Journal of Experimental Botany, Vol. 57, No. 4, pp. 755–766, 2006
doi:10.1093/jxb/erj135 Advance Access publication 22 February, 2006
FOCUS PAPER
Transcriptomics and functional genomics of plant defence
induction by phloem-feeding insects
Gary A. Thompson1,* and Fiona L. Goggin2
1
Department of Applied Science, University of Arkansas at Little Rock, 2801 South University Ave, Little Rock,
AR 72204-1099, USA
2
Department of Entomology, University of Arkansas, 320 Agriculture Building, Fayetteville, AR 72701, USA
Abstract
Introduction
The relationship between phloem-feeding insects (PFIs)
and plants offers an intriguing example of a highly
specialized biotic interaction. These insects have
evolved to survive on a nutritionally imbalanced diet of
phloem sap, and to minimize wound responses in their
host plants. As a consequence, plant perception of and
responses to PFIs differ from plant interactions with
other insect-feeding guilds. Transcriptome-wide analyses of gene expression are currently being applied to
characterize plant responses to PFIs in crop plants with
race-specific innate resistance, as well as in compatible
interactions with susceptible hosts. Recent studies indicate that PFIs induce transcriptional reprogramming
in their host plants, and that plant responses to PFIs
appear to be quantitatively and qualitatively different
from responses to other insects or pathogens. Transcript profiling studies also suggest that PFIs induce
cell wall modifications, reduce photosynthetic activity,
manipulate source–sink relations, and modify secondary metabolism in their hosts, and many of these
responses appear to occur within the phloem tissue.
Plant responses to these insects appear to be regulated
in part by the salicylate, jasmonate, and ethylene signalling pathways. As additional transcript profiling
data become available, forward and reverse genetic approaches will be necessary to determine which changes
in gene expression influence resistance or susceptibility to PFIs.
The majority of insects in the suborder Homoptera, such as
aphids, whiteflies, psyllids, and planthoppers, are specialized to feed on phloem sap. Phloem-feeding insects (PFIs)
are the most prevalent vectors of plant viruses and also
damage crops by depleting photoassimilates, manipulating
growth and nutrient partitioning, and, in some cases,
injecting toxins into the plant (Nault, 1997; Madhusudhan
and Miles, 1998; Macedo et al., 2003; Girousse et al.,
2005). Because of the impact of PFIs on agriculture, it is
important to identify the factors that regulate plant resistance or susceptibility to these insects.
The complexity of plant–insect interactions makes it
difficult to determine which anatomical features, metabolites, and signalling pathways effectively limit PFI infestation. The field of genomics provides powerful tools to
investigate these critical factors. Transcript profiling techniques allow the simultaneous examination of thousands
of genes, and can be utilized to study changes in gene
expression that are transcriptionally regulated. Microarray
analysis is among the most common profiling tools, but
requires the previous identification of a set of relevant
transcripts. Other techniques such as cDNA amplified
fragment length polymorphisms (cDNA-AFLPs) and suppression subtractive hybridization (SSH) are useful to
identify previously unknown transcripts that are differentially regulated among treatment groups. These approaches
can readily be combined to identify plant transcript profiles
that correlate with PFI resistance or symptom development.
Furthermore, genome-wide transcript analysis is currently
being applied to identify putative avirulence genes, detoxification mechanisms, or virulence factors in PFIs.
Beyond transcript profiling, genomics also facilitates the
functional analysis of genes implicated in resistance or
Key words: Aphid, gene expression, induced resistance, innate
resistance, microarray, phloem, planthopper, sieve element,
whitefly.
* To whom correspondence should be addressed. E-mail: gathompson@ualr.edu
ª The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For Permissions, please e-mail: journals.permissions@oxfordjournals.org
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Received 24 August 2005; Accepted 25 January 2006
756 Thompson and Goggin
susceptibility. As signalling cascades and metabolic pathways are elucidated in model systems and crop plants,
key regulatory genes can be targeted for silencing or overexpression to study the role of these pathways in plant–
insect interactions.
To date, the majority of molecular and genomic studies
on plant interactions with PFIs are limited to the analysis of
plant gene expression in response to infestation. Therefore,
this review will focus on plant transcriptomics, and will
examine the effects of PFI infestation on known defensive
pathways, oxidative stress responses, cell wall composition,
and primary and secondary metabolism.
Herbivore damage is limited by a wide variety of constitutive
or induced plant defences. Constitutive traits such as
trichomes or preformed chemical defences are expressed
prior to insect damage and frequently have deterrent effects
on insect settling or feeding behaviours. Plants can display
phenotypic plasticity even in preformed defences; trichome
densities, for example, may increase in response to prior
herbivory (Traw and Bergelson, 2003). Other forms of insect
resistance depend upon far more rapid defence responses
that are expressed only under herbivore pressure. In the case
of race-specific innate resistance, plants that carry a particular resistance gene (R gene) recognize a corresponding
avirulence gene product in the pest, resulting in an incompatible interaction (Flor, 1971). A rapid, local defence
response occurs at the site of infection and blocks or
dramatically reduces the initial establishment of the pest.
The proximate mechanisms of race-specific insect resistance
are not yet well understood, but possible defences include
the generation of reactive oxygen species, a hypersensitive
response at the feeding site, or the rapid generation of
antibiotic compounds such as pathogenesis-related (PR)
proteins (Kaloshian, 2004). Frequently, R-gene-mediated
aphid resistance is characterized by reduced sap ingestion
after the aphid contacts the phloem, suggesting that resistance might also involve phloem-limited feeding
deterrents or phloem-sealing mechanisms (Caillaud and
Niemeyer, 1996; Klingler et al., 1998; Kaloshian et al.,
2000). Local disruption of assimilate transport triggered by
PFI-induced intercellular calcium fluxes could limit the
insect’s food supply. Elegant experiments examining aphidfeeding behaviours in the sieve elements of Vicia faba
suggest that calcium-mediated phloem sealing is modulated
by calcium chelating components within aphid saliva, and
this interaction could play an important role in determining
susceptibility or resistance (Will and van Bel, 2006).
The majority of published studies have focused on
transcript profiles of compatible interactions in plant
species for which no genetic variation in resistance levels
have been identified (Table 1). These studies seek to
identify highly conserved, multigenic, induced defences
Plant perception of PFIs
PFIs minimize wounding and plant wound responses
Plant responses to herbivore attack can be correlated with
the mode of feeding and the amount of tissue damage
occurring at the feeding site (Walling, 2000). Chewing
insects such as caterpillars cause extensive cellular disruption, which plays an important role in plant perception of
these herbivores. Transcript profiles induced by caterpillar
feeding show significant overlap with profiles involved in
wound responses (Reymond et al., 2000). By contrast, most
PFIs probe plant tissue intercellularly to establish feeding
sites in the phloem sieve elements that can be maintained
for hours or even weeks (reviewed in Tjallingii, 2006). This
mode of feeding minimizes wounding and limits the local
induction of defence responses to a minimal number of
cells and tissue types. Probing does, however, result in cell
wall disturbance, disruption of plasma membranes, and
penetration of epidermal, mesophyll, and parenchyma cells
(Pollard, 1973; Tjallingii and Hogen Esch, 1993). As a
result, limited local induction of proteinase inhibitors and
other wound-responsive transcripts have been observed in
response to PFI infestation (Martinez de Ilarduya et al.,
2003; Zhu-Salzman et al., 2004; Park et al., 2005). The
degree of injury that occurs during probing varies considerably among PFI species.
PFI saliva may regulate plant–insect interactions
While wounding plays a major role in plant response to
chewing insects, insect oral secretions are also important
in modulating plant transcript profiles (Korth and Dixon,
1997; Lawrence and Novak, 2004). Volicitin and other
fatty acid conjugates in caterpillar oral secretions trigger the
release of plant volatiles that attract the natural enemies
of insect herbivores (Alborn et al., 1997). Conversely,
caterpillars also produce glucose oxidase, that is postulated
to benefit herbivores by suppressing plant defence responses (Eichenseer et al., 1999; Musser et al., 2002).
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Determinants of plant interactions with PFIs
that limit the severity of insect infestations, or mechanisms
of tolerance that allow plants to sustain infestation while
limiting symptom development. Plant traits that have been
implicated in broad-spectrum induced resistance (IR) include cell wall modifications, proteins or secondary
metabolites that have antixenotic or antibiotic properties,
and plant volatiles that repel PFIs or attract their natural
enemies (Kaloshian and Walling, 2005). In addition to
broad-spectrum defences, many of the changes in gene
expression observed in compatible interactions are involved in symptom development, such as chlorophyll
loss. The primary challenge in plant transcriptomics is to
discriminate among the complex array of changes that
are induced by PFIs, to determine which of these changes
have adaptive value to plants.
Transcriptional induction of plant defences by phloem-feeding insects 757
Table 1. Transcript profiling studies of plant responses to phloem-feeding insects
Insect
Number of Durationb Analysis
infestationsa
Array type
Reference
Arabidopsis thaliana (S)c
Green peach aphid
(Myzus persicae)
10
72–96 h
Array
Selected ESTs (105)
Moran et al., 2002
Arabidopsis thaliana (S)
Green peach aphid
(Myzus persicae)
40
72 h
Array, QPCR,
RNA blot
Arabidopsis
GeneChip (23 750)
De Vos et al., 2005
Sorghum (S)
(Sorghum bicolor)
Greenbug aphid
20
(Schizaphis graminum)
Sorghum (S/R)
(Sorghum bicolor)
Greenbug aphid
30
(Schizaphis graminum)
Native tobacco (S)
(Nicotiana attenuata)
Myzus nicotianae
Native tobacco (S)
(Nicotiana attenuata)
Myzus nicotianae
Rice (S/R)
(Oryza sativa)
Array and RNA blot Subtracted cDNA
(672)
Zhu-Salzman et al.,
2004
72 h
Array and RNA blot Subtracted cDNA
(3508)
Park et al., 2005
5
72 h
Array
Selected Oligo (789)
Heidel and Baldwin,
2004
4
48 h
Array
Selected cDNA (240) Voelckel et al., 2004
Brown plant hopper
(Nilaparvata lugens)
10
72 h
Array and RNA blot Selected cDNA (108) Zhang et al., 2004
Rice (S)
(Oryza minuta)
Brown plant hopper
(Nilaparvata lugens)
10
Celery (S)
(Apium graveolens)
Green peach aphid
(Myzus persicae)
10–20
Apple (S/R)
(Malus domestica)
Rosy apple aphid
20
(Dysaphis plantaginae)
Tomato (S)
Silverleaf whitefly
(Lycopersicon esculentum) (Bemisia argentifolii)
25
6–48 h
6–72 h
Array and RNA blot Subtracted cDNA
(960)
Cho et al., 2005
72–168 h Array and RNA blot Subtracted cDNA
ESTs (1278)
Divol et al., 2005
72 h
cDNA-AFLP
and RNA blot
Qubbaj et al., 2005
25 d
Array
CGEP
tomato arrays
McKenzie et al.,
2005
a
Number of insects at the initial infestation.
Duration of the infestation.
c
S, susceptible; R, resistant.
b
Given the significance of oral secretions in plant interactions with chewing insects, it is highly probable that
insect secretions also mediate plant interactions with PFIs.
PFI salivas contain complex mixtures of lipoproteins,
phospholipids, and carbohydrates, as well as numerous
enzymes with proteolytic, hydrolytic, oxidative, or cell walldegrading activities (Miles, 1999; Cherqui and Tjallingii,
2000; Tjallingii, 2006). In compatible interactions, these
factors probably aid in stylet penetration and could detoxify
defensive compounds in the host plant (Jiang, 1996; Miles,
1999). In some cases, transport of salivary components
within the plant contributes to the development of symptoms such as veinal chlorosis (Madhusudhan and Miles,
1998). In incompatible interactions, PFI oral secretions are
also a potential source of avirulence (avr) factors. To date,
no avr genes have been cloned in an insect; however, N
Lapitan and coworkers (personal communication) have
identified a protein fraction isolated from Russian wheat
aphids (RWA; Diuraphis noxia) that could have a key role
in determining plant compatibility. When injected into
susceptible wheat genotypes, this protein fraction induced
the leaf-rolling symptom typical of RWA feeding in
compatible interactions. Injecting the protein fraction into
RWA-resistant genotypes did not induce leaf rolling, but
increased the expression of defensive peroxidases and
catalases compared with the RWA-susceptible genotypes.
In the future, construction of cDNA libraries derived from
insect salivary glands should assist in identifying other
determinants of virulence in PFIs. High-throughput transient expression systems can also be used to express aphid
gene products in plant tissue to test the effects of putative
a/virulence factors on plant defence and symptom expression. This approach has proven effective in the study of
bacterial effector proteins (Kamoun et al., 2003; Van der
Hoorn et al., 2000).
Transcriptional reprogramming by PFIs
Transcriptomics reveals a high degree of overlap
between plant transcript profiles in compatible and
incompatible interactions with PFIs
Whether elicited by mechanical damage or oral secretions,
herbivores induce numerous changes in their host plants,
many of which are transcriptionally regulated. Relatively
few studies, however, have examined plant transcript
profiles in incompatible interactions with PFIs (Zhang
et al., 2004; Park et al., 2005; Qubbaj et al., 2005). Studies
that compare insect-responsive gene expression in incompatible (resistant) and compatible (susceptible) interactions
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Plant
758 Thompson and Goggin
The experimental design of transcriptomics
experiments may influence their outcome
The widely accepted MIAME (Minimum Information
About a Microarray Experiment) guidelines dictate how
the experimental methods for microarray experiments
should be documented for publication (Brazma et al.,
2001). When it comes to setting standards for the methods
themselves, however, researchers have yet to reach a consensus on many basic issues, such as minimum requirements for replication or preferred statistical analyses.
Researchers who study plant interactions with PFIs must
also decide what bioassay design for tissue collection is
best-suited to their particular biological system. As mentioned earlier, the time scale over which transcript profiles
are monitored is critical, and should be chosen based upon
observations of the plant–insect interaction. Other aspects
of experimental design that could influence the outcome
of genomic studies include the developmental stages of
the plants and insects and the inoculum level used. For
example, Van de Ven et al. (2000) demonstrated that
whitefly larvae induced different transcriptional responses
than adults.
The outcome of transcript profiling studies will also vary
depending upon the tissue types examined. PFIs have both
local and systemic effects on plant gene expression, and
these effects may differ among cell types. Because PFIs
have an intimate and sustained interaction with the phloem
sieve elements and inject watery saliva into the phloem,
many important plant responses to PFIs may be localized to
the vascular tissue. This tissue makes up a small proportion
of the leaf, however, and whole leaf transcriptional assays
could miss rare transcripts that are expressed within sieve
elements. Divol and co-workers (2005) have exploited the
unique anatomy of celery petioles to examine transcriptional changes that occur specifically in the phloem tissue in
a compatible interaction with green peach aphid. This study
identified 126 genes that were systemically induced by
aphid feeding, including transcripts involved in oxidative
stress, signalling, cell wall modification, water transport,
metal homeostasis, vitamin biosynthesis, carbon assimilation, and nitrogen and carbon mobilization. Conspicuously
absent from this analysis was the induction of high levels of
pathogenesis-related (PR) proteins that are characteristic of
the local response to aphid feeding in whole leaf tissues.
This study illustrates that localizing gene expression is
critical to understanding the role of specific genes involved
in the plant–PFI interaction.
The nature of the gene sets used in microarray experiments, as well as the manner in which the experiments are
replicated and analysed can also influence the conclusions
that are drawn from the data. For example, the current
literature presents conflicting views of the extent and
magnitude of PFI-induced transcriptional reprogramming
in plants. Several studies of selected stress-responsive
genes have suggested that PFIs have less impact on plant
gene expression than chewing insects (Fidansef et al.,
1999; Heidel and Baldwin, 2004; Kaloshian and Walling,
2005). By contrast, De Vos et al. (2005) identified 2181
genes (832 up-regulated and 1349 down-regulated) in an
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are designed to identify a subset of genes that are directly
related to innate resistance. Qubbaj et al. (2005) utilized
cDNA-AFLP and RNA blot analyses to investigate the
interaction between apple and the rosy apple aphid 72 h
after infestation, but identified only six transcriptional
responses that were unique to the incompatible interaction.
In resistant, but not in susceptible plants, aphid feeding upregulated expression of genes encoding a pectin acetyl
esterase, RNase L inhibitor-like protein, ADP-ribosylation
factor, vacuolar H+-ATPase subunit-like protein, and
inositol phosphatase-like protein, and down-regulated the
large-chain precursor of Rubisco. In addition, He and
coworkers utilized a 108-element selected cDNA array to
examine gene expression in resistant and susceptible rice
cultivars 72 h after infestation with the brown planthopper
(Zhang et al., 2004). In the resistant cultivar, planthopper
feeding up-regulated expression of glutamine synthase and
S-adenosylmethionine synthase 2, whereas these transcripts
were down-regulated in susceptible rice plants. A BTF3
transcription factor was also down-regulated in resistant
plants and up-regulated in the compatible interaction. Aside
from these three genes, insect-responsive transcripts identified in resistant plants showed similar expression patterns
in the susceptible cultivar. Transcriptional differences
between resistant and susceptible sorghum lines in response
to greenbug feeding are difficult to evaluate because of the
extreme damage caused by aphid feeding on susceptible
lines (Park et al., 2005). After 72 h of aphid feeding on
a susceptible sorghum line the plants were severely wilted
with widespread necrotic spots, whereas the resistant line
had only a few necrotic spots and otherwise appeared
healthy. Greenbug feeding on the resistant sorghum line for
a similar period of time resulted in differential expression
of 84 genes (72 up-regulated, 12 down-regulated), which
included 13 genes (11 up-regulated, 2 down-regulated) that
were co-regulated in the susceptible line. Potentially, innate
resistance in these systems is due to differences in the
timing and magnitude of plant defences, rather than to
qualitatively different responses. Furthermore, the initial
recognition and signalling events are likely to be rapid,
fleeting, and highly localized to the feeding site. For
example, electronic monitoring of aphid feeding behaviour
on resistant tomato and melon cultivars suggests that the
resistance response in these plants occurs within 2 h of the
onset of probing, and involves defences that are localized to
the phloem (Klingler et al., 1998; Kaloshian et al., 2000).
Future transcriptional studies should examine earlier time
points in the plant–insect interaction, and consider the
temporal and spatial components of plant responses to PFIs.
Transcriptional induction of plant defences by phloem-feeding insects 759
Influence of PFIs on known defence signalling
pathways
PFI-induced gene expression reveals mixed signals
PFI infestation has been shown to modulate salicylic acid,
jasmonic acid, and ethylene, three signalling compounds
that play key roles in regulating plant defence. Salicylic
acid (SA) is required for systemic acquired resistance
(SAR) to many viruses, bacteria, and fungi, as well as for
certain forms of race-specific disease resistance (Rairdan
and Delaney, 2002; Durrant and Dong, 2004). Jasmonic
acid (JA) and related oxylipins mediate induced resistance
to chewing insects and cell-content feeders, as well as to
certain fungal pathogens (Halitschke and Baldwin, 2004;
Pozo et al., 2004). JA and ethylene (ET) are both woundresponsive, and are required for the elicitation of systemic
induced disease resistance (ISR) by rhizobacteria (Pozo
et al., 2004). Plant transcriptional responses to pathogens
and herbivores are determined in part by the co-ordinate
regulation of the SA, JA, and ET signalling pathways that
can have both synergistic and antagonistic interactions.
ET, for example, enhances certain JA- and SA-dependent
responses, but inhibits others (Rojo et al., 2003). Numerous
studies have also demonstrated negative cross-talk between
SA and JA (Rojo et al., 2003; Felton and Korth, 2000), but
recent evidence indicates that these hormones can also
have overlapping or even synergistic effects (Schenk et al.,
2000; van Wees et al., 2000; Salzman et al., 2005). The
interaction between SA and JA varies depending upon
hormone concentration and the relative timing of induction
(Devadas et al., 2002; Thaler et al., 2002). Further studies
are needed to determine how SA, JA, and ET contribute to
the outcome of plant interactions with PFIs.
PFIs elicit the SA signalling pathway
Aphid feeding induces expression of PR genes and other
transcripts associated with SA-mediated signalling in
several plant species, including Arabidopsis, tomato,
sorghum, and Nicotiana attenuata (Moran and Thompson,
2001; Moran et al., 2002; Martinez de Ilarduya et al., 2003;
Heidel and Baldwin, 2004; Zhu-Salzman et al., 2004; De
Vos et al., 2005; Park et al., 2005). Direct quantification
has also demonstrated that aphids induce salicylate accumulation in wheat, barley, soybean, and tomato (Mohase
and van der Westhuizen, 2002; Chaman et al., 2003; Zhu
and Park, 2005; DA Navarre and FL Goggin, unpublished
data), although no changes in SA levels were detected in
aphid-infested Arabidopsis or N. attenuata (Heidel and
Baldwin, 2004; De Vos et al., 2005). In wheat, SA
induction was observed in incompatible but not compatible
interactions with the Russian wheat aphid (Mohase and van
der Westhuizen, 2002). In tomato, accumulation of the SAresponsive PR-1 transcript was stronger and more rapid in
incompatible than compatible interactions (Martinez de
Ilarduya et al., 2003). Furthermore, Kaloshian (2004) stated
the tomato plants carrying the aphid resistance gene Mi lost
resistance when transformed with NahG, a gene encoding
a bacterial enzyme that degrades SA. These results suggest that SA plays a role in certain forms of innate aphid
resistance.
The effects of SA induction on aphid performance in
compatible interactions, however, are not yet clear. Exogenous application of benzothiadiazole (BTH), a synthetic
analogue of SA, reduced aphid population growth on the
foliage of both resistant and susceptible tomato cultivars
(Cooper et al., 2004), but the range of defences induced by
BTH was recently reported to differ from those induced by
SA (Heidel and Baldwin, 2004). In Arabidopsis, analysis
of mutant lines deficient in SA-signalling suggested that
SA does not play a direct role in limiting aphid infestation
on this species (Table 2). Shah and coworkers observed
a decrease in aphid numbers on two mutant lines that
have elevated SA levels (cpr5 and ssi2) and an increase in
aphid populations on a mutant that has reduced SA accumulation (pad4); however, they attributed this variation
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Arabidopsis thaliana full-genome array that were differentially expressed in response to the green peach aphid
(Myzus persicae). The number of genes differentially
expressed in response to aphids was much greater than
observed for chewing insects (186 genes: cabbage white
butterfly larvae, Pieris rapae) or cell-content feeders (199
genes: thrips, Frankliniella occidentalis), and was comparable to the number of genes that were responsive to the
bacterial pathogen Pseudomonas syringae (2034 genes).
Potentially, the use of a whole-genome array rather than
a preselected gene set allowed the identification of a larger
set of aphid-responsive genes. However, it is also important to note that this study utilized only one biological replicate, pooled from 20 plants, and identified differentially
regulated genes on the basis of fold-changes, rather than
statistical analysis (De Vos et al., 2005). More recently, the
green peach aphid–Arabidopsis interaction was studied
using six biological replicates to probe the Arabidopsis fullgenome array, and this study found only 27 genes (2 at 2 h
and 25 at 36 h) with altered expression (J Pritchard,
personal communication). These conflicting data sets
demonstrate the importance of standardizing the experimental design in both performing and interpreting global
transcription studies.
Although relatively few published studies have examined plant transcript profiles in response to PFIs, these
studies have used a wide range of experimental systems and
methodologies (Table 1), and this limits our ability to
compare the outcome of these studies. Based on the
analysis of both compatible and incompatible interactions,
however, it is evident that PFIs influence known defensive
pathways, oxidative stress responses, and plant structure
and metabolism.
760 Thompson and Goggin
Table 2. Functional genomics of Arabidopsis–aphid interactions: jasmonic acid (JA), ethylene (ET), and salicylic acid (SA)
signalling
Mutant
Effect on signalling
Reference
Aphid species
Populationa
Stage
Reference
coi1
JA-insensitive
Ellis and Turner, 2002
Feys et al., 1994
M. persicae
B. brassicaceae
Increase (7)
Increase (10)
Increase (10)
Bolting
Rosette
Rosette
Ellis et al., 2002
Mewis et al., 2005
Mewis et al., 2005
ET-insensitive
Gamble et al., 1998
M. persicae
B. brassicaceae
No effect (10)
No effect (10)
Rosette
Rosette
Mewis et al., 2005
Mewis et al., 2005
cev1
Constitutive JA and ET
signalling
Ellis and Turner, 2001
M. persicae
Decrease (7)
Bolting
Ellis et al., 2002
hrl1
Elevated SA and
constitutive SA- and
JA-dependent responses
Devadas et al., 2002
M. persicae
B. brassicaceae
Increase (10)
No effect (10)
Rosette
Rosette
Mewis et al., 2005
Mewis et al., 2005
cpr5
Elevated SA levels and
constitutive SA-dependent
responses; increased
leaf senescence
Bowling et al., 1997
M. persicae
Decrease (2)
Not stated
Pegadaraju et al., 2005
snc1
Elevated SA levels and
constitutive SA-dependent
responses
Zhang et al., 2003
M. persicae
No effect (2)
Not stated
Pegadaraju et al., 2005
ssi2
Elevated SA levels and
constitutive SA-dependent
responses; increased
leaf senescence
Shah et al., 2001
M. persicae
Decrease (2)
Not stated
Pegadaraju et al., 2005
eds5
Reduced SA accumulation
Rogers and Ausubel, 1997
Nawrath et al., 2002
M. persicae
No effect (7)
Bolting
Moran and Thompson, 2001
eds9
Reduced SA-mediated
pathogen resistance
Rogers and Ausubel, 1997
M. persicae
No effect (7)
Bolting
Moran and Thompson, 2001
NahG
Reduced SA accumulation:
degradation by salicylate
hydroxylase
Delaney et al., 1994
M. persicae
Decrease (10)
No effect (2)
Decrease (10)
Rosette
Not stated
Rosette
Mewis et al., 2005
Pegadaraju et al., 2005
Mewis et al., 2005
Reduced SA-dependent
responses and enhanced
JA signalling
Cao et al., 1994
Spoel et al., 2003
B. brassicaceae
Decrease (10)
Inconsistent (7)
No effect (2)
Decrease (10)
Rosette
Bolting
Not stated
Rosette
Mewis et al., 2005
Moran and Thompson, 2001
Pegadaraju et al., 2005
Mewis et al., 2005
npr1
B. brassicaceae
M. persicae
pad4-1
Reduced SA accumulation;
delayed leaf senescence
Glazebrook et al., 1997
M. persicae
Increase (2)
Not stated
Pegadaraju et al., 2005
sid2-2
Reduced SA synthesis
Wildermuth et al., 2001
M. persicae
No effect (2)
Not stated
Pegadaraju et al., 2005
a
Population development compared with the wild type (number of days population development was monitored).
in aphid performance to differences in leaf senescence,
rather than to direct effects of SA-dependent defences
(Pegadaraju et al., 2005). Aphid resistance was maintained
in the ssi2-NahG double mutant despite its dramatically
reduced SA levels, and several other mutations that affected
SA signalling but not senescence (snc1, npr1, sid2-2) failed
to influence aphid populations (Pegadaraju et al., 2005).
Similarly, Moran and Thompson (2001) observed no
difference in green peach aphid reproduction between
wild-type plants and the eds5 and eds9 mutants, which
are compromised in SA signalling. Furthermore, the results
of Schultz and coworkers suggest that certain mutations
in SA signalling can enhance basal aphid resistance in
Arabidopsis (Mewis et al., 2005). They observed reduced
aphid performance on npr1 and NahG mutants compared
with the wild-type plants, which suggests that SA accumulation and signalling may enhance host suitability in
compatible interactions. These results are consistent with
the ‘decoy’ hypothesis, that proposes aphids manipulate
plant defence responses through pathway cross-talk, amplifying the SA-signalling pathway to repress a potentially
more biologically effective JA-signalling pathway (ZhuSalzman et al., 2004, 2005). Some caution is required in
interpreting these results, however, because the effects of
npr1 and NahG are not limited to salicylate signalling. A
functional Npr1 gene was required for JA- and ETdependent ISR (Dong, 2004), and NahG had pleiotropic
effects on gene expression that also reduced JA and ET
signalling (Heck et al., 2003).
PFIs trigger modest induction of JA/ET-dependent
responses
Exogenous application of jasmonates to cotton, wheat,
sorghum, and tomato reduce aphid host preference, survival, and fecundity (Omer et al., 2001; Bruce et al., 2003;
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etr1
Transcriptional induction of plant defences by phloem-feeding insects 761
a significant effect of ET insensitivity (conferred by the etr1
mutation) on aphid population growth on Arabidopsis.
Jasmonate-insensitive Arabidopsis mutants (coi1) showed
a modest increase in aphid population growth, suggesting
that JA-dependent responses can limit aphid performance
on wild-type plants (Ellis et al., 2002; Mewis et al., 2005).
By contrast, suppression of JA signalling in tomato had
neutral or, in some cases, negative effects on aphid performance. The jasmonate-insensitive jai-1 mutant in tomato
had no detectable effect on population growth of the potato
aphid (Macrosiphum euporbiae) (FL Goggin, unpublished
data). Furthermore, aphid survival and fecundity on tomato
was dramatically reduced by the spr2 mutation (FL Goggin,
unpublished data), which blocks the conversion of linoleic
to linolenic acid and the subsequent synthesis of JA (Li
et al., 2003). Aphid resistance in spr2 might be due to
enhanced SA-dependent responses, or to the impact of
modified fatty acid profiles on other biosynthetic pathways.
Data from potato suggest that volatile aldehydes derived
from linoleic acid and other oxylipins play a role in limiting
aphid infestation (Vancanneyt et al., 2001).
Taken together, these results suggest that the roles of SA
and JA in plant defence vary among plant species, and
between compatible and incompatible interactions. Further
work is also needed to explore the potential roles of other
hormones, including auxin and gibberellins, in plant
responses to PFIs (Park et al., 2005).
Oxidative stress responses to PFIs
PFIs induce enzymes involved in both generating and
detoxifying reactive oxygen species
Components of aphid salivary secretions generate local and
systemic production of reactive oxygen species (ROS)
(reviewed in Tjallingii, 2006). In addition, plants respond
to many forms of biotic stress by generating ROS that
participate in defensive signalling and potentiate a hypersensitive response (HR) at the infection site (Lamb and
Dixon, 1997). Induction of isolate-specific aphid resistance
in certain plants has been correlated with localized cell
death that resembles HR, although this phenomenon is not
observed in all cases of innate aphid resistance (BelefantMiller et al., 1994; Moran et al., 2002; Sauge et al., 2002;
Martinez de Ilarduya et al., 2003; Klingler et al., 2005). In
general, plants appear to strike a balance between generating ROS as a defensive mechanism and producing ROSdetoxifying enzymes to cope with their own oxidative
damage (Zhu-Salzman et al., 2004). Systemic responses
within the phloem appear to favour detoxification (Divol
et al., 2005), but oxidative stress-related genes are not
uniformly regulated in whole leaf tissues in response to
PFIs. Within a single plant species, aphid feeding can
induce expression of certain antioxidant enzymes while
suppressing others. In Arabidopsis, for example, green
peach aphid infestation up-regulated expression of one
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Cooper et al., 2004; Zhu-Salzman et al., 2004; Cooper and
Goggin, 2005). Furthermore, population growth of the
green peach aphid was significantly reduced on the cev1
mutant in Arabidopsis, in which JA and ET signalling is
constitutively activated (Ellis et al., 2002). These results
suggest that defences regulated by JA and/or ET can
effectively reduce aphid infestations, although the extent
to which aphids induce these defences is unclear. In barley,
ET generation was positively correlated with greenbug
(Schizaphis graminum) resistance, but was associated with
susceptibility to the Russian wheat aphid (Miller et al.,
1994; Argandoña et al., 2001). In Medicago truncatula, the
blue green aphid (Acyrthosiphon kondoi) induced marker
genes associated with JA signalling in a resistant but not
a susceptible cultivar (LL Gao, KB Singh, OR Edwards,
personal communication). In tomato, however, transcripts
of the JA- and wound-responsive proteinase inhibitors (PinI
and PinII) and MeJA/ET-responsive basic b-1,3-glucanase
(GluB) showed only a weak, local, and transient accumulation in response to aphids, and patterns of induction did
not differ between compatible and incompatible interactions
(Martinez de Ilarduya et al., 2003). These data suggest
that JA and ET signalling may be involved in some, but
not all, forms of innate aphid resistance.
In compatible interactions, studies of marker genes
associated with SA and JA/ET signalling suggested that
aphids elicited local induction of all three pathways, but
that induction of SA signalling was more pronounced
(Moran and Thompson, 2001; Zhu-Salzman et al., 2004).
Cluster analysis of microarray data showed that several
genes encoding enzymes required for JA and ET synthesis
were co-ordinately up-regulated at low levels by Myzus
nicotianae feeding on Nicotiana attenuata (Heidel and
Baldwin, 2004; Voelckel et al., 2004). Some, but not all,
isozymes of lipoxygenase that are involved in JA synthesis
were also induced by aphid feeding in tomato, Arabidopsis,
and sorghum (Fidantsef et al., 1999; Moran and Thompson,
2001; Zhu-Salzman et al., 2004). Compared with chewing
insects or artificial wounding, however, aphid feeding had
a far weaker influence on genes encoding JA and ET
biosynthetic enzymes (Fidantsef et al., 1999; Heidel and
Baldwin, 2004). To date, few studies have directly
quantified JA or ET production in response to PFIs.
Argandoña et al. (2001) and Miller et al. (1994) demonstrated that greenbug infestation induces ET production in
barley, but no significant changes in ET levels were
observed in Arabidopsis in response to the green peach
aphid (De Vos et al., 2005). Aphid infestation also did not
modify JA levels in N. attenuata or Arabidopsis (Heidel
and Baldwin, 2004; De Vos et al., 2005).
Several studies on plant–aphid interactions have utilized
mutant plant lines deficient in JA or ET signalling to
investigate the role of these pathways in compatible
interactions with aphids (Table 2). The contribution of ET
remains unclear, as Mewis et al. (2005) did not observe
762 Thompson and Goggin
superoxide dismutase gene (Cu/ZnSOD or CSD1) but
down-regulated another (FeSOD) (Moran et al., 2002).
Greenbug infestation of susceptible sorghum induced transcripts of two glutathione-S-transferase genes, but downregulated one isoform of catalase (Zhu-Salzman et al., 2004).
Similarly, greenbug feeding on resistant sorghum induced
the expression of peroxidase, glutathione-S-transferase, and
quinone oxidoreductase genes, but both up- and downregulated different catalase genes (Park et al., 2005).
PFI-induced changes in structure and
metabolism
PFIs influence primary metabolism in their hosts
Even at low populations, PFIs can significantly reduce
photosynthetic rates in their host plants (Macedo et al.,
2003). Transcript profiling has revealed that PFI infestation
down-regulates expression of photosynthesis-related genes,
such as those required for Rubisco synthesis (Heidel and
Baldwin, 2004; Zhu-Salzman et al., 2004; Voelckel et al.,
2004; Qubbaj et al., 2005; Yuan et al., 2005). Similar
responses that are induced across multiple insect feeding
guilds could represent a shift in resource allocation from
growth to defence (Heidel and Baldwin, 2004). PFIs also
PFIs modify secondary metabolite production
Many secondary metabolites have been implicated in
plant defences against PFIs, including phenylpropanoids,
terpenoids, alkaloids, hydroxamic acids, and glucosinolates. Transcript profiling studies suggest that PFI feeding
modulates expression of enzymes required for secondary
metabolite synthesis. In rice, for example, brown planthopper feeding down-regulated several genes involved in
phenylpropanoid biosynthesis and up-regulated a gene
required for sesquiterpene synthesis (Zhang et al., 2004;
Cho et al., 2005). Functional genomic tools can be applied
to investigate the impact of secondary metabolites on PFIs.
Aharoni et al. (2003) dramatically increased terpenoid
volatile production in Arabidopsis by transforming plants
with a terpene synthase gene from strawberry and determined that transgenic plants significantly repelled the
green peach aphid. For most secondary metabolites,
however, further work is needed to identify key biosynthetic genes before we can manipulate their synthesis
in a targeted manner or understand how PFIs modulate
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Do PFIs elicit plant cell wall remodelling?
A common feature among the transcript profiling studies
was the identification of genes encoding proteins that alter
cell wall structure. Genes encoding cell wall-modifying
enzymes such as xyloglucan endotransglycosylase (XTH)
and pectin methyl esterases were typically up-regulated in
infested plants (Moran et al., 2002; Heidel and Baldwin,
2004; Voelckel et al., 2004; Divol et al., 2005; Qubbaj
et al., 2005). XTH modifies hemicelluloses by removing
and re-attaching oligosaccharides to strengthen cell walls,
while pectin esterases can also contribute to cell wall
stiffening by controlling both the assembly and disassembly
of the pectin network (Willats et al., 2001). Divol et al.
(2005) also found strong systemic up-regulation of genes
encoding cellulose synthase and expansin in celery petiole
phloem in response to green peach aphid feeding on the
leaves. Modification of the cell wall structure could play
a role in aphid resistance in plants. Genes encoding pectin
methyl esterase and inositol phosphatase-like protein were
specifically up-regulated in response to rosy apple aphid
feeding on a resistant cultivar of apple (Qubbaj et al., 2005),
and five cell wall-related genes (2 glucosyl transferases,
caffeic acid O-methyl transferase, proline-rich protein, delta
pyrroline-5-carboxylate dehydrogenase) were up-regulated
in response to greenbug feeding on resistant sorghum (Park
et al., 2005). These structural modifications are thought
to deter PFI herbivory both locally and systemically by
strengthening barriers to insect probing within the host
tissues.
modify source–sink relationships and water relations within
the plant, because they must extract large volumes of
phloem sap to attain adequate nitrogen (Douglas, 2006).
Sugar depletion at PFI feeding sites created localized
metabolic sinks by inducing genes involved in carbon
assimilation and mobilization (Moran and Thompson,
2001; Moran et al., 2002; Zhu-Salzman et al., 2004).
Within the phloem of celery petioles, for example, green
peach aphid feeding up-regulated genes implicated in
remobilizing mannitol reserves (Divol et al., 2005). Mannitol remobilization might also represent a response to
osmotic stress caused by aphid feeding. Aphid infestation
reduced foliar water potential (Cabrera et al., 1994) and upregulated genes encoding aquaporins, membrane-intrinsic
proteins, and other transcripts associated with water stress
(Zhu-Salzman et al., 2004; Divol et al., 2005). PFIs also
modified nitrogen allocation in their hosts by competing
with plant sinks and altering the amino acid composition
of the phloem sap (Sandstrom et al., 2000; Heidel and
Baldwin, 2004; Voelckel et al., 2004; Girousse et al.,
2005). Unlike other herbivores, PFIs up-regulated genes
involved in nitrogen assimilation (Heidel and Baldwin,
2004; Zhu-Salzman et al., 2004). In particular, aphids
induced genes encoding enzymes required for synthesis
of tryptophan and certain other amino acids (Moran
et al., 2002; Zhang et al., 2004; Divol et al., 2005). These
responses can benefit PFIs by enhancing the content of
essential amino acids in the phloem sap (Sandstrom et al.,
2000). Overall, further work is needed to determine if
PFI-induced changes in carbon and nitrogen assimilation, allocation, and water balance contribute to host
susceptibility, or are a means for the plant to compensate
for insect damage.
Transcriptional induction of plant defences by phloem-feeding insects 763
their accumulation. To date, the majority of molecular and
genomic studies on the role of secondary metabolites in
plant–aphid interactions have focused on glucosinolates.
Glucosinolates in brassicaceous plants
Emerging areas of research
To achieve a detailed understanding of plant interactions
with PFIs, it will ultimately be necessary to combine
transcriptomic approaches with proteomic, metabolomic,
and mutational analyses. While plant responses have been
the focus of most transcriptomic studies, additional levels
of complexity can also be analysed with genomic tools.
Investigating changes that occur concurrently within the
insect is essential to understand the basis of an effective
Acknowledgements
This project was supported by the National Research Initiative of
the USDA Cooperative State Research, Education and Extension
Service (CSREES), grant number 2005-03384. GAT was supported
by an Independent Research Plan while working at the National
Science Foundation. Any opinions, findings, and conclusions or
recommendations contained in this material are those of the authors
and do not necessarily reflect the views of the National Science
Foundation.
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These multitrophic interactions must be investigated in
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that occurs under field conditions.
It will also be necessary to conduct future genomic
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sets from different laboratories and different species. It is
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