Insect eggs suppress plant defence against chewing herbivores

Plants activate direct and indirect defences in response to insect egg deposition. However, whether eggs can manipulate plant defence is unknown. In Arabidopsis thaliana, oviposition by the butterfly Pieris brassicae triggers cellular and molecular changes that are similar to the changes caused by biotrophic pathogens. In the present study, we found that the plant defence signal salicylic acid (SA) accumulates at the site of oviposition. This is unexpected, as the SA pathway controls defence against fungal and bacterial pathogens and negatively interacts with the jasmonic acid (JA) pathway, which is crucial for the defence against herbivores. Application of P. brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of insect‐responsive genes after challenge with caterpillars, suggesting that egg‐derived elicitors suppress plant defence. Consequently, larval growth of the generalist herbivore S. littoralis, but not of the specialist P. brassicae, was significantly higher on plants treated with egg extract than on control plants. In contrast, suppression of gene induction and enhanced S. littoralis performance were not seen in the SA‐deficient mutant sid2‐1, indicating that it is SA that mediates this phenomenon. These data reveal an intriguing facet of the cross‐talk between SA and JA signalling pathways, and suggest that insects have evolved a way to suppress the induction of defence genes by laying eggs that release elicitors. We show here that egg‐induced SA accumulation negatively interferes with the JA pathway, and provides an advantage for generalist herbivores.     

Mechanisms of plant defense against insect herbivores

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.     

Nonglandular silicified trichomes are essential for rice defense against chewing herbivores

Interspecific New Rice for Africa (NERICA) varieties have been recently developed and used in Sub-Saharan Africa but herbivore resistance properties of these plants remain poorly understood. Here we report that, compared to a local Japanese cultivar Nipponbare, NERICA 1, 4 and 10 are significantly more damaged by insect herbivores in the paddy fields. In contrast to high levels of leaf damage from rice skippers and grasshoppers, constitutive and induced volatile organic compounds for indirect plant defense were higher or similar in NERICAs and Nipponbare. Accumulation of direct defense secondary metabolites, momilactones A and B, and p-coumaroylputrescine (CoP) was reduced in NERICAs, while feruloylputrescine accumulated at similar levels in all varieties. Finally, we found that Nipponbare leaves were covered with sharp nonglandular trichomes impregnated with silicon but comparable defense structures were virtually absent in herbivory-prone NERICA plants. As damage to the larval gut membranes by Nipponbare silicified trichomes that pass intact through the insect digestive system, occurs, and larval performance is enhanced by trichome removal from otherwise chemically defended Nipponbare plants, we propose that silicified trichomes work as an important defense mechanism of rice against chewing insect herbivores.     

植物诱导性直接防御

众所周知,植物对植食性昆虫危害的反应表现在3个方面：直接防御,间接防御,和耐害性。直接防御是指植物自身所具有的能影响寄主植物感虫性的所有特性。植物对昆虫危害的直接防御包括：限制食物供给,降低营养价值,减少偏嗜程度,破坏组织结构和抑制害虫代谢途径。目前已知的防御化合物主要包括植物次生代谢物质、昆虫消化酶（蛋白）抑制剂、蛋白酶、凝集素、氨基酸脱氨酶和氧化酶。植物在防御某种昆虫为害时多个因素往往具有累加效应或协同作用,并且对一种昆虫起主导作用的因素在防御另一种昆虫时可能仅仅起次要作用甚至根本不起作用。因此,对寄主植物基因表达、蛋白水平和活性以及代谢物含量在不同时空条件下进行广泛的定量和定性的高通量分析,不仅可以促进对植物直接防御机制的全面理解,而且有助于在农业生产中加快对作物抗性的特定靶标的鉴定。     

Indirect plant defense against insect herbivores: a review

Plants respond to herbivore attack by launching 2 types of defenses: direct defense and indirect defense. Direct defense includes all plant traits that increase the resistance of host plants to insect herbivores by affecting the physiology and/or behavior of the attackers. Indirect defense includes all traits that by themselves do not have significant direct impact on the attacking herbivores, but can attract natural enemies of the herbivores and thus reduce plant loss. When plants recognize herbivore‐associated elicitors, they produce and release a blend of volatiles that can attract predators, parasites, and other natural enemies. Known herbivore‐associated elicitors include fatty acid–amino acid conjugates, sulfur‐containing fatty acids, fragments of cell walls, peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous compounds, and indoles. In addition, constitive traits including extrafloral nectars, food bodies, and domatia can be further induced to higher levels and attract natural enemies as well as provide food and shelter to carnivores. A better understanding of indirect plant defense at global and componential levels via advanced high throughput technologies may lead to utilization of indirect defense in suppression of herbivore damage to plants.     

Inducible direct plant defense against insect herbivores: A review

Plants respond to insect herbivory with responses broadly known as direct defenses, indirect defenses, and tolerance. Direct defenses include all plant traits that affect susceptibility of host plants by themselves. Overall categories of direct plant defenses against insect herbivores include limiting food supply, reducing nutrient value, reducing preference, disrupting physical structures, and inhibiting chemical pathways of the attacking insect. Major known defense chemicals include plant secondary metabolites, protein inhibitors of insect digestive enzymes, proteases, lectins, amino acid deaminases and oxidases. Multiple factors with additive or even synergistic impact are usually involved in defense against a specific insect species, and factors of major importance to one insect species may only be of secondary importance or not effective at all against another insect species. Extensive qualitative and quantitative high throughput analyses of temporal and spatial variations in gene expression, protein level and activity, and metabolite concentration will accelerate not only the understanding of the overall mechanisms of direct defense, but also accelerate the identification of specific targets for enhancement of plant resistance for agriculture.     

Interactions between plants and herbivores: A review of plant defense

Ecologists have long ignored or underestimated the importance of plant–herbivore interactions owing to the diversities of herbivores, plant defensive strategies and ecological systems. In this review, we briefly discussed the categories of herbivores. Then we reviewed the major types of plant defenses against herbivores. Selective forces of herbivore pressures have led to the evolution of various defensive mechanisms in plants, which can be classified into (i) resistance traits that reduce the amount of damage received, including physical, chemical, and biotic traits; (ii) tolerance mechanisms that decrease the impact of herbivore damage, and (iii) escape strategies that reduce the probability of plants to be found by herbivores. These strategies have been studied at different levels from molecular genetics and genomics, to chemistry and physiology, to community and ecosystem ecology. We summarized the development of the methodology for studying plant defenses against herbivores. Particularly, 24 of those hypotheses and models, which are influential in the international community concerning the relationship between plants and herbivores, including the defensive mimicry hypothesis, the compensatory continuum hypothesis, the slow-growth-high-mortality hypothesis, etc, were introduced and grouped into four categories according to plant defense strategies in the present review. Finally, we also reviewed the research progress of plant–herbivore interactions in China, and discussed the perspectives of studies on plant–herbivore interactions.     

Stability of plant defense proteins in the gut of insect herbivores

Plant defense against insect herbivores is mediated in part by enzymes that impair digestive processes in the insect gut. Little is known about the evolutionary origins of these enzymes, their distribution in the plant kingdom, or the mechanisms by which they act in the protease-rich environment of the animal digestive tract. One example of such an enzyme is threonine (Thr) deaminase (TD), which in tomato (Solanum lycopersicum) serves a dual role in isoleucine (Ile) biosynthesis in planta and Thr degradation in the insect midgut. Here, we report that tomato uses different TD isozymes to perform these functions. Whereas the constitutively expressed TD1 has a housekeeping role in Ile biosynthesis, expression of TD2 in leaves is activated by the jasmonate signaling pathway in response to herbivore attack. Ingestion of tomato foliage by specialist (Manduca sexta) and generalist (Trichoplusia ni) insect herbivores triggered proteolytic removal of TD2's C-terminal regulatory domain, resulting in an enzyme that degrades Thr without being inhibited through feedback by Ile. This processed form (pTD2) of TD2 accumulated to high levels in the insect midgut and feces (frass). Purified pTD2 exhibited biochemical properties that are consistent with a postingestive role in defense. Shotgun proteomic analysis of frass from tomato-reared M. sexta identified pTD2 as one of the most abundant proteins in the excrement. Among the other tomato proteins identified were several jasmonate-inducible proteins that have a known or proposed role in anti-insect defense. Subtilisin-like proteases and other pathogenesis-related proteins, as well as proteins of unknown function, were also cataloged. We conclude that proteomic analysis of frass from insect herbivores provides a robust experimental approach to identify hyperstable plant proteins that serve important roles in defense.     

Constitutive plant toxins and their role in defense against herbivores and pathogens

Most recent investigations have focused on induced, rather than constitutive, plant defenses. Yet significant research has helped to illuminate some of the principal characteristics of constitutive defenses, including mechanisms of action and synergistic effects, as well as strategies used by herbivores and pathogens to circumvent them.     

Effects of different secondary metabolite profiles in plant defense syndromes on specialist and generalist herbivores

Plants defend themselves against herbivores not only by a single trait but also by diversified multiple defense strategies. It remains unclear how these multiple defense mechanisms are effectively organized against herbivores. In this study, we focused on Brassicaceae plants, which have one of the most diversified secondary metabolites, glucosinolates (GSLs), as a defense against herbivores. By analyzing various defense traits including GSL profiles among 12 species (11 genera) of Brassicaceae plants, it is revealed that their defense strategies can be divided into three categories as multiple defenses. The GSL profiles differed between these three categories: (i) high nutritional level with long‐chain aliphatic GSLs; (ii) low nutritional level and high physical defenses with short‐chain aliphatic GSLs; and (iii) high nutritional level and low defense. The feeding experiment was conducted using two types of herbivores, Pieris rapae (Lepidoptera: Pieridae) as a specialist herbivore and the Eri silkmoth Samia cynthia ricini (Lepidoptera: Saturniidae) as a generalist, to assess the ability of each plant in multiple defense strategy. It was observed that the Eri silkmoth's performance differed according to which defense strategy it was exposed to. However, the growth rate of P. rapae did not vary among the three categories of defense strategy. These results suggest that the diversified defense strategies of Brassicaceae species have evolved to cope with diversified herbivores.     

The role of jasmonic acid and ethylene crosstalk in direct defense of Nicotiana attenuata plants against chewing herbivores

We examined performance of herbivores on plants lacking either jasmonate (JA, asLOX3) or ethylene (ET, mETR1) signaling or both (mETR1asLOX3). Plant defenses against Manduca sexta caterpillars were strongly impaired in JA-deficient asLOX3 plants; however, making asLOX3 plants ethylene insensitive did not further increase the performance of the larvae on a mETR1asLOX3 genetic cross. This result demonstrates the dominant role of JA over ET in the regulation of plant defenses against herbivores. However, ET-insensitivity combined with otherwise normal levels of JA in mETR1 plants promoted faster caterpillar growth, which correlated with reduced accumulation of the alkaloidal direct defense nicotine in mETR1 compared to WT plants. Our data points to an important accessory function of ET in the activation of JA-regulated plant defenses against herbivores at the level of alkaloid biosynthesis in the roots and/or accumulation in the leaves.Key words: herbivory, jasmonic acid and ethylene crosstalk, Nicotiana attenuata, nicotine, trypsin proteinase inhibitors (TPIs)     

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores.Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied.We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses.Plant quality was quantified through oviposifion of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species.Spider-mite oviposifion data show that T.evansi could suppress an earlier induction of plant defenses by T.urticae,and T.urticae could induce defenses in plants previously attacked by T.evansi in 1 day.Longer attacks by the second species did not result in further changes in oviposifion.Proteinase inhibitor activity levels showed that T.evansi suppressed the high activity levels induced by T.urticae to constitutive levels in 1 day,and further suppressed activity to levels similar to those in plants attacked by T.evansi alone.Attacks by T.urticae induced proteinase inhibitor activity in plants previously attacked by T.evansi,eventually to similar levels as induced by T.urticae alone.Hence,plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance,but does affect proteinase inhibitor activity levels.Based on our results,we discuss the evolution of suppression of plant defenses.     

New evidence for a multi-functional role of herbivore-induced plant volatiles in defense against herbivores

A diverse, often species-specific, array of herbivore-induced plant volatiles (HIPVs) are commonly emitted from plants after herbivore attack. Although research in the last 3 decades indicates a multi-functional role of these HIPVs, the evolutionary rationale underpinning HIPV emissions remains an open question. Many studies have documented that HIPVs can attract natural enemies, and some studies indicate that neighboring plants may eavesdrop their undamaged neighbors and induce or prime their own defenses prior to herbivore attack. Both of these ecological roles for HIPVs are risky strategies for the emitting plant. In a recent paper, we reported that most branches within a blueberry bush share limited vascular connectivity, which restricts the systemic movement of internal signals. Blueberry branches circumvent this limitation by responding to HIPVs emitted from neighboring branches of the same plant: exposure to HIPVs increases levels of defensive signaling hormones, changes their defensive status, and makes undamaged branches more resistant to herbivores. Similar findings have been reported recently for sagebrush, poplar and lima beans, where intra-plant communication played a role in activating or priming defenses against herbivores. Thus, there is increasing evidence that intra-plant communication occurs in a wide range of taxonomically unrelated plant species. While the degree to which this phenomenon increases a plant’s fitness remains to be determined in most cases, we here argue that withinplant signaling provides more adaptive benefit for HIPV emissions than does between-plant signaling or attraction of predators. That is, the emission of HIPVs might have evolved primarily to protect undamaged parts of the plant against potential enemies, and neighboring plants and predators of herbivores later co-opted such HIPV signals for their own benefit.Key words: intra-plant signaling, plantplant communication, eavesdropping, systemic wound signals, plant defense, tri-trophic interactionsPlants often emit a unique blend of volatiles in response to herbivore attack. The emission of these herbivore-induced plant volatiles (HIPVs) is an active response to herbivore feeding, producing a blend of volatiles that is distinct from those emitted following mechanical injury alone.¹ Their emission can be variable; while some compounds follow a diurnal pattern with increasing amounts during the time of high photosynthesis,^2,3 others are emitted primarily at night.⁴ In some cases, the HIPV blend produced also differs depending on the species of herbivore feeding on the plant.⁵ This specificity is thought to be due to chemicals in the herbivore’s regurgitant, such as the fatty-acid amino-acid conjugate volicitin, that activate the emission of volatiles in plants.^6,7 Furthermore, HIPVs are emitted not only from the site of damage, but also at times from systemically undamaged parts of the plant.⁸ This and other systemic responses are, however, restricted within a plant such that only parts of the plant that share vascular connections with the damaged tissue receive wound signals and have the potential to respond.^9,10The ecological role of HIPVs has been a subject of fascination and the evolutionary advantage gained for plants by emitting HIPVs remains an unresolved topic of discussion. While some HIPV compounds, and some of their precursors, have sufficient volatility that their release is essentially inevitable after synthesis,¹¹ most tend to be tightly regulated. Assuming that HIPV emissions evolved as a result of trophic interactions among plants, herbivores, and natural enemies, there are four general ecological roles that HIPVs may play: (1) a direct negative effect on the herbivore, (2) a signal to alert natural enemies of the herbivore, (3) a warning signal to nearby undamaged plants, and (4) a systemic warning signal within the damaged plant (Fig. 1). The first two potential roles involve the manipulation of animal behavior, while the last two may alter plant “behavior”.Open in a separate windowFigure 1Herbivore-induced plant volatiles (HIPVs) play multiple roles in interactions among plants, herbivores, and natural enemies (possible interactions are depicted by arrows). Some of them benefit the HIPV-emitting plant (Emitter); these positive interactions include repellent effects on herbivores, attraction of natural enemies of herbivores, activation or priming of defenses in unwounded parts within the emitting plant (within-plant signaling), and growth inhibitory effects on neighboring plants (Receiver) through allelopathy. On the other hand, HIPVs may negatively affect the emitting plant by attracting herbivores or natural enemies (e.g., certain parasitoids) that result in increased damage. Finally, neighboring plants may “eavesdrop” from the emitting plant by responding to HIPVs (between-plant signaling). This latter interaction may be negative to the emitter if it is outcompeted by neighbors who receive wound signals, but beneficial to the receiving plant. Drawing by Robert Holdcraft.Scents can have a demonstrable effect on animal behavior. With respect to plant-herbivore interactions, scents can provide information about the status of a plant to herbivores and their natural enemies. For example, HIPVs may repel adults moths searching for oviposition sites,³ which has been interpreted from the perspective of either a plant minimizing damage or, perhaps more realistically, an adult moth searching for an undamaged, high quality resource for her offspring. Conversely, HIPV-emitting plants may increase their chance of being injured if herbivores are attracted to these volatiles.¹² The more commonly accepted role of HIPVs in manipulating animal behavior is to attract natural enemies of the herbivores. This tri-trophic “cry for help”¹³ has a potential evolutionary benefit for both the plant emitting the volatiles and the natural enemies responding to this emission.^14–16 Although this idea makes sense in an evolutionary perspective, only a few studies have documented the occurrence of this phenomenon in natural systems.¹⁷ Indeed, the effectiveness of a cry for help depends on the presence of a helper and, equally importantly, the ability of the helper to increase plant fitness. In the case of predator attraction, the herbivore may be removed from the plant and consumed, thereby reducing damage for the emitting plant.¹⁸ However, insect herbivores infected by parasitoids, which also use HIPV cues to locate hosts,¹⁹ may also consume less plant material²⁰ but may also in some cases consume more plant material than unparasitized insect herbivores.²¹ Since there is currently no evidence that plants can modify HIPV blends to attract selectively predators versus parasitoids, an answered cry for help may not reliably decrease the total amount of damage to an emitting plant. Thus, the fact that natural enemies respond to HIPVs does not imply that these volatiles evolved for this purpose or that there is an adaptive advantage for a plant to use HIPVs to attract natural enemies. Rather, natural enemies of insect herbivores may have learned to co-opt the HIPV signal emitted by plants and, by doing so, increased their fitness irrespective of the ultimate fitness outcome to the plant.Though more controversial, scents can also have an effect on plant behavior.²² Early work suggested that HIPVs from wounded willows,²³ poplars²⁴ and sugar maples²⁴ could trigger defense responses from other neighboring conspecifics. More recent studies have shown that this signaling can occur between different species of plants.²⁵ While these results are intriguing, they appear to have little adaptive function from the perspective of an emitting plant, which could be facilitating the fitness of potential resource competitors. Further, unless the individual within the same plant species shared some degree of kinship,²⁶ an emitting plant would also be at a disadvantage by providing an HIPV wound signal to a conspecific that, in theory, occupies the same competitive niche space. On the other hand, unwounded conspecific should benefit from being able to ‘eavesdrop’ by detecting HIPVs from wounded plants as they share the same herbivore complex and thus are vulnerable to attack. Moreover, from a heterospecific receiver’s perspective, the benefits of eavesdropping can be confounded by the potential of mounting defenses against a signal generated by incompatible herbivores feeding on a different plant species.²⁷ So, eavesdropping may be adaptive for a receiving plant if it realizes increased fitness relative to a conspecific that did not receive the signal. The emitting plant derives no apparent adaptive benefit of using HIPVs to warn neighboring plants. However, the emitting plant may benefit if their HIPVs have inhibitory allelopathic activity on neighboring plants.²⁸Our recent work¹ highlighted another scenario by which an HIPV-emitting plant would derive a direct benefit from the emissions: when HIPVs act as systemic wound signals within damaged plants. We showed that branches of blueberry shrubs lack effective vascular connections and thus cannot transmit wound signals among branches via the vasculature. To compensate, HIPVs can be transmitted among branches and, in so doing, overcome the vascular constraints of the branching life history strategy. Exposure to HIPVs increased levels of defensive signaling hormones in undamaged branches, changed their defensive chemical status, and made them more resistant to herbivores.¹ This idea that HIPVs may function in intra-plant communication to activate or prime defenses in other parts of the emitting plant against future attack was first suggested separately by Farmer²⁹ and Orians.⁹ The hypothesis was first tested with mechanically clipped wild sagebrush,³⁰ and it was further tested with insect herbivores of wild lima bean³¹ and hybrid poplar.³² Under this scenario, the emitting plant derives a direct benefit from the HIPVs, providing an unambiguous fitness advantage.So, what is the most beneficial factor to a plant for emitting volatiles in response to herbivore feeding? In terms of maximizing the potential benefit and minimizing the potential risk to the emitting plant, the function of HIPVs in mediating systemic wound signaling clearly provides the greatest potential adaptive advantage. Thus, we propose that the primary adaptive benefit for the evolution of HIPVs is to signal and protect unwounded parts of the attacked plant with high risk of infestation against herbivores. Later, these volatiles provided cues that led to adaptive fitness advantages for neighboring plants and natural enemies of herbivores, which may or may not benefit the HIPV-emitting plant. Indeed, ecologically adaptive advantages have emerged and contribute to a diverse, multi-functional chemical ecology mediated by HIPVs.     

Fire severity alters plant regeneration patterns and defense against herbivores in mixed aspen forests

Fire and herbivory are primary disturbances that often overlap and strongly influence plant community development, but it is unclear how herbivory changes in relation to variability in burn severity. With climate change expected to alter fire regimes globally there is a critical need to understand how heterogeneity in post‐fire habitat conditions modifies plant–herbivore interactions. We examined herbivory patterns, growth responses and defense chemistry expression (phenolic glycoside, condensed tannins) of regenerating aspen Populus tremuloides that experienced variable burn severity in the 2010 Twitchell Canyon Fire, Utah, USA. Browse damage was approximately 60% lower in moderate and high burn severity plots compared to low severity and unburned plots. Aspen regeneration density was 2.3 and 3.1 fold greater in high and moderate severity burn plots than in low severity and unburned plots. High burn severity stimulated photosynthesis, vertical growth and biomass accumulation. Defense chemistry expression responded dynamically over time depending on burn severity. From June to August, phenolic glycoside concentrations showed no significant change in unburned and low severity fire conditions but increased 79% and 139% in moderate and high severity burn environments. By the end of summer, condensed tannins increased six‐fold in high severity burn plots, with increases of 50% or less in the lower burn severity plots. Deer activity, as defined by pellet counts, was inversely related to fire severity and positively related to browse damage. Elk and cattle activity showed no significant relationship with browse activity. Greater light availability in higher severity burn environments appears to enhance tolerance and resistance of aspen against herbivory by increasing growth potential and defense chemistry expression of aspen. These results suggest that burn severity influences plant–herbivore interactions through bottom–up and top–down mechanisms, and that higher fire severity increases post‐disturbance vegetation recruitment potential by increasing resilience to herbivory.     

Interactions between above- and belowground insect herbivores as mediated by the plant defense system

Plants are frequently attacked by both above- and belowground arthropod herbivores. Nevertheless, studies rarely consider root and shoot herbivory in conjunction. Here we provide evidence that the root-feeding insect Agriotes lineatus reduces the performance of the foliage feeding insect Spodoptera exigua on cotton plants. In a bioassay, S. exigua larvae were allowed to feed on either undamaged plants, or on plants that had previously been exposed to root herbivory, foliar herbivory, or a combination of both. Previous root herbivory reduced the relative growth rates as well as the food consumption of S. exigua by more than 50% in comparison to larvae feeding on the undamaged controls. We found no effects in the opposite direction, as aboveground herbivory by S. exigua did not affect the relative growth rates of root-feeding A. lineatus . Remarkably, neither did the treatment with foliar herbivory affect the food consumption and relative growth rate of S. exigua in the bioassay. However, this treatment did result in a significant change in the distribution of S. exigua feeding. Plants that had been pre-exposed to foliar herbivory suffered significantly less damage on their young terminal leaves. While plant growth and foliar nitrogen levels were not affected by any of the treatments, we did find significant differences between treatments with respect to the level and distribution of plant defensive chemicals (terpenoids). Exposure to root herbivores resulted in an increase in terpenoid levels in both roots as well as in mature and immature foliage. Foliar damage, on the other hand, resulted in high terpenoid levels in young, terminal leaves only. Our results show that root-feeding herbivores may change the level and distribution of plant defenses aboveground. Our data suggest that the reported interactions between below- and aboveground insect herbivores are mediated by induced changes in plant secondary chemistry.