Update on Herbivory Effects on Primary Metabolism
Alteration of Plant Primary Metabolism in Response to
Insect Herbivory1
Shaoqun Zhou 2, Yann-Ru Lou 2, Vered Tzin 2, and Georg Jander*
Boyce Thompson Institute for Plant Research (S.Z., Y.-R.L., V.T., G.J.) and School of Integrated Plant Sciences
(S.Z., Y.-R.L.), Cornell University, Ithaca, New York 14853
ORCID IDs: 0000-0002-3643-7875 (S.Z.); 0000-0002-4716-4323 (Y.-R.L.); 0000-0002-5912-779X (V.T.); 0000-0002-9675-934X (G.J.).
Plants in nature, which are continuously challenged by diverse insect herbivores, produce constitutive and inducible defenses to
reduce insect damage and preserve their own fitness. In addition to inducing pathways that are directly responsible for the
production of toxic and deterrent compounds, insect herbivory causes numerous changes in plant primary metabolism. Whereas
the functions of defensive metabolites such as alkaloids, terpenes, and glucosinolates have been studied extensively, the fitness
benefits of changes in photosynthesis, carbon transport, and nitrogen allocation remain less well understood. Adding to the
complexity of the observed responses, the feeding habits of different insect herbivores can significantly influence the induced
changes in plant primary metabolism. In this review, we summarize experimental data addressing the significance of insect
feeding habits, as related to herbivore-induced changes in plant primary metabolism. Where possible, we link these physiological
changes with current understanding of their underlying molecular mechanisms. Finally, we discuss the potential fitness benefits
that host plants receive from altering their primary metabolism in response to insect herbivory.
Plants in nature are subject to attack by a wide variety
of phytophagous insects. Nevertheless, the world is
green, and most plants are resistant to most individual
species of insect herbivores. To a large extent, this resistance is due to an array of toxic and deterrent small
molecules and proteins that can prevent nonadapted insects from feeding. Although many plant defenses are
produced constitutively, others are inducible (i.e. defenserelated metabolites and proteins that are normally present
at low levels become more abundant in response to insect
feeding). Inducible defense systems, which allow more
energy to be directed toward growth and reproduction in
the absence of insect herbivory, represent a form of resource conservation. Well-studied examples of inducible
plant defenses include the production of nicotine in tobacco (Nicotiana tabacum; Baldwin et al., 1998), protease
inhibitors in tomato (Solanum lycopersicum; Ryan, 2000),
benzoxazinoids in maize (Zea mays; Oikawa et al., 2004),
and glucosinolates in Arabidopsis (Arabidopsis thaliana;
Mewis et al., 2005). Additionally, herbivore-induced plant
responses can include the production of physical defenses
such as trichomes or thickened cell walls that can make
insect feeding more difficult. Some plant defensive metabolites are highly abundant, suggesting that their biosynthesis can have a significant effect on overall plant
metabolism. For instance, benzoxazinoids can constitute
1% to 2% of the total dry matter of some Poaceae (Zúñiga
et al., 1983), and up to 6% of the nitrogen in herbivore-
induced Nicotiana attenuata can be devoted to nicotine
production (Baldwin et al., 1998).
In addition to the herbivore-induced production of
physical and chemical defenses, numerous changes in
plant primary metabolism occur in response to insect
herbivory. Among other observed effects, these can
include either elevated or suppressed photosynthetic
efficiency, remobilization of carbon and nitrogen resources, and altered plant growth rate. However, although the defensive value of induced toxins such as
nicotine, terpenes, benzoxazinoids, and glucosinolates
is clear, it is sometimes more difficult to elucidate the
function of herbivore-induced changes in plant primary
metabolism. Insects may also manipulate plant primary
metabolism for their own benefit, making it challenging
to determine whether the observed changes are actually
a plant defensive response.
Here, we describe commonly observed changes in
plant primary metabolism, focusing on carbohydrates
and nitrogen, and discuss their possible functions in
plant defense against insect herbivory. There are large
differences among published studies involving different
plant-herbivore combinations, and no universal patterns
in the herbivory-induced changes in plant primary metabolism. Therefore, we also discuss how the potential
benefits can depend on the tissue that is being attacked,
the extent of the tissue damage, and the type of insect
herbivore that is involved in the interaction.
1
This work was supported by the National Science Foundation
(grant nos. 1139329 and 1339237).
2
These authors contributed equally to the article.
* Address correspondence to [email protected].
www.plantphysiol.org/cgi/doi/10.1104/pp.15.01405
BIOSYNTHESIS AND MOVEMENT OF
PRIMARY METABOLITES
Research on changes in primary metabolism associated with insect feeding has been focused largely on the
1488 Plant PhysiologyÒ, November 2015, Vol. 169, pp. 1488–1498, www.plantphysiol.org Ó 2015 American Society of Plant Biologists. All Rights Reserved.
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Herbivory Effects on Primary Metabolism
role of carbohydrates and amino acids. Carbohydrates,
as products of photosynthesis, are the major source of
stored energy for both host plants and insect herbivores. Amino acids, the major form of nitrogen found in
plants, are not only growth limiting for insect herbivores but also serve as precursors for many defenserelated plant metabolites. Thus, regulation of amino
acid biosynthesis represents an important control
mechanism in plant defense against herbivory. Both
local responses at the site of insect feeding and systemic
responses that can involve resource reallocation are
important components of plant-herbivore interactions.
Carbohydrate Metabolism
Photosynthesis, which is the source of almost all
carbohydrates in green plants, is central to any discussion of carbon allocation in response to herbivory.
There are divergent theories as to how plants should
alter photosynthesis, and thereby carbon fixation, to
optimize defense. On the one hand, photosynthetic
activity might be promoted because (1) synthesis
of defensive metabolites requires carbon fixation, (2)
plants may compensate for the loss of leaf area by increasing photosynthetic activity in the remaining tissue,
or (3) insects could manipulate plant metabolism to
increase carbon fixation and thereby obtain more resources. On the other hand, photosynthetic activity
could be reduced because (1) production of the photosynthetic apparatus itself is energy intensive and, as a
trade-off for the production of increased defensive
metabolites, photosynthesis would be compromised;
(2) if insect feeding is localized, senescence and eventual abscission of the affected foliar tissue could involve
a reduction in photosynthesis; or (3) less carbon assimilation could make fewer carbohydrates available
for the insect herbivores.
In most cases, the latter hypothesis, reduced photosynthesis in response to herbivory, is supported by
actual measurements of changes in photosynthesis rate,
photosynthesis-related gene expression, or production
of proteins that are part of the photosynthetic apparatus
(Reymond et al., 2004; Giri et al., 2006; Wei et al., 2009;
Bilgin et al., 2010; Coppola et al., 2013; Appel et al.,
2014). Reduced photosynthetic capacity can exceed
what would be expected from the observed amount of
foliar tissue that is removed (Zangerl et al., 2002).
However, actual insect damage is not a prerequisite for reduced photosynthetic activity. Feeding by
both chewing herbivores that remove leaf material
(Reymond et al., 2004; Lawrence et al., 2008) and
phloem-feeding insects that do not (Zhu-Salzman et al.,
2004; Botha et al., 2006) resulted in lower levels of
photosynthesis-related gene expression. Even plantperceived evidence of insect attack that does not lead
to any actual damage (e.g. insect oviposition [Little
et al., 2007; Velikova et al., 2010] or exposure to volatiles
from infested plants [Arimura et al., 2000]) can reduce
photosynthetic capacity. Together, these observations
indicate that reduction in photosynthetic activity is an
active plant response, rather than just a side effect of
metabolic limitation during insect herbivory.
A regulated plant response is also indicated by the fact
that the jasmonic acid signaling pathway, which influences many aspects of plant defense against insect herbivory, is required for the observed suppression of
photosynthesis and growth (Wasternack and Hause,
2013). Treatment of Arabidopsis with coronatine, which
induces defenses as a molecular mimic of jasmonate-Ile
conjugate, reduced photosynthesis-related gene expression within 2 h (Attaran et al., 2014). However, actual
photosynthetic output was not reduced until the following day in this experiment. Thus, it may be possible
for plants to increase the production of defensive metabolites without having an immediate deficit in photosynthesis and carbon fixation.
Despite the general pattern of decreased photosynthesis in response to insect feeding, there are also welldocumented exceptions. When mirid bugs (Tupiocoris
notatus) are feeding from N. attenuata (Halitschke et al.,
2011), increases in CO2 fixation that occurred in response to components of mirid bug saliva compensated
for the loss of functional leaf tissue during insect feeding. Thus, there was no observed decrease in plant fitness due to mirid bug feeding. Similar increases in
photosynthetic capacity have been observed in other
plant species that are tolerant of herbivory (i.e. growth
and reproductive fitness are not significantly impacted
by insect damage). For instance, wheat (Triticum aestivum)
and barley (Hordeum vulgare) resistance to Russian wheat
aphids (Diuraphis noxia) has been associated with increased expression of photosynthesis-related genes
after attack (Botha et al., 2006; Gutsche et al., 2009).
In the more common case, where there is reduced
photosynthetic activity in response to insect feeding,
plants nevertheless face increased energetic and carbon
demands to support production of inducible defenses.
With reduced carbohydrate supply from photosynthesis, cells in herbivore-attacked plant tissues may need
other sources of carbon and energy to produce defenserelated metabolites. To cope with this challenge, many
plants respond to herbivore attack by promoting local
catabolism of energy storage compounds (e.g. Suc or
starch). For instance, a transcriptomic study involving
Arabidopsis and four different insect herbivores
showed increased expression of invertases and genes
encoding enzymes involved in degrading complex
carbohydrates (Appel et al., 2014; Fig. 1A). Similarly, in
grain amaranth (Amaranthus cruentus), foliar herbivory
induced a local increase in cytoplasmic invertase and
amylolytic enzyme activities (Castrillon-Arbelaez et al.,
2012). Furthermore, this study showed lower concentrations of monosaccharides, Suc, and starch in local
tissues in the days after herbivore infestation.
As in the case of altered photosynthetic activity, not
all studies show the same pattern of local, herbivoreinduced carbohydrate catabolism. For example, tomato
leaves that were fed upon by two caterpillar species
(Helicoverpa zea and Manduca sexta) exhibited few or no
changes in sugar content (Steinbrenner et al., 2011).
Plant Physiol. Vol. 169, 2015
1489
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Figure 1. Overview of Arabidopsis primary metabolism gene expression changes. Gene expression data from Appel et al. (2014)
were analyzed using MapMan (http://mapman.gabipd.org/web/guest/mapman), identifying 178 genes of primary metabolism
that showed significantly altered expression in response to at least one herbivore treatment. A, Overrepresentation analyses of the
primary metabolism pathways induced in response to feeding by two chewing herbivores (cabbage butterfly [Pieris rapae] and
1490
Plant Physiol. Vol. 169, 2015
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Herbivory Effects on Primary Metabolism
Instead, monosaccharide levels were significantly depleted in the shoot apex and root, tissues that were not
directly attacked, whereas Suc and raffinose concentrations were not affected.
Although increased photosynthesis and/or local carbohydrate catabolism can serve as energy sources for the
production of plant defenses in many plant-herbivore
interactions, the observed exceptions suggest that there
are also other mechanisms of defense induction. As
discussed below, herbivore-attacked tissue could draw
energy from systemic tissues through carbon reallocation. Or, alternatively, there are other potential energy
sources (e.g. protein degradation to release free amino
acids, which is observed in response to a variety of plant
stress treatments [Caldana et al., 2011]).
Nitrogen Metabolism
Plant amino acids play a central role in plantherbivore interactions, both as major growth-limiting
nutrients and as precursors for the production of many
plant defense compounds. Given this dual function of
amino acids, herbivore-infested plants are hypothesized to enhance their amino acid production for the
synthesis of defensive metabolites, while striving to
limit the herbivores’ access to free amino acids. For instance, genes involved in both amino acid biosynthesis
and sulfur assimilation, which is required for Cys and
Met biosynthesis, are overrepresented among those
that are induced by caterpillar feeding on Arabidopsis
(Appel et al., 2014; Fig. 1A). Increased expression of
genes related to Met and Trp biosynthesis (Appel et al.,
2014) can lead to greater accumulation of defenserelated glucosinolates, which are largely derived from
Met and Trp in Arabidopsis (Halkier and Gershenzon,
2006). Similarly, foliar insect herbivory induced strong
accumulation of Trp, which can serve as a precursor for
defensive metabolites, in systemic stem and apex tissue
of tomatoes (Steinbrenner et al., 2011). Hence, in some
scenarios, herbivore-induced amino acid biosynthesis
likely serves as a response to support inducible production of defense metabolites.
In other cases, herbivore-induced changes in amino
acid metabolism may be related to subsequent amino
acid movement between attacked and systemic tissues.
Phloem transport of nitrogen in many plant species, including Arabidopsis, is dominated by Gln, Glu, Asn, and
Asp, the four main amino acids involved in nitrogen
assimilation (Coruzzi and Last, 2000). Indeed, transcript
profiling experiments generally show herbivory-induced
changes in the expression of genes related to the production of these amino acids. For instance, herbivory on
sorghum induced expression of nitrate and nitrite reductases that are required for nitrogen assimilation into
Gln and Glu (Zhu-Salzman et al., 2004); expression of
Glu synthase (also known as Gln oxoglutarate aminotransferase, or GOGAT) was induced by aphid feeding
on N. attenuata (Voelckel et al., 2004); and aphid feeding
induced Gln synthetase, which acts together with
GOGAT in the Gln synthetase/GOGAT cycle, in celery
(Apium graveolens; Divol et al., 2005). However, examination of multiple such data sets shows that either
production or degradation amino acids can be preferred, depending on the specific plant-herbivore system being investigated and the type of tissue (local or
systemic) being analyzed (Dorschner et al., 1987;
Sandström et al., 2000; Arnold et al., 2004; Koyama
et al., 2004; Caldana et al., 2011; Appel et al., 2012).
Since nitrogen is a key nutrient for most insect herbivores, transcriptional changes of genes involved in
amino acid metabolism also may result from insect manipulation of plant gene expression. Particularly in the
case of some aphids, there is good evidence of increased
free amino acids levels being the direct result of insect
feeding. For instance, chlorosis-inducing greenbugs
(Schizaphis graminum) enhance the content of essential
amino acids in the phloem sap of wheat (Dorschner et al.,
1987; Sandström et al., 2000). A similar scenario has been
reported in Japanese rowan (Sorbus commixta) leaves
infested with apple-grass aphids (Rhopalosiphum insertum), such that the amount of amino acids exuded from
galled leaves was 4-fold higher than from ungalled ones
(Koyama et al., 2004). Yet, the exact physiological events
underlying these ecological observations are not fully
elucidated. It is likely that these herbivores enrich the
amino acid content of their diet by some combination of
(1) increasing free amino acid biosynthesis, (2) inducing
early senescence and proteolysis to release free amino
acids into the phloem, or (3) manipulating the sinksource relationship to allow more transport of nitrogen
into infested leaves.
Reallocation of Primary Metabolites
Insect attack frequently induces mobilization of
existing and newly assimilated primary metabolites
Figure 1. (Continued.)
beet armyworm [Spodoptera exigua]) and two piercing-sucking herbivores (cabbage aphid [Brevicoryne brassicae] and green
peach aphid [Myzus persicae]). Data analysis and representation were conducted using the PageMan function of MapMan
(Usadel et al., 2006). Blue indicates decreases and red indicates increases in transcription of the affected genes. B, Correlation and
clustering of the expression of the 178 genes in response to the applied treatments. Analysis was conducted using JMP Pro 11 (SAS,
www.jmp.com). Red indicates positive correlation and blue indicates negative correlation of the respective data sets. PS, Photosynthesis; LHC-II, photosystem II light-harvesting complex; CHO, carbohydrate metabolism; TPS, trehalose synthase; TPP,
trehalose phosphatase; OPP, oxidative pentose phosphate; PP, pentose phosphate; FA, fatty acid; ATPS, ATP sulfurylase; APR,
adenylyl-sulfate reductase; AKN, adenosine-5’-phosphosulfate-kinase.
Plant Physiol. Vol. 169, 2015
1491
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Zhou et al.
between attacked and systemic tissues. Movement of
primary metabolites toward herbivore-attacked tissue
can be interpreted as (1) providing substrates for the
reinforcement of local defenses, or (2) manipulation of
plant metabolism by the insects, as described above. In
contrast, movement of primary metabolites away from
insect feeding sites has been hypothesized to (1) directly
starve herbivores, (2) promote tolerance of herbivore
damage by preserving resources for later regrowth, or
(3) recruit beneficial soil microbes as an indirect defense
response. Numerous studies examining carbon and
nitrogen movement in response to insect feeding have
been conducted, and specific examples fitting all of
these scenarios can be found in nature.
Consistent with the hypothesis that import of systemic resources promotes plant defense, treatment with
volatile defense signal methyl jasmonate, mechanical
damage, and actual insect feeding all can increase
movement of carbohydrates toward treatment sites in
many plant species (Sturm and Chrispeels, 1990; Zhang
et al., 1996; Ehness et al., 1997; Ohyama and Hirai, 1999;
Allison and Schultz, 2005; Schultz et al., 2013). In
methyl jasmonate-treated or wounded Arabidopsis,
radioactively labeled carbohydrates were imported
into sink leaves within hours after treatment, and were
incorporated into defense-related compounds such as
cinnamic acid and phenolic glycosides (Ferrieri et al.,
2012). When carbohydrate import was disrupted by
removing source leaves or cutting vascular connections, hybrid poplar (Populus deltoides 3 Populus nigra)
defenses were induced less efficiently (Arnold and
Schultz, 2002; Arnold et al., 2004). In contrast to carbohydrate transport, labeled nitrogen tracking studies
have shown little evidence of jasmonic acid-induced
nitrogen transport to elicited leaves in poplar (Arnold
et al., 2004; Appel et al., 2012). Nevertheless, it is well
established that defense-related nitrogenous compounds such as nicotine and other alkaloids are transported from roots to leaves upon insect attack (Baldwin
et al., 1994; Hartmann and Ober, 2000; Ziegler and
Facchini, 2008). Hence, it may be a common theme that
plants deliver nitrogen as premanufactured resistance
compounds but carbon as free carbohydrates for local
production of defensive metabolites. Possible explanations for this dichotomy are that (1) carbohydrates are
relatively inexpensive in plants growing under full
sunlight, and (2) given that nitrogen is often the
growth-limiting nutrient for herbivores, direct delivery
of nitrogen in the form of phloem-transported amino
acids could inadvertently lead to improved nutrition of
the herbivores, rather than the production of defensive
metabolites.
In support of contrasting hypotheses, herbivore attack or chemical elicitation of plant defenses can redirect primary metabolites away from treated tissues
(Holland et al., 1996; Lu et al., 2015). Such reallocation
of primary metabolites may hamper herbivore performance by reducing the nutritive value of plant tissue.
For example, both the generalist cucumber beetle
(Diabrotica balteata) and the specialist rice water weevil
(Lissorhoptrus oryzophilus) grew significantly slower on
a jasmonate-deficient rice (Oryza sativa) mutant, despite
the fact that these plants suffered greater loss of biomass than wild-type controls (Lu et al., 2015). This observation was correlated with herbivore-induced
depletion of Suc in the infested tissue of the mutant rice
line. In an example that indicates nitrogen transport
away from insect feeding sites, foliar feeding by monarch caterpillars (Danaus plexippus) decreased nitrogen
allocation to the leaves of common milkweed (Asclepias
syriaca), whereas a below-ground herbivore, larvae of
red milkweed beetle (Tetraopes tetrophthalmus), significantly induced nitrogen movement away from roots to
stems and leaves (Tao and Hunter, 2013).
In addition to making plant tissue less nutritious,
herbivore-induced reallocation of primary metabolites
could be a tolerance strategy that allows later regrowth
after the threat of herbivory has passed (Millard and
Grelet, 2010). For instance, carbohydrate was transported away from maize roots infested with western
corn rootworm (Diabrotica virgifera) into stem tissue,
thereby allowing better regrowth of crown roots after
herbivory (Robert et al., 2014). In the opposite phenomenon, simulated herbivory of N. attenuata promoted carbon movement to the roots, which provided
reserves to subsequently delay senescence and prolong
the reproductive phase of the plants (Schwachtje et al.,
2006).
Finally, metabolites that are transported in response
to herbivore attack may be exuded rather than stored
within the plants themselves (Holland et al., 1996; Lee
et al., 2012). Lee et al. (2012) suggested that increased
root exudation by pepper (Capsicum annuum) upon foliar aphid herbivory can attract beneficial rhizospheric
microbes that are known to promote plant health, and
hence should be considered a means of indirect defense.
Similarly, grasshopper feeding on maize leaves caused
increased carbon release and respiration in the root
system (Holland et al., 1996).
Although physiological experiments have provided
evidence describing the pattern of herbivore-induced
primary metabolite reallocation, and some studies have
gone further to test particular hypotheses, the signaling
and molecular mechanisms that control resource reallocation remain relatively uninvestigated. Reallocation
of carbohydrates is thought to be primarily driven by
differential sink strength of tissues, which is in turn
heavily influenced by activities of cell wall-bound invertases (Sturm and Tang, 1999; Schultz et al., 2013). In
congruence with this framework, herbivore-induced
carbohydrate depletion has coincided with decreased
invertase activities in the same tissues (Machado et al.,
2013; Robert et al., 2014). Carbohydrate movement in
source tissues is facilitated by sets of membrane transporters (Burkle et al., 1998; Gottwald et al., 2000; Ayre,
2011; Chen et al., 2012). Although expression of these
transporters is required for herbivore-induced carbohydrate reallocation (Ferrieri et al., 2012), there is so far
little evidence showing that their expression is directly influenced by herbivore attack. In contrast, genes
1492
Plant Physiol. Vol. 169, 2015
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Herbivory Effects on Primary Metabolism
encoding transporters for both inorganic nitrogen and
specific amino acids have been shown to be differentially expressed in response to wounding (Grallath
et al., 2005; Meyer et al., 2006), jasmonic acid treatment
(Okamoto et al., 2006; Camañes et al., 2012), and insect
herbivory (Voelckel et al., 2004; Coppola et al., 2013).
Thus, these herbivore-induced changes in gene expression could provide a gateway for future efforts to
incorporate resource reallocation into the current signaling and molecular framework of herbivore-induced
responses.
OPTIMAL PLANT RESPONSES IN PRIMARY
METABOLISM DEPEND ON THE SPECIFIC NATURE
OF THE PLANT-HERBIVORE INTERACTION
Although there are some recurring themes, there are
by no means universal patterns in the observed
herbivore-induced changes in plant primary metabolism. For instance, whereas photosynthetic activity is
generally reduced upon herbivore attack, some studies show the exact opposite. Although many publications show reallocation of carbohydrates toward
herbivore-attacked plant tissues, others support resource
sequestration. Together, this sometimes contradictory
experimental evidence suggests that herbivore-attacked
plants are genetically programmed to adopt different responses in primary metabolism based on the nature of a
specific plant-herbivore interaction. Therefore, in addition
to testing functional hypotheses of herbivore-induced
primary metabolic changes on a case-by-case basis, it is
necessary to establish a theoretical framework to address
the many variables that will influence the reconfiguration
of primary metabolism. Recent reviews have addressed
aspects of this challenging question (Schwachtje and
Baldwin, 2008; Orians et al., 2011; Massad, 2013). For instance, Orians et al. (2011) proposed a fulcrum model
containing several intrinsic and extrinsic factors that may
shift plants between resource reallocation toward and
away from herbivore-attacked tissues. In contrast, Massad
(2013) discussed how plant ontogeny affects broader
herbivore-induced plant responses. Here, we focus on the
effects that specific herbivore characteristics, including (1)
the feeding guild, (2) dietary specialization, (3) the extent
and type of damage that is caused, and (4) the composition of insect secretions, can have on plant primary metabolism during responses to insect herbivory.
Insect Feeding Guilds
The diverse mouthparts of insects, ranging from
mandibles to stylets, vary in the amount of damage that
they inflict on plant tissue (Fig. 2). Chewing herbivores
such as caterpillars and beetle larvae cause extensive
tissue damage. In contrast, piercing/sucking Hemiptera, including whiteflies, aphids, and psyllids, remove
phloem sap and cause relatively little visible damage.
Other arthropods such as mites (Tetranychoidea) and
thrips (Thysanoptera) feed on cell contents, damaging
Figure 2. Different insect herbivores differ in the amount of physical
damage that they impose on plants. Beet armyworm (A) and corn leaf
aphid (Rhopalosiphum maidis; B) are shown feeding from maize.
the surface without macerating the entire leaf. These
diverse feeding habits lead to highly differentiated
metabolic changes in plants.
Correlation of changes in primary metabolism gene
expression that are induced by caterpillars and aphids,
respectively, indicates that the feeding guild (chewing
versus piercing/sucking) has an important effect on the
metabolic pathways that are induced or repressed
(Appel et al., 2014; Fig. 1B). Arabidopsis gene expression induced by two caterpillar species, cabbage butterfly and beet armyworm, is highly correlated, but
different from that induced by two aphid species, green
peach aphid and cabbage aphid. A variety of factors,
ranging from the amount of physical tissue damage
to manipulation of plant defenses by insect salivary
components, could influence these differences in the
gene expression induced by different feeding guilds.
Intuitively, chewing herbivores would cause greater
loss of photosynthetic capacity due to greater tissue
damage. Although this hypothesis has received some
experimental support (Duceppe et al., 2012), there are
also examples showing photosynthesis reduction in the
absence of extensive tissue damage, as we have discussed above. Because herbivore-induced reduction in
photosynthesis is an active plant response, one cannot
simply assume that chewing herbivores tend to cause a
more drastic decrease in photosynthetic activity than
phloem and cell content feeders.
Less is known about how carbohydrate breakdown,
amino acid metabolism, and resource reallocation are
differentially affected in plants when challenged by
herbivores from different feeding guilds. Orians et al.
(2011) hypothesized that greater tissue damage would
make resource sequestration a preferred strategy. In
support of this hypothesis, the chewing herbivore
Egyptian cotton worm (Spodoptera littoralis) feeding on
cotton reduced leaf growth, whereas leaf growth was
not affected by a cell content feeder, the red spider mite
(Tetranychus urticae; Schmidt et al., 2009). Similarly,
caterpillar feeding on young turnip (Brassica rapa) increased the mass of storage bulbs, whereas aphid infestation promoted leaf growth (Sotelo et al., 2014).
Plant Physiol. Vol. 169, 2015
1493
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Zhou et al.
These changes, however, were not observed on older
plants, suggesting that plant ontogeny was more influential in this particular system.
Dietary Specialization
Although there is obviously a continuum in the
degree of host plant specialization, for convenience,
individual species of insect herbivores are often classified as being specialists or generalists (Fox, 1981;
Berenbaum et al., 1989; Ali and Agrawal, 2012). Specialist herbivores are generally limited to feeding from
plants in a specific family or even genus, and are
typically able to tolerate the characteristic defensive
metabolites (Agrawal and Kurashige, 2003; Gols et al.,
2008). In contrast, generalist herbivores have a wider
host range, typically show a lower tolerance of specialized plant toxins, and tend to feed from lessdefended parts of the host plant (Ballhorn et al.,
2010; e.g. senescing leaves). By themselves, such divergent feeding preferences could influence the type
of changes in plant primary metabolism that are induced by insect feeding.
As specialist herbivores are often highly resistant to
the toxins of their host plants, there may be greater
benefits resulting from sequestering primary metabolites rather than increasing the production of specialized defenses. Steinbrenner et al. (2011) supported this
hypothesis by showing that feeding by the generalist
H. zea induced more phenolics, amino acids, and other
defense-related compounds, whereas the specialist
M. sexta primarily caused accumulation of metabolites
such as Glu and Gln that associated with carbon and
nitrogen transport. As the sample size consists of only
two species, there clearly are other possible explanations for this observation (e.g. differing amounts of leaf
area consumed by the two herbivores). Nevertheless,
these results are consistent with the hypothesis that, in
response to specialist herbivores, plants should modify
their growth rate and change resource allocation instead of increasing chemical defenses that are predicted
to have less impact. In another study on tomato, M. sexta
regurgitant treatment was shown to decrease plant
growth and chlorophyll content, but accelerate regrowth
after defoliation, a collection of responses resembling a
resource sequestration and herbivore tolerance strategy
(Korpita et al., 2014).
There are, however, counterexamples to the hypothesis that responses of plant primary metabolism to
specialist and generalist herbivores should be different.
The duration of feeding (6 or 24 h) had a greater effect
than the herbivore species when measuring gene expression induced by the specialist cabbage butterfly
and the generalist beet armyworm feeding on Arabidopsis (Appel et al., 2014; Fig. 1B). Similarly, comparison of cabbage butterfly with the generalist Egyptian
cotton worm showed almost identical induced gene
expression patterns, including genes that are involved
in primary metabolism (Reymond et al., 2004).
Duration of Infestation
The time of exposure to insect infestation, and by
extension the amount of tissue damage that occurs
during feeding, is another parameter that significantly
affects plant metabolic responses (Frost et al., 2008;
Bruce, 2015). Metabolites and energy can be allocated
more efficiently if there is not only recognition of herbivory, but also reprogramming over time (Mithöfer
and Boland, 2012). Within an hour after exposure to
herbivore feeding, expression of genes encoding diverse plant metabolic pathways is altered (FürstenbergHägg et al., 2013). However, most published research
on plant responses to herbivory has been focused on
longer time periods ranging from 6 hours to several
days after the start of infestation. Coppola et al. (2013)
performed transcriptomic and proteomic analyses of
tomato leaves infested with potato aphids (Macrosiphum
euphorbiae) for 1, 2, and 4 d. Comparison of significantly
altered transcripts showed limited overlap; expression of
only three genes was significantly altered at all three
measurement times. Appel et al. (2014) found that the
duration of caterpillar infestation had a greater effect on
primary metabolism than the degree of herbivore specialization or even the tissue being assayed (local versus
systemic; Fig. 1B). Given the dynamic changes in plant
metabolism that occur during insect feeding, any conclusion about changes in plant primary metabolism in
response to insect feeding must be tempered with the
statement “at this particular time point.”
Insect Secretions
Plants can recognize insect herbivores by perceiving
so-called herbivore-associated molecular patterns
(Heil, 2009), characteristic changes in the plant metabolite profile that can result from the addition of insectderived compounds, modification of plant metabolites
by insect enzymes, or changes in the abundance of endogenous plant metabolites (e.g. the accumulation of
cell wall fragments due to damage from chewing herbivores). Specific metabolites that trigger plant defenses
have been found in the saliva of both lepidopteran and
orthopteran herbivores (Alborn et al., 1997, 2000, 2007).
In N. attenuata, insect-derived fatty acid-amino acid
conjugates are perceived by a protein that acts as a
suppressor of abscisic acid catabolism (Dinh et al.,
2013). As abscisic acid regulates free amino acid accumulation in plants (Nambara et al., 1998), this provides
a direct link between herbivore-derived elicitors and
primary metabolism. Species-specific differences in the
metabolites secreted by lepidopteran herbivores are
thus likely to affect the types of changes that are induced in plant primary metabolism.
In contrast to chewing insects, most of the reported
functional molecules in aphid saliva are proteins that
are secreted into the phloem (Tjallingii and Esch, 1993;
Moreno et al., 2011; Ammar and Hall, 2012). Several
proteomic studies have identified potential effectors in
aphid saliva (Harmel et al., 2008; Carolan et al., 2009;
1494
Plant Physiol. Vol. 169, 2015
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Herbivory Effects on Primary Metabolism
Rao et al., 2013), and specific proteins have been reported
to affect aphid performance on host plants (Bos et al.,
2010; Elzinga et al., 2014). Although there are clearly
differences in the salivary proteomes of different aphid
species, it is not yet known whether this variation
causes differences in plant primary metabolism, such as
those that are observed when the specialist cabbage
aphid and the generalist green peach aphid are feeding
from Arabidopsis (Fig. 1).
In addition to salivary components, waste products
that are secreted by insects onto host plant leaves likely
influence plant primary metabolism. Aphids and other
Hemiptera secrete sugar-rich honeydew that contains
abundant trehalose (Hodge et al., 2013). Trehalose and
trehalose-6-phosphate are important plant-signaling
molecules regulating the relative allocation of carbon
into starch and sugar (Cortina and Culiáñez-Macià,
2005), as well as plant growth and development (SatohNagasawa et al., 2006). As the concentration of trehalose in aphid honeydew is higher than what is normally
found in plants, it may influence sugar metabolism in
the leaves from which the aphids are feeding. Research
involving both Arabidopsis and tomato genes suggested that TREHALOSE PHOSPHATE SYNTHASE11
activity regulates host defense during infestation with
green peach aphid by providing a threshold level of
signaling trehalose (Singh et al., 2011; Singh and Shah,
2012). However, whether plants regulate trehalose
signaling through an internal pool or in response to
exogenous addition from insect honeydew remains an
open question (Lunn et al., 2014).
CONCLUSION
Insect herbivory clearly has profound effects on plant
primary metabolism. However, the specific costs and
benefits are not yet fully defined. Depending on factors
such as the host plant species, the tissue being infested,
the feeding style of the particular insect herbivore, and
the duration of insect feeding, different plant defensive
strategies may provide optimal fitness gains. The situation is further complicated by the fact that any observed changes in plant primary metabolism may result
from the ability of some insect herbivores to manipulate
plant primary metabolism for their own benefit. Thus, it
is probably not possible to make universal statements
about the regulation of primary metabolism during
insect herbivory, but rather one must consider each
plant-insect interaction individually to determine how
plants are responding in a particular situation and what
fitness benefits these responses may provide.
FUTURE PERSPECTIVES
In this review, we have outlined hypotheses regarding changes in plant primary metabolism that should
occur in response to insect feeding to promote plant
fitness. We have compiled experimental evidence that
supports or refutes specific hypotheses. Because
herbivore-induced metabolic changes are influenced by
a large number of variables, we have emphasized the
importance of accounting for these intrinsic and environmental factors in a more comprehensive framework.
One of the major challenges for drawing overarching
conclusions from these studies was the inconsistency in
experimental conditions and the resulting poor comparability of results from different studies. Hence,
experiments that are more specifically designed to
evaluate how different plant and insect characteristics
and environmental factors influence herbivore-induced
changes in plant metabolism are required for answering
this complex and important question. Additionally,
most published studies describe investigation of plant
responses to herbivory using either transcriptomic or
metabolomic approaches, but rarely both at the same
time. Although both approaches generate large
amounts of data, they are also inherently limited. For
example, Castrillon-Arbelaez et al. (2012) found little
correlation between transcript abundance and enzymatic
activities when studying herbivore-induced changes
in carbohydrate metabolism. Similarly, Coppola et al.
(2013), from among a thousand differentially expressed
transcripts and 87 differentially abundant proteins,
found only three transcript-protein matches in herbivoreattacked tomato leaves. These observations highlight
the role of posttranscriptional effects in herbivoreinduced responses in plants, especially when sampling after a short period of infestation. On the other
hand, metabolite profiling of the static pool in tissues at
different time points does not differentiate the dynamics of different metabolic pathways that may result
in a similar accumulation or depletion of certain metabolites. An observed accumulation of free amino
acids, for example, gives limited information about
whether they are a result of reallocation from systemic
tissues or local protein degradation. Therefore, it is
important to combine transcriptomic, proteomic, and
metabolomic approaches to devise testable hypotheses
and draw valid conclusions.
There also are notable gaps in our understanding
of plant primary metabolism during insect feeding.
Lipids, for instance, are an important group of primary
metabolites that remain comparatively uninvestigated.
Whereas many lipids serve important storage and
structural purposes, others are precursors of plant
defense signaling molecules such as jasmonic acid.
However, little is known about the dynamic changes in
the lipid metabolism of plants facing herbivore attack.
Pioneering work has shown remarkable diversity in the
plant lipidome, which can be restructured during abiotic stress in a genotype-specific manner (Degenkolbe
et al., 2012). The relatively few lipidomic studies of
herbivore infestation (e.g. measurement of maize lipid
responses to Egyptian cotton worm feeding; Marti
et al., 2013) demonstrate significant induced responses.
Thus, further research is warranted to explore the role
of endogenous plant lipids in plant-herbivore interactions.
Plant Physiol. Vol. 169, 2015
1495
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Zhou et al.
In another frontier, exciting progress has been made
in elucidating the signaling pathways that trigger and
regulate herbivore-induced changes in plant primary
metabolism. Lu et al. (2015), for example, found that
herbivore-induced carbohydrate sequestration can still
occur in the roots of jasmonate signaling-deficient rice
mutants, whereas reallocation of carbohydrates toward
herbivore-attacked leaves and away from roots in
N. attenuata is modulated by both jasmonate and auxin
signaling (Machado et al., 2013, 2015). Following this
same line of investigation, concomitant with the incorporation of less-studied signaling networks, one would
expect the eventual union of defense signaling networks that control herbivore-induced changes in both
primary and secondary metabolism.
Received September 9, 2015; accepted September 15, 2015; published September
16, 2015.
LITERATURE CITED
Agrawal AA, Kurashige NS (2003) A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J Chem Ecol 29:
1403–1415
Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz
EA, Teal PE (2007) Disulfooxy fatty acids from the American bird
grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl
Acad Sci USA 104: 12976–12981
Alborn HT, Jones TH, Stenhagen GS, Tumlinson JH (2000) Identification
and synthesis of volicitin and related components from beet armyworm
oral secretions. J Chem Ecol 26: 203–220
Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH,
Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276: 945–949
Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores
and plant defense. Trends Plant Sci 17: 293–302
Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a
galling cynipid. J Chem Ecol 31: 151–166
Ammar ED, Hall DG (2012) New and simple methods for studying hemipteran stylets, bacteriomes, and salivary sheaths in host plants. Ann
Entomol Soc Am 105: 731–739
Appel HM, Arnold TM, Schultz JC (2012) Effects of jasmonic acid,
branching and girdling on carbon and nitrogen transport in poplar. New
Phytol 195: 419–426
Appel HM, Fescemyer H, Ehlting J, Weston D, Rehrig E, Joshi T, Xu D,
Bohlmann J, Schultz J (2014) Transcriptional responses of Arabidopsis
thaliana to chewing and sucking insect herbivores. Front Plant Sci 5: 565
Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J
(2000) Herbivory-induced volatiles elicit defence genes in lima bean
leaves. Nature 406: 512–515
Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J (2004) Carbohydrate translocation determines the phenolic content of Populus
foliage: a test of the sink-source model of plant defense. New Phytol 164:
157–164
Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for
induced tannin biosynthesis in developing leaves of Populus. Oecologia
130: 585–593
Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J, Kramer DM, He SY,
Howe GA (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165: 1302–1314
Ayre BG (2011) Membrane-transport systems for sucrose in relation to
whole-plant carbon partitioning. Mol Plant 4: 377–394
Baldwin IT, Gorham D, Schmelz EA, Lewandowski CA, Lynds GY (1998)
Allocation of nitrogen to an inducible defense and seed production in
Nicotiana attenuata. Oecologia 115: 541–552
Baldwin IT, Schmelz EA, Ohnmeiss TE (1994) Wound-induced changes in
root and shoot jasmonic acid pools correlate with induced nicotine
synthesis in Nicotiana sylvestris Spegazzini and Comes. J Chem Ecol 20:
2139–2157
Ballhorn DJ, Kautz S, Lieberei R (2010) Comparing responses of generalist
and specialist herbivores to various cyanogenic plant features. Entomol
Exp Appl 134: 245–259
Berenbaum MR, Zangerl AR, Lee K (1989) Chemical barriers to adaptation
by a specialist herbivore. Oecologia 80: 501–506
Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic
stress globally downregulates photosynthesis genes. Plant Cell Environ
33: 1597–1613
Bos JI, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A
functional genomics approach identifies candidate effectors from the
aphid species Myzus persicae (green peach aphid). PLoS Genet 6:
e1001216, doi: 10012
Botha AM, Lacock L, van Niekerk C, Matsioloko MT, du Preez FB, Loots
S, Venter E, Kunert KJ, Cullis CA (2006) Is photosynthetic transcriptional regulation in Triticum aestivum L. cv. ‘TugelaDN’ a contributing
factor for tolerance to Diuraphis noxia (Homoptera: Aphididae)? Plant
Cell Rep 25: 41–54
Bruce TJA (2015) Interplay between insects and plants: dynamic and
complex interactions that have coevolved over millions of years but act
in milliseconds. J Exp Bot 66: 455–465
Burkle L, Hibberd JM, Quick WP, Kuhn C, Hirner B, Frommer WB (1998)
The H+-sucrose cotransporter NtSUT1 is essential for sugar export from
tobacco leaves. Plant Physiol 118: 59–68
Caldana C, Degenkolbe T, Cuadros-Inostroza A, Klie S, Sulpice R,
Leisse A, Steinhauser D, Fernie AR, Willmitzer L, Hannah MA (2011)
High-density kinetic analysis of the metabolomic and transcriptomic
response of Arabidopsis to eight environmental conditions. Plant J 67:
869–884
Camañes G, Pastor V, Cerezo M, García-Agustín P, Flors Herrero V (2012)
A deletion in the nitrate high affinity transporter NRT2.1 alters metabolomic and transcriptomic responses to Pseudomonas syringae. Plant
Signal Behav 7: 619–622
Carolan JC, Fitzroy CI, Ashton PD, Douglas AE, Wilkinson TL (2009) The
secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9: 2457–2467
Castrillon-Arbelaez PA, Martinez-Gallardo N, Arnaut HA, Tiessen A,
Delano-Frier JP (2012) Metabolic and enzymatic changes associated
with carbon mobilization, utilization and replenishment triggered in
grain amaranth (Amaranthus cruentus) in response to partial defoliation
by mechanical injury or insect herbivory. BMC Plant Biol 12: 163
Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB
(2012) Sucrose efflux mediated by SWEET proteins as a key step for
phloem transport. Science 335: 207–211
Coppola V, Coppola M, Rocco M, Digilio MC, D’Ambrosio C, Renzone
G, Martinelli R, Scaloni A, Pennacchio F, Rao R, et al (2013) Transcriptomic and proteomic analysis of a compatible tomato-aphid interaction reveals a predominant salicylic acid-dependent plant response.
BMC Genomics 14: 515
Cortina C, Culiáñez-Macià FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169: 75–82
Coruzzi GM, Last RL (2000) Amino Acids. In RB Buchanan, W Gruissem, R
Jones, eds, Biochemistry and Molecular Biology of Plants. Am. Soc. Plant
Physiol. Wiley Press, Rockville, MD, pp 358–410
Degenkolbe T, Giavalisco P, Zuther E, Seiwert B, Hincha DK, Willmitzer
L (2012) Differential remodeling of the lipidome during cold acclimation
in natural accessions of Arabidopsis thaliana. Plant J 72: 972–982
Dinh ST, Baldwin IT, Galis I (2013) The HERBIVORE ELICITOR-REGULATED1 gene enhances abscisic acid levels and defenses against herbivores in Nicotiana attenuata plants. Plant Physiol 162: 2106–2124
Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui JC, Kusiak C,
Dinant S (2005) Systemic response to aphid infestation by Myzus persicae
in the phloem of Apium graveolens. Plant Mol Biol 57: 517–540
Dorschner KW, Ryan JD, Johnson RC, Eikenbary RD (1987) Modification of host nitrogen levels by the greenbug (Homoptera: Aphididae):
Its role in resistance of winter wheat to aphids. Environ Entomol 16:
1007–1011
Duceppe MO, Cloutier C, Michaud D (2012) Wounding, insect chewing
and phloem sap feeding differentially alter the leaf proteome of potato,
Solanum tuberosum L. Proteome Sci 10: 73
Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via
signal transduction pathways involving protein phosphorylation. Plant Cell
9: 1825–1841
1496
Plant Physiol. Vol. 169, 2015
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Herbivory Effects on Primary Metabolism
Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a
Myzus persicae (green peach aphid) salivary effector protein. Mol Plant
Microbe Interact 27: 747–756
Ferrieri AP, Appel H, Ferrieri RA, Schultz JC (2012) Novel application of
2-[(18)F]fluoro-2-deoxy-D-glucose to study plant defenses. Nucl Med
Biol 39: 1152–1160
Fox LR (1981) Defense and dynamics in plant-herbivore systems. Am Zool
21: 853–864
Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense
priming against herbivores: getting ready for a different battle. Plant
Physiol 146: 818–824
Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against
insect herbivores. Int J Mol Sci 14: 10242–10297
Giri AP, Wünsche H, Mitra S, Zavala JA, Muck A, Svatos A, Baldwin
IT (2006) Molecular interactions between the specialist herbivore
Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuate: VII. Changes in the plant’s proteome. Plant Physiol 142:
1621–1641
Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke M, Bullock
JM, Harvey JA (2008) Genetic variation in defense chemistry in wild
cabbages affects herbivores and their endoparasitoids. Ecology 89: 1616–
1626
Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR (2000) Genetic
evidence for the in planta role of phloem-specific plasma membrane
sucrose transporters. Proc Natl Acad Sci USA 97: 13979–13984
Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus
JM, Rentsch D (2005) The AtProT family: compatible solute transporters
with similar substrate specificity but differential expression patterns.
Plant Physiol 137: 117–126
Gutsche A, Heng-Moss T, Sarath G, Twigg P, Xia Y, Lu G, Mornhinweg D
(2009) Gene expression profiling of tolerant barley in response to Diuraphis noxia (Hemiptera: Aphididae) feeding. Bull Entomol Res 99: 163–
173
Halitschke R, Hamilton JG, Kessler A (2011) Herbivore-specific elicitation
of photosynthesis by mirid bug salivary secretions in the wild tobacco
Nicotiana attenuata. New Phytol 191: 528–535
Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57: 303–333
Harmel N, Létocart E, Cherqui A, Giordanengo P, Mazzucchelli G,
Guillonneau F, De Pauw E, Haubruge E, Francis F (2008) Identification
of aphid salivary proteins: a proteomic investigation of Myzus persicae.
Insect Mol Biol 17: 165–174
Hartmann T, Ober D (2000) Biosynthesis and metabolism of pyrrolizidine
alkaloids in plants and specialized insect herbivores. Biosynthesis 209:
207–243
Heil M (2009) Damaged-self recognition in plant herbivore defence. Trends
Plant Sci 14: 356–363
Hodge S, Ward JL, Beale MH, Bennett M, Mansfield JW, Powell G (2013)
Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237: 1057–1064
Holland JN, Cheng WX, Crossley DA (1996) Herbivore-induced changes in
plant carbon allocation: Assessment of below-ground C fluxes using
carbon-14. Oecologia 107: 87–94
Korpita T, Gomez S, Orians CM (2014) Cues from a specialist herbivore
increase tolerance to defoliation in tomato. Funct Ecol 28: 395–401
Koyama Y, Yao I, Akimoto SÄ (2004) Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall
formation. Entomol Exp Appl 113: 35–44
Lawrence SD, Novak NG, Ju CJ, Cooke JE (2008) Potato, Solanum tuberosum, defense against Colorado potato beetle, Leptinotarsa decemlineata
(Say): microarray gene expression profiling of potato by Colorado potato beetle regurgitant treatment of wounded leaves. J Chem Ecol 34:
1013–1025
Lee B, Lee S, Ryu CM (2012) Foliar aphid feeding recruits rhizosphere
bacteria and primes plant immunity against pathogenic and nonpathogenic bacteria in pepper. Ann Bot (Lond) 110: 281–290
Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis.
Plant Physiol 143: 784–800
Lu J, Robert CA, Riemann M, Cosme M, Mène-Saffrané L, Massana J,
Stout MJ, Lou Y, Gershenzon J, Erb M (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol 167: 1100–1116
Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose
metabolism in plants. Plant J 79: 544–567
Machado RA, Arce CC, Ferrieri AP, Baldwin IT, Erb M (2015) Jasmonatedependent depletion of soluble sugars compromises plant resistance to
Manduca sexta. New Phytol 207: 91–105
Machado RA, Ferrieri AP, Robert CA, Glauser G, Kallenbach M, Baldwin
IT, Erb M (2013) Leaf-herbivore attack reduces carbon reserves and
regrowth from the roots via jasmonate and auxin signaling. New Phytol
200: 1234–1246
Marti G, Erb M, Boccard J, Glauser G, Doyen GR, Villard N, Robert CA,
Turlings TC, Rudaz S, Wolfender JL (2013) Metabolomics reveals
herbivore-induced metabolites of resistance and susceptibility in maize
leaves and roots. Plant Cell Environ 36: 621–639
Massad TJ (2013) Ontogenetic differences of herbivory on woody and
herbaceous plants: a meta-analysis demonstrating unique effects of
herbivory on the young and the old, the slow and the fast. Oecologia
172: 1–10
Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling
pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:
1149–1162
Meyer A, Eskandari S, Grallath S, Rentsch D (2006) AtGAT1, a high affinity transporter for gamma-aminobutyric acid in Arabidopsis thaliana. J
Biol Chem 281: 7197–7204
Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees:
ecophysiological relevance in a changing world. Tree Physiol 30: 1083–
1095
Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical
aspects. Annu Rev Plant Biol 63: 431–450
Moreno A, Garzo E, Fernandez-Mata G, Kassem M, Aranda MA, Fereres
A (2011) Aphids secrete watery saliva into plant tissues from the onset of
stylet penetration. Entomol Exp Appl 139: 145–153
Nambara E, Kawaide H, Kamiya Y, Naito S (1998) Characterization of an
Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABAdependent and ABA-independent accumulation of free amino acids
during dehydration. Plant Cell Physiol 39: 853–858
Ohyama A, Hirai M (1999) Introducing an antisense gene for a cell-wallbound acid invertase to tomato (Lycopersicon esculentum) plants reduces
carbohydrate content in leaves and fertility. Plant Biotechnol 16: 147–151
Oikawa A, Ishihara A, Tanaka C, Mori N, Tsuda M, Iwamura H (2004)
Accumulation of HDMBOA-Glc is induced by biotic stresses prior to the
release of MBOA in maize leaves. Phytochemistry 65: 2995–3001
Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass
ADM (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiol 140:
1036–1046
Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167: 1–9
Rao SA, Carolan JC, Wilkinson TL (2013) Proteomic profiling of cereal
aphid saliva reveals both ubiquitous and adaptive secreted proteins.
PLoS One 8: e57413, doi 57410.51371/journal.pone.0057413
Reymond P, Bodenhausen N, Van Poecke RM, Krishnamurthy V, Dicke
M, Farmer EE (2004) A conserved transcript pattern in response to a
specialist and a generalist herbivore. Plant Cell 16: 3132–3147
Robert CAM, Ferrieri RA, Schirmer S, Babst BA, Schueller MJ, Machado
RAR, Arce CCM, Hibbard BE, Gershenzon J, Turlings TCJ, et al
(2014) Induced carbon reallocation and compensatory growth as root
herbivore tolerance mechanisms. Plant Cell Environ 37: 2613–2622
Ryan CA (2000) The systemin signaling pathway: differential activation of
plant defensive genes. Biochim Biophys Acta 1477: 112–121
Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host
plants by aphids - a comparison of three aphid species on grasses. J
Insect Physiol 46: 33–40
Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D
(2006) A trehalose metabolic enzyme controls inflorescence architecture
in maize. Nature 441: 227–230
Schmidt L, Schurr U, Röse US (2009) Local and systemic effects of two
herbivores with different feeding mechanisms on primary metabolism of
cotton leaves. Plant Cell Environ 32: 893–903
Schultz JC, Appel HM, Ferrieri AP, Arnold TM (2013) Flexible resource
allocation during plant defense responses. Front Plant Sci 4: 324
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure
primary metabolism? Plant Physiol 146: 845–851
Plant Physiol. Vol. 169, 2015
1497
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
Zhou et al.
Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U,
Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci USA 103: 12935–
12940
Singh V, Louis J, Ayre BG, Reese JC, Pegadaraju V, Shah J (2011)
TREHALOSE PHOSPHATE SYNTHASE11-dependent trehalose
metabolism promotes Arabidopsis thaliana defense against the
phloem-feeding insect Myzus persicae. Plant J 67: 94–104; erratum
Singh V, Louis J, Ayre BG, Reese JC, Pegadaraju V, Shah J (2011)
Plant J 68: 938
Singh V, Shah J (2012) Tomato responds to green peach aphid infestation
with the activation of trehalose metabolism and starch accumulation.
Plant Signal Behav 7: 605–607
Sotelo P, Pérez E, Najar-Rodriguez A, Walter A, Dorn S (2014) Brassica
plant responses to mild herbivore stress elicited by two specialist insects
from different feeding guilds. J Chem Ecol 40: 136–149
Steinbrenner AD, Gómez S, Osorio S, Fernie AR, Orians CM (2011)
Herbivore-induced changes in tomato (Solanum lycopersicum) primary
metabolism: a whole plant perspective. J Chem Ecol 37: 1294–1303
Sturm A, Chrispeels MJ (1990) cDNA cloning of carrot extracellular
b-fructosidase and its expression in response to wounding and bacterial
infection. Plant Cell 2: 1107–1119
Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are
crucial for development, growth and carbon partitioning. Trends Plant
Sci 4: 401–407
Tao L, Hunter MD (2013) Allocation of resources away from sites of herbivory under simultaneous attack by aboveground and belowground
herbivores in the common milkweed, Asclepias syriaca. Arthropod-Plant
Interact 7: 217–224
Tjallingii WF, Esch TH (1993) Fine structure of aphid stylet routes in plant
tissues in correlation with EPG signals. Physiol Entomol 18: 317–328
Usadel B, Nagel A, Steinhauser D, Gibon Y, Bläsing OE, Redestig H,
Sreenivasulu N, Krall L, Hannah MA, Poree F, et al (2006) PageMan:
an interactive ontology tool to generate, display, and annotate overview
graphs for profiling experiments. BMC Bioinformatics 7: 535
Velikova V, Salerno G, Frati F, Peri E, Conti E, Colazza S, Loreto F (2010)
Influence of feeding and oviposition by phytophagous pentatomids on
photosynthesis of herbaceous plants. J Chem Ecol 36: 629–641
Voelckel C, Weisser WW, Baldwin IT (2004) An analysis of plant-aphid
interactions by different microarray hybridization strategies. Mol Ecol
13: 3187–3195
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal
transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot (Lond)
111: 1021–1058
Wei Z, Hu W, Lin Q, Cheng X, Tong M, Zhu L, Chen R, He G (2009)
Understanding rice plant resistance to the Brown Planthopper (Nilaparvata lugens): a proteomic approach. Proteomics 9: 2798–2808
Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum
MR, de Lucia EH (2002) Impact of folivory on photosynthesis is greater than
the sum of its holes. Proc Natl Acad Sci USA 99: 1088–1091
Zhang L, Cohn NS, Mitchell JP (1996) Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant
Physiol 112: 1111–1117
Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional
regulation of sorghum defense determinants against a phloem-feeding
aphid. Plant Physiol 134: 420–431
Ziegler J, Facchini PJ (2008) Alkaloid biosynthesis: metabolism and trafficking. Annu Rev Plant Biol 59: 735–769
Zúñiga GE, Argandoña VH, Niemeyer HM, Corcuera LJ (1983) Hydroxamic acid content in wild and cultivated Gramineae. Phytochemistry 22: 2665–2668
1498
Plant Physiol. Vol. 169, 2015
Downloaded from on June 14, 2017 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.