differences in the ‘odors’
et al. 2003). induced by these two aphid species feeding on the
For example, broad bean plants infested by the same plant and to forage only on those infested by its
pea aphid Acyrthosiphon pisum are six times more natural host A. pisum. In contrast, no significant
attractive than uninfested plants towards the para- preference in orientation behavior by the aphid
sitoid Aphidius ervi Haliday (Guerrieri et al. 1993). In parasitoid Diaeretiella rapae (McIntosh) was ob-
this system, it has been shown that the changes in served in response to the volatile chemicals produced
 Journal of Plant Interactions 229

by turnip (Brassica rapa L. var rapifera) exposed to city effect of plant-arbuscular mycorrhizal fungus
either Lipaphis erysimi (Kaltenbach) (a specialist on associations in terms of the final output of these
Brassicaceae) or Myzus persicae (a true generalist) complex interactions. On a completely different
(Blande et al. 2008). There are at least two main system, including different plant, fungal symbiont
differences that can be noted in respect to the broad and aphid species, mycorrhizal symbiosis seemed to
bean case. First of all, both L. erysimi and M. have a positive effect on the fitness of a generalist
persicae can be attacked by D. rapae and thus there aphid (Gange et al. 1999).
is no advantage for the parasitoid in discriminating Although contrasting, these findings stressed how
between volatiles induced by the two aphid species. belowground interactions could shape the above-
Moreover, regardless the herbivore species involved, ground insect pest populations through plant media-
the volatile profile of infested Brassica is dominated tion (Guerrieri and Digilio 2008).
by isothiocyanates that are highly attractive towards
D. rapae. Current issues in aphid-plant interactions and
The possibility of using plant attractiveness to conclusions
enhance the natural control of aphid pests has
prompted a series of studies aiming at indicating There is probably one main issue that can be
possible ways of eliciting it in uninfested plants. considered pivotal in aphid-plant interactions: plant
Aboveground, exogenous applications of a com- resistance. As mentioned above, aphids can be serious
pound derived from jasmonic acid, namely (Z)- pests of agricultural crops, especially when they are
jasmone, resulted in a significant change in the able to transmit phytopathogenic viruses. In these
emission of volatile compounds from uninfested cases there is virtually no tolerance to their attack,
Downloaded By: [Maffei, Massimo] At: 07:31 25 November 2008

broad bean plants, making them as attractive and chemical treatments are required to save the
towards A. ervi as the plants infested by A. pisum yield.
We are just starting to understand the molecular
(Birkett et al. 2000). More recently, these findings
basis of the varied plant response to aphid attack, and
were confirmed for the model plant Arabidopsis
resistance sources are actively searched in order to
thaliana (L.), with differences noted in the behavior
introduce resistance traits in crops (Goggin 2007).
of a specialist aphid versus a generalist one on
Now tomato plants commonly cultivated are Mi-
induced plants (Bruce et al. 2008). However, a
1.2, i.e., resistant to root nematode Meloidogyne
deterrent effect towards aphids was also noted
incognita and to aphid Macrosiphum euphorbiae
following treatment with (Z)-jasmone (Birkett et al.
(Kaloshian et al. 1995, 1998; Rossi et al. 1998).
2000; Pickett et al. 2007). Belowground, plant
However, this feature can be even enhanced by
responses are regulated by a myriad of interactions
applications of foliar inducers such as the jasmonic
that include the soil microfauna as well as neighbor-
acid and the salicylic acid analog, benzothiadiazole
ing plants, either conspecific or not, that can affect (BTH) (Cooper et al. 2004).
indirect and direct defences. For example, root A decade has passed since this discovery, and just
exudates from A. pisum-infested plants were able recently there are a few indications of genes that can
to induce a dramatic increase of attractiveness be responsible for aphid resistance. A great help in
towards aphid parasitoids in a nearby uninfested this topic has been given by the use of the model
broad bean plant (Guerrieri et al. 2002). Also weeds plants Arabidopsis thaliana, whose genome has been
can play a role in the aphid-plant interaction, as completely sequenced, and Medicago truncatula. In
demonstrated for barley plants. Indeed, following the characterization of aphid
plant interactions it is
exposure to root allelochemicals from the aggressive of extreme help the use of both mutants, with known
weed couch-grass, Agropyron repens (L.), barley genes overexpressed or silenced (Girling et al. 2008),
plants were less accepted by the bird cherry-oat and of near-isogenic lines (NILs) (Gao et al. 2007).
aphid, Rhopalosiphum padi (L.), and became repel- This is true both for direct resistance, which directly
lent for the aphids in olfactometer bioassay (Glin- hampers aphid development and reproduction, and
wood et al. 2003). for indirect defence, which is based on the production
Much more complex is the response of a plant to of volatile compounds attractive towards the natural
aphid attack in presence of soil symbionts. For enemies of aphids. For species like tomato, these
example, the presence of an arbuscular mycorrhizal features can be also investigated by using wild species
fungus, Glomus mossae (Nicol and Gerd), is able to that are highly resistant to phloem feeders, such as
induce an increase on both direct and indirect Solanum pennellii and Solanum habrochaites Knapp
defences in tomato plants (Guerrieri et al. 2004). In and Spooner, whose entire genome has been intro-
other words, a drastic reduction in the reproductive gressed into a cultivated variety leading to a series of
rate of Macrosiphum euphorbiae and a significant introgression lines (ILs) that are available for biolo-
increase of attractiveness towards the parasitoid A. gical tests.
ervi has been recorded on mycorrhizal tomato plants In the absence of viral transmission, the augmen-
in respect to non mycorrhizal ones (Guerrieri et al. tation of the attractiveness of cultivated plants can be
2004). However, there seems to be a species-specifi- considered as a profitable strategy, inducing no
 230 E. Guerrieri and M.C. Digilio

ecological pressure on aphid populations being linked Bin F. 1979. Influenza dei peli glandolari sugli insetti in
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as an insect semiochemical and in plant defence.
modern techniques can be of great help in reducing
PNAS. 97:9329
9334.
the time needed to transfer the genes involved in
Blande JD, Pickett JA, Poppy GM. 2007. A comparison of
direct and indirect defence against aphids, in respect
semiochemically mediated interactions involving spe-
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cally modified plants can also integrate the knowl- braconid parasitoid Diaeretiella rapae. J Chem Ecol.
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The authors are deeply grateful to Prof. E. Tremblay for his critical review on the role of colours in host finding.
continuous and invaluable guide in approaching and Arthropod-Plant Interact. 1:3
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