Insect Science (2013) 20, 286–296, DOI 10.1111/1744-7917.12004
INVITED REVIEW
Emerging role of roots in plant responses to aboveground
insect herbivory
Vamsi J. Nalam1 , Jyoti Shah2 and Punya Nachappa1
1 Department
of Biology, Indiana University-Purdue University, Fort Wayne, Indiana and
for Plant Lipid Research, University of North Texas, Denton, Texas, United States
2 Department
of Biological Sciences and Center
Abstract Plants have evolved complex biochemical mechanisms to counter threats from
insect herbivory. Recent research has revealed an important role of roots in plant responses
to above ground herbivory (AGH). The involvement of roots is integral to plant resistance
and tolerance mechanisms. Roots not only play an active role in plant defenses by acting
as sites for biosynthesis of various toxins and but also contribute to tolerance by storing
photoassimilates to enable future regrowth. The interaction of roots with beneficial soilborne microorganisms also influences the outcome of the interaction between plant and
insect herbivores. Shoot-to-root communication signals are critical for plant response to
AGH. A better understanding of the role of roots in plant response to AGH is essential in
order to develop a comprehensive picture of plant-insect interactions. Here, we summarize
the current status of research on the role of roots in plant response to AGH and also discuss
possible signals involved in shoot-to-root communication.
Key words jasmonic acid, secondary metabolites, shoot-to-root communication, soilborne microorganisms
Introduction
Current understanding of plant–insect interactions is
drawn largely from the response of plant foliar tissue to
insect herbivory (Howe & Jander, 2008; Wu & Baldwin,
2010). Plants combat insect feeding using both constitutive defenses and defenses that are induced only in response to attack (Karban & Baldwin, 1997). Inducible
defenses can be classified as either direct or indirect. Direct defenses affect the biology of the attacker directly,
whereas indirect defenses, which are more relevant in defense against herbivores, affect the herbivore by attracting
its natural enemies (Karban & Baldwin, 1997). Inducible
defenses offer several advantages compared to constitutive defenses, such as reduced cost and increased vari-
Correspondence: Punya Nachappa, Department of Biology, Indiana University-Purdue University, Fort Wayne, Indiana
46805, USA. email: [email protected]
ability in the plant phenotype, resulting in increased efficiency of the inducible defense (Karban & Baldwin, 1997;
Zangerl, 2002; Cipollini et al., 2003). Given that all plant
tissues (leaves, roots, stems, flowers, and fruits) are consumed by insect herbivores, our understanding of plant–
insect interactions is skewed. In several plant species, the
biomass of roots is far greater than that of the shoots;
hence, roots provide an incredibly attractive resource to
various soil-dwelling insect pests. And indeed, herbivory
of roots by belowground herbivores (BGH) results in substantial damage to plant roots and significantly impacts
overall plant fitness (Blossey & Hunt-Joshi, 2003). Studies examining plant responses to BGH have revealed that
similar to aboveground responses, roots also employ direct and indirect induced defenses (Rasmann & Agrawal,
2008; van Dam, 2009; Erb et al., 2012). The activation
of defenses due to insect herbivory either belowground
or aboveground often results in the induction of defenses
systemically throughout the plant. Systemic defenses can
thereby influence the outcome of not only plant–insect
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Zoology, Chinese Academy of Sciences
Root responses to aboveground herbivory
interactions but also link the belowground and aboveground biota (reviewed in Bezemer & van Dam, 2005;
Johnson et al., 2008).
In terrestrial plants, roots serve many different purposes
including, absorption of water and nutrients, anchoring
the plant to soil, and storage of photoassimilates (Öpik
et al., 2005). Roots are also increasingly being recognized as active participants in plant responses to AGH
(Erb, 2012). The earliest report that root-derived secondary metabolites are involved in plant defenses against
aboveground herbivores (AGH) was made as early as 1941
when it was shown that the alkaloid nicotine was primarily
synthesized in the roots of tobacco plants (Dawson, 1941).
Of late, there has been a surge of interest in elucidating
the contribution of roots in shoot defenses against insect
herbivores (Kaplan et al., 2008b; Rasmann & Agrawal,
2008; Erb et al., 2009b; Erb et al., 2012). For example, a
recent study shows that root-derived oxylipins contribute
to host susceptibility by promoting population growth rate
of an aboveground insect herbivore. Feeding by the generalist aphid (Myzus persicae) resulted in the induction
of expression of a 9-lipoxygenase encoding LIPOXYGENASE5 (LOX5) gene and a corresponding increase in
the LOX5-synthesized oxylipins, 9-hydroperoxy, and 9hydroxy-fatty acids only in the roots of aphid-infested
Arabidopsis plants. These oxylipins were translocated to
the shoot, where they promoted aphid feeding, body water
content and fecundity (Nalam et al., 2012). Studies such as
these and others highlight the need to include roots to develop a better understanding of plant–insect interactions.
In this review, we will focus on recent advances in understanding (i) the contribution of roots to plant defenses
against AGH and (ii) the identity of potential signal(s)
involved in integrating shoot and root responses to AGH.
Contribution of roots to defense against AGH
Root-derived defenses
Plants synthesize a variety of secondary metabolites to
withstand insect attack. While some of these secondary
metabolites are toxic to the herbivore, others reduce
the palatability of the plant to the insect. Alkaloids and
terpenoids, which are among the most metabolically diverse classes of secondary metabolites, represent a major
class of insecticidal metabolites (Facchini, 2001; Aharoni
et al., 2006; Ziegler & Facchini, 2008). Others include
glucosinolates, saponins, tannins, furanocoumarins, and
cyanogenic glycosides (Wu & Baldwin, 2010; Yamane
et al., 2010). In addition to secondary metabolites, a
broad array of proteins that are induced in response to
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herbivory are also involved in plant defense responses
(Zhu-Salzman & Liu, 2011). The elucidation of the
biosynthetic pathways for some of these metabolites and
induced proteins highlight roots as an important site of
synthesis (Table 1; reviewed in van der Putten et al.,
2001; Rasmann & Agrawal, 2008; Erb et al., 2009b; Erb,
2012).
The most well studied insecticidal secondary metabolite
is nicotine, a neuroactive compound synthesized in large
amounts by plants of the genus Nicotiana. Nicotine is synthesized in roots from where it is translocated to shoots
and stored in vacuoles of leaf cells, thus providing a constitutive defense against insects (Dawson, 1941; Morita
et al., 2009). In response to herbivory or methyl jasmonate
treatment, the accumulation of nicotine increased in roots
and lead to increased concentrations in shoots and thus
enhanced protection against insect herbivory (Baldwin
et al., 1994). The synthesis of alkaloids in roots is not
limited to plants of the genus Nicotiana. A similar pattern
is observed for the synthesis of tropane alkaloids that may
be involved in leaf defense in the Solanaceae family of
plants (Ziegler & Facchini, 2008).
In some instances, the precursors for secondary metabolites that participate in shoot defense are synthesized
in roots and then transported to shoots where they undergo further modifications. For example, the precursor
for pyrrolizidine alkaloids, senecionine N-oxide is produced in the roots and then translocated throughout the
plant tissue (Toppel et al., 1987; Hartmann & Ober, 2000).
A second example is umelliferone, which is synthesized
in significant quantities in roots of the bishopweed (Ammi
majus) (Sidwa-Gorycka et al., 2003). Umelliferone is the
precursor for several furanocoumarins that act as feeding
deterrents for insects and have antifungal and antibacterial
properties (Berenbaum, 1978; Yamane et al., 2010).
Another class of compounds, the glucosinolates found
mainly in plants belonging to Brassicaceae, function in
defense against herbivores and pathogens. In black mustard (Brassica nigra), foliar herbivory by the larvae of
cabbage butterfly (Pieris brassicae) resulted in the accumulation of higher levels of indole glucosinolates in
the roots (Soler et al., 2009). An increase in the levels
of indole glucosinolates was also observed in roots of
field mustard (Brassica campestris), when shoots were
treated with the defense elicitors salicylic acid (SA) and
jasmonic acid (JA; Ludwig-Müller et al., 1997). However,
since glucosinolates can be readily loaded and transported
through the phloem (Chen et al., 2001), it is as yet unclear
whether these compounds are synthesized exclusively in
the roots or whether they are synthesized in infested shoots
and then transported systemically throughout the plant including the root.
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Table 1 Insecticidal factors synthesized in roots in response to AGH.
Plant
Induction by
Altered root defense
Increase/
decrease of
root defense
Influence
on
AGH
Brassica nigra
Zea mays
Arabidopsis thaliana
Senecio jacobea
Gossypium herbaceum
Brassica campestris
Pieris brassicae
Spodoptera frugiperda
Myzus persicae
Mamestra brassicae
Spodoptera exigua
JA, SA
Indole glucosinolates
Mir1-CP
9-LOX derived oxylipins
Pyrrolizidone alkaloid
Terpenoid aldehydes
Indole glucosinolates
Increase
Increase
Increase
Decrease
Decrease
Increase
Yes
Yes
Yes
Yes
NA
NA
Abelmoschus esculentus
Nicotiana attenuata
SA
MJ, MD
Increase
Increase
NA
NA
Nicotiana sylvestris
Cynoglossum offininale
MD
MD
PR proteins
Trypsin proteinase
inhibitors
Nicotine
Pyrrolizidone alkaloid
Increase
Increase
NA
NA
Secale cereale
MD
Hydroxamic acids
Increase
NA
Reference
Soler et al., 2009
Lopez et al., 2007
Nalam et al., 2012
Hol et al., 2004
Bezemer et al., 2004
Ludwig-Müller et al.,
1997
Nandi et al., 2003
van Dam et al., 2001
Baldwin et al., 1994
van Dam & Vrieling,
1994
Collantes et al., 1999
MD, mechanical damage; MJ, methyl jasmonate; SA, salicylic acid; JA, jasmonic acid; PR, pathogenesis proteins; NA, not applicable.
Arthropod-inducible proteins (AIPs) also provide a
broad spectrum of resistance in several plant species by
providing postingesting plant defenses (Zhu-Salzman &
Liu, 2011). In the case of one such AIP, the levels of Maize
insect resistance 1-cysteine protease (Mir1-CP) increased
in the leaf tissue of a resistant maize (Zea mays) genotype (Mp708) in response to foliar herbivory by the larvae
of fall armyworm (Spodoptera frugiperda) (Lopez et al.,
2007). Mir1-CP accumulated in root xylem tissue 24 h
after foliar feeding and was also found in the xylem tissue
of leaves. Furthermore, removal of roots prior to larval
feeding prevented the accumulation of Mir1-Cp in leaves,
suggesting that the protein is first synthesized in the roots
and transported to the leaf tissue through the vasculature.
The synthesis of defensive factors by roots in response
to foliar herbivory is not a universal phenomenon. In certain instances, there is a reduction in the levels of plant
toxins that are normally synthesized in roots. For example, the levels of pyrrolizide alkaloids, which are produced in roots (Toppel et al., 1987) decreased in the roots
of ragwort (Senecio jacobea) in response to AGH by the
cabbage moth (Mamestra brassicae) (Hol et al., 2004).
In other cases, defensive compounds normally induced in
roots in response to BGH are not induced during AGH. For
instance, belowground herbivory by wireworms (Agriotes
lineatus) resulted in increased accumulation of terpenoids
in both roots and shoots. However, a similar increase in
terpenoid content was observed only in shoots during
aboveground herbivory by beet armyworm (Spodoptera
exigua) (Bezemer et al., 2003, 2004). This observation
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suggests that although BGH may change the level and
distribution of defensive secondary metabolites, the same
may not hold true for all cases of AGH. One possibility to explain the suppression of root-induced defense in
these cases is that herbivores themselves manipulate host
responses to suit their needs by either suppressing host
defenses or activating alternate mechanisms that promote
the AGH.
Roots limit resource availability to AGH
A major function of plant roots in many species is
the storage of food and nutrients. Roots can potentially
contribute to the plants ability to tolerate AGH by acting as storage sites for photoassimilates. For instance,
in response to AGH, photoassimilates are translocated to
the roots making them inaccessible to the herbivore. The
reallocation of stored photoassimilates aboveground can
then occur after AGH pressure has reduced, thus enabling
aboveground growth and reproduction to resume. There
are several lines of evidence that indicate that foliar herbivory, shoot hormone applications or mechanical damage can result in reallocation to storage tissue (reviewed
in Orians et al., 2011). In maize for instance, foliar insect herbivory by grasshoppers resulted in the mobilization of photoassimilates to roots (Holland et al., 1996). A
similar process occurs in Nicotiana tabaccum after AGH
by tobacco hornworm (Manduca sexta) larvae (Kaplan
et al., 2008a). In Populus, treatment of the shoot with the
defense hormone JA or AGH by Gypsy moth (Lymantria
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Root responses to aboveground herbivory
dispar) larvae resulted in the increased transport of leaf
photosynthate to the stems and roots within hours of treatment (Babst et al., 2005; Babst et al., 2008). In tomato
(Solanum lycopersicum), AGH by tobacco hornworm
(M. sexta) resulted in a significant increase in the concentrations of various sugars, sugar alcohols and organic
acids in the roots (Steinbrenner et al., 2011).
To achieve an increase in the transport of photosynthate
to the roots, plants can either increase loading into phloem
and/or increase unloading into the roots (Turgeon & Wolf,
2009). The increased carbon sink strength of the roots can
be achieved in part by an increase in the activity of invertases, a sugar-cleaving enzyme (Roitsch & González,
2004). Indeed, an increase in invertase activity was found
in roots in response to AGH by the tobacco hornworm
(Kaplan et al., 2008a). Insect-derived elicitors present in
the regurgitant of chewing insects are also capable of inducing resource reallocation to roots (Schwachtje et al.,
2006). The application of M. sexta regurgitant to leaves
of tomato plants resulted in increased allocation of carbon to the roots (Gómez et al., 2012). This herbivoreinduced resource-reallocation is thought to be regulated
by SNF1-related kinases, which play a central role in cell
energy metabolism (Halford & Hey, 2009). In Nicotiana
attenuata, the transcript levels of SNF1-related kinases
were rapidly downregulated in leaves treated with insectderived elicitors resulting in increased assimilates transported to roots (Schwachtje et al., 2006). Although the
regulatory mechanisms that initiate and control reallocation are not fully understood (Erb et al., 2009a; Erb, 2012),
it is clear that roots play an active role in limiting resource
availability to AGH.
Interaction of roots with beneficial soil-microbes
influences AGH
The interaction of roots with beneficial soil-borne microbes also influences the outcome of the aboveground
interactions between the plant and herbivore. The association of roots with certain plant growth-promoting rhizobacteria and mycorrhizal fungi not only results in the
promotion of plant growth but also the induction of resistance against a wide variety of AGH and pathogens. This
phenomenon termed induced systemic resistance (ISR)
provides protection against a wide range of diseases (van
Oosten et al., 2008; Doornbos et al., 2010). Although, several different beneficial soil-borne microorganisms can
induce ISR, the mechanism of induction of ISR follows
similar patterns and is mediated by JA or jasmonic ethylene (ET) sensitive pathways which are commonly involved in plant defense responses (van Oosten et al.,
2008; Doornbos et al., 2010). Beneficial soil-borne mi
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croorganisms can therefore indirectly influence with outcome of plant interaction with an AGH via plant-mediated
mechanisms. There are examples of both positive and
negative effects of such interactions (reviewed in Pineda
et al., 2010). For instance, the association of Acremonium alternatum Gams (Ascomycotina), an endophytic
fungus with the roots of cabbage (Brassica oleracea) resulted in increased mortality and reduced growth rate of
the surviving larvae of the diamond back moth (Plutella
xylostella) (Raps & Vidal, 1998). The association of a
plant-growth promoting rhizobacteria, Bacillus amyloquefaciens, with tomato or sweet pepper (Capsicum annuum) roots conferred protection against phloem-feeding
insects, the green peach aphid (M. persicae) and silverleaf whiteflies (Bemisia argentifolii) (Murphy et al., 2000;
Herman et al., 2008). In these cases it is plausible that root
association with the beneficial soil-microbes resulted in
the activation of ISR. In a more recent study, the role
of ISR was demonstrated in the association of Bacillus subtillis with the roots of tomato plants, which retarded silverleaf whitefly development (Valenzuela-Soto
et al., 2010). By comparison, the association of Rhizobium
leguminosarum with white clover (Trifolium repens) resulted in a positive effect on the Egyptian cotton leafworm
(Spodoptera littoralis) and a neutral effect on the green
peach aphid (Kempel et al., 2009). The species or the
strain of the beneficial soil-borne microorganisms also
impacts the outcome of plant interaction with a specific
AGH. For instance, in rice (Oryza sativa) a combination of
different Pseudomonas fluorescens strains had a stronger
impact as compared to the influence of the strains individually (Saravanakumar et al., 2007).
The impact of root-colonizing microbes on AGH can
also be influenced by the degree of specialization of the
herbivore. Studies on Arabidopsis show that association of
roots with P. fluorescens results in the activation of JA/ET
responsive defense pathways which do not affect feeding by the specialist caterpillar, Pieris rapae. By contrast,
activation of the same plant defenses negatively affected
feeding by the generalist herbivore S. exigua (van Oosten
et al., 2008). Another factor that determines the effectiveness of root-colonizing microbe induced defenses is
the insect feeding guilds. Chewing insects encounter several secondary metabolites when they feed on plant tissue.
Piercing-sucking insects on the other hand avoid contact
with these compounds by inserting their slender needle
like stylets into the phloem sieve elements. Therefore, the
degree of specialization and the feeding guild should be
taken into account while considering the impact of beneficial soil-microbes on the aboveground herbivore.
In order to recruit beneficial soil-dwelling organisms,
plant roots produce copious amounts of exudates. The
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production of root exudates can therefore indirectly impact the outcome of plant interaction with the AGH. Root
exudates comprise of an enormous range of small molecular weight compounds and the interactions mediated by
these exudates can be either positive or negative (reviewed
in Walker et al., 2003; Bais et al., 2006; Hiltpold et al.,
2011). For instance, a large number of soil organisms rely
on root exudates as a major source of carbon (Walker
et al., 2003; Bais et al., 2006). On the other hand, root
exudates also contain compounds with antimicrobial, nematicidal, or insecticidal properties. Several studies have
shown that AGH influence soil microbial communities
(Hamilton et al., 2008; van Dam, 2009). For example, silverleaf whitefly and green peach aphid feeding on pepper
plants resulted in a significant increase in population density of several beneficial rhizobacteria (Yang et al., 2011;
Lee et al., 2012). Whether root association with these
rhizobacteria results in ISR against the phloem-feeding
insects is unknown. It is however plausible to conclude
from these and other studies (Murphy et al., 2000; Herman
et al., 2008) that recruitment of beneficial rhizobacteria
can have a negative impact on the AGH. These studies
provide new insights into the tritrophic interactions between the AGH, the plant, and beneficial soil microbes.
Herbivory induced root exudation can also result in unique
soil legacy effects. For instance, AGH by M. brassicae on
ragwort plants resulted in the production of root exudates
that altered the composition of soil fungi. Plants grown
subsequently in the same soil displayed increased biomass
and higher content of pyrrolizidine alkaloids that enabled
them to counter future threats by AGH (Kostenko et al.,
2012).
Roots are also involved in interplant communication
via the interaction with the mycelia of mycorrhizal fungi.
Mycorrhizal mycelia can interconnect roots of multiple
plants to form common mycorrhizal netwroks (CMNs;
Selosse et al., 2006). CMNs are known to act as conduits
for the transfer of water and also nutrients such as nitrogen, phosphorous and other elements from one plant
root to another (He et al., 2003; Meding & Zasoski, 2008;
Mikkelsen et al., 2008). Exchange between plants connected by CMNs is not only limited to transfer of water
and nutrients but also to the exchange of signals. For instance, CMNs mediate plant to plant communication between healthy and pathogen-infected tomato plants (Song
et al., 2010). Pathogen-infected tomato plants transmit
a defence signal to healthy plants where the expression
of defence genes and activity is induced resulting in increased resistance to future attacks (Song et al., 2010).
Although, a similar study with insects is lacking it is plausible to hypothesize that a similar exchange of defence signals between plants connected physically by CMNs also
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occurs during insect herbivory. The interaction of plant
roots with mycorrhiza forming CMNs could therefore act
as defence networks in plant communities.
Root-colonizing microbes also contribute to indirect defenses against AGH by stimulating shoots to emit volatile
organic compounds that attract natural enemies of AGH
(Guerrieri et al., 2004). For instance, the rate of parasitism
of the Bird cherry oat aphid, Rhopalosiphum padi, by the
parasitic wasp, Aphidius rhopalosiphi, increased by 140%
on timothy grass (Phleum pratense) that were associated
with arbuscular mycorrhizal fungi (Glomus intraradices)
(Hempel et al., 2009). Additionally, belowground interaction of plants with root-colonizing microbes not only
promotes plant growth but also has a beneficial effect on
the nutritional status of the plant (Pineda et al., 2010).
Root associations with soil-dwelling microbes enable the
increased uptake of not only water but also a variety of nutrients such as nitrogen and phosphorus. Further, some microbes enhanced photosynthesis by modulating sugar and
ABA signaling, and also synthesized plant growth promoting hormones (van Loon, 2007; Zhang et al., 2008).
In general, increased content of nitrogen and other limiting nutrients in plant tissues and phloem sap benefits both
chewing and phloem-sap feeding insects (Schoonhoven
et al., 2005). The final result of root-colonizing microbes
on AGH, therefore, depends on a fine balance between the
positive effect on AGH due to enhanced nutritional status
of the plant and negative effect on AGH due to promotion
of induced resistance and indirect defenses in shoots.
Signal(s) involved in shoot-to-root communication
The involvement of roots in defense against AGH suggests communication by shoots with roots. Erb et al.
(2009b) suggested the presence of a shoot–root–shoot
loop in which signal(s) generated in response to AGH
spread systemically throughout the plant including the
roots. The translocation of the signal(s) to the roots results in the activation of root-based defenses, which then
directly or indirectly influence the AGH. Several classes
of compounds have the potential to act as signals. In order
to qualify as a defense signal however, the compound(s)
must be synthesized at the site of attack, from where it is
systemically translocated to induce defense responses.
Plant hormones such as JA and SA are critical signals
in plant defense regulatory networks that are involved
in long-distance signaling (Heil & Ton, 2008) and may
therefore play a critical role in shoot-to-root communication. JA and associated compounds termed jasmonates
are involved in long-distance wound signaling and are
considered to be central to governing plant responses to
chewing insects (Wu & Baldwin, 2010; Woldemariam
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Root responses to aboveground herbivory
et al., 2011). Furthermore, methyl jasmonate is readily
transported through the plants vasculature (Thorpe et al.,
2007). Support for the role of jasmonates as shoot-toroot signals comes from studies on diverse plant–insect
interactions. In Nicotiana sylvestris, JA concentrations increased locally within 30 min of wounding and in the roots
after 90 min resulting in the stimulation of nicotine synthesis (Baldwin et al., 1994; Winz & Baldwin, 2001). Foliar
treatment of N. sylvestris with methyl jasmonate resulted
in the upregulation of Putrescine N-methyltransferases,
the enzymes that catalyze the first committed step of nicotine biosynthesis (Shoji et al., 2000). In poplar, simulated
herbivory by the application of methyl jasmonate, or mechanical wounding, also resulted in the induction of a
poplar trypsin inhibitor (PtdT13), a marker for poplar defenses, in both the leaves and roots (Major & Constabel,
2007). In Brassica rapa, foliar application of methyl jasmonate resulted in an increase in glucosinolate levels in
the roots (Loivamäki et al., 2004). Furthermore, methyl
jasmonate treatment resulted in the accumulation of Mir1CP in maize leaves in a dose-dependent manner (Ankala
et al., 2009). Since Mir1-CP is synthesized exclusively
in the roots of maize plants, it is plausible that JA or its
conjugates function as long-distance signals to stimulate
Mir1-CP synthesis. Taken together, these results highlight
the importance of jasmonates as important shoot-to-root
signals during AGH by chewing insects.
The role of SA and its derivative methyl salicylate in
shoot-to-root communication is less clear. SA-mediated
defenses play an important role in locally expressed defenses and in the enhancement of resistance to secondary
infection in distal uninfected plant parts against biotrophic
pathogens. The crosstalk between the SA and JA pathways
is thought to modulate plant defense responses and limit
the expression of costly and ineffective defenses (Glazebrook, 2005). Although, SA-based defenses are normally
induced in response to pathogen attack, insect herbivory
can also result in an increase in the levels of endogenous
SA and/or the activation of SA-inducible genes (Moran &
Thompson, 2001; Heidel & Baldwin, 2004; Zarate et al.,
2007; Kanno et al., 2012). However, the lack of a negative
effect on herbivore performance due to the activation of
SA-mediated defenses (Moran & Thompson, 2001; Heidel & Baldwin, 2004; Zarate et al., 2007; Kanno et al.,
2012) raises the possibility of herbivore-mediated manipulation of plant defenses. Indeed, nymphs of silverleaf
whitefly induce SA-mediated defenses in order to suppress the more effective JA-mediated defenses (Zarate
et al., 2007). However, the role of methyl salicylate as a
signal molecule cannot be overlooked. Methyl salicylate
in addition to being readily transported in the phloem is
also volatile and is a key signaling molecule involved in
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plant-to-plant communication (Shulaev et al., 1997; Park
et al., 2007). Furthermore, methyl salicylate mediates resistance against certain insects by attracting their respective predators (van Poecke & Dicke, 2002). Therefore,
although SA and methyl salicylate may not be directly
involved in shoot-to-root communication, they can indirectly influence the plants response to insect herbivory by
modulating JA-mediated defenses.
There may be yet undiscovered molecules that are involved in shoot-to-root communication. In maize plants
infested with African cotton leafworm (S. littoralis), transcriptomic analyses revealed no overlap between the genes
induced in the shoots and the roots. Furthermore, although
JA and SA-mediated genes were induced in shoots in response to the AGH, the same set of genes were not induced
in the roots during AGH suggesting the presence of alternative shoot-to-root signals (Erb dissertation, University
of Neuchatel, 2009). In plants, small interfering RNA and
micro RNA play an important role in plant defense responses to AGH (reviewed in Padmanabhan et al., 2009).
For example, herbivory induced large-scale changes in the
small RNA transcriptome of N. attenuata (Pandey et al.,
2008). These small RNAs are thought to contribute to
plant defenses by playing a central role in coordinating
the large-scale transcriptional changes that occur in response to AGH. However, small RNAs are highly mobile
and are readily transported in the phloem tissue and thus
may have an important role in the regulation of systemic
defenses (Yoo et al., 2004; Kehr & Buhtz, 2008). Further
experimentation is however needed to confirm whether
small RNAs play a role in shoot-to-root communication
during AGH. The ability to simply and efficiently micrograft/graft various model species such as Arabidopsis,
N. attenuata, Nicotiana benthamiana, and tomato (Voinnet et al., 2000; Turnbull et al., 2002; Kimura & Sinha,
2008; Fragoso et al., 2011), can greatly aid in evaluating
the role of small RNAs and other candidates as potential
shoot to root signals. In addition to plant-derived factors
acting as shoot-to-root signals during AGH, insect elicitors may also function as signal molecules. Both chewing
and piercing/sucking insects release a large repertoire of
elicitors that are capable of inducing characteristic plant
defense responses (Wu & Baldwin, 2009; Hogenhout &
Bos, 2011). Insect elicitors have been identified in oral secretions, regurgitant, oviposition liquid, and saliva. Insect
elicitors are not only capable of inducing JA, ethylene,
and SA signaling but can also activate mitogen-activated
protein kinases, produce reactive oxygen species and induce calcium ion fluxes (Wu & Baldwin, 2009). However,
whether insect elicitors function as shoot-to-root signals
directly or indirectly through plant-mediated mechanisms
warrants further research.
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Conclusions
Roots are play an integral role in plant defense against
AGH by acting as sites of synthesis for various secondary
metabolites and proteins that either kill or deter the herbivore from feeding. Roots also contribute to plant defenses
indirectly by acting as temporary sites of storage for photoassimilates. Furthermore, the association of roots with
beneficial soil-borne microorganisms not only aids in the
growth and development of the plant, but also results in
the induction of ISR and aids in the recruitment of natural enemies of insect herbivores. There is increasing evidence that plant signaling molecules such as JA and/or its
derivatives, play an important role in shoot-to-root communication. There are several questions that are yet to be
answered. For example, does the root response to AGH
depend on the insect feeding guilds? Are the signal(s)
involved in shoot-to-root communication derived from
the plant and/or the insect? Do other phytohormones besides JA play a role in shoot-to-root communication? Does
AGH alter root physiology to suppress host defenses?
What is the metabolic cost to the plants due to root involvement in AGH defense? Answers to these and other
relevant questions will provide a better understanding of
the contribution of roots to plant defense against AGH.
Acknowledgments
We thank Dr. Keyan Zhu-Salzman for the invitation to
contribute to this special issue. We would like to thank Dr.
David C. Margolies for helpful comments on an earlier
version of this manuscript. Work in the Shah lab was supported by grants from the National Science Foundation
(Division of Integrative Organismal Systems-0919192
and Division of Molecular and Cellular Biosciences0920600). This work was supported by start-up funds
from Indiana University – Purdue University Fort Wayne
to Dr. Punya Nachappa.
Disclosure
The views presented in the review article represent the
author’s views. The authors have declared no competing
interests exist and are not involved in any potential conflicts of interest including financial interests, relationships
and affiliations.
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