Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison

Plants may respond both to feeding and oviposition by herbivorous insects. While responses of plants to feeding damage by herbivores have been studied intensively during the past decades, only a few, but growing number of studies consider the reactions of plants towards egg deposition by herbivorous insects. Plants showing defensive response to oviposition by herbivores do not `wait' until being damaged by feeding, but may instead react towards one of the initial steps of herbivore attack, the egg deposition. Direct plant defensive responses to feeding act directly against the feeding stages of the herbivores. However, a plant may also show direct defensive responses to egg deposition by (a) formation of neoplasms, (b) formation of necrotic tissue (= hypersensitive response), and (c) production of oviposition deterrents. All these plant reactions have directly negative effects on the eggs, hatching larvae, or on the ovipositing females. Indirect plant defensive responses to feeding result in the emission of volatiles (= synomones) that attract predators or parasitoids of the feeding stages. A few recent studies have shown that plants are able to emit volatiles also in response to egg deposition and that these volatiles attract egg parasitoids. Studies on the mechanisms of induction of synomones by egg deposition show several parallels to the mechanisms of induction of plant responses by feeding damage. When considering induced plant defence against herbivores from an evolutionary point of view, the question arises whether herbivores evolved the ability to circumvent or even to exploit the plant's defensive responses. The reactions of herbivores to oviposition induced plant responses are compared with their reactions to feeding induced plant responses.     

Gone with the wind: trembling leaves may deter herbivory

Plants employ various defensive tactics against herbivores but are rarely considered to use rapid movements to resist predation. However, the aboveground parts of plants are often forcefully moved by wind and rain. This passive movement has been overlooked as an anti‐herbivore trait. The leaves of many plant species, such as aspens, Indian sacred fig, bamboos, and palms, tremble even in a slight breeze. Leaves that are easily moved by gentle winds can sometimes resist strong winds and may have other benefits as well. In the present study, it is proposed that the movement of such plant leaves physically deters arthropod herbivory and pathogen infection by repelling colonization and oviposition by herbivorous insects. This leads to herbivores and pathogens being dislodged from the plants, and the ensuing death of the herbivores on the ground or at least their recolonization to other plants, as well as the interruption of feeding, intraspecific communication and the mating behaviour of herbivores, thus lowering their performance on the plant or increasing enemy attack of the herbivores. In addition, passive leaf movements may undermine herbivore camouflage and expose them to predation, and may also allow plant volatiles to diffuse efficiently to repel herbivores and attract natural enemies. Thus, the mechanistic properties of these leaves may have anti‐herbivore effects in the wind and rain. This hypothesis can also be applied to aquatic plants that tremble in gentle water currents. In addition, genetic manipulation of the tendency for leaf movement may be beneficial for the management of pest insects and pathogens with reduced pesticides in forestry and agriculture. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 738–747.     

Direct and indirect chemical defence of pine against folivorous insects

The chemical defence of pine against herbivorous insects has been intensively studied with respect to its effects on the performance and behaviour of the herbivores as well as on the natural enemies of pine herbivores. The huge variety of terpenoid pine components play a major role in mediating numerous specific food web interactions. The constitutive terpenoid pattern can be adjusted to herbivore attack by changes induced by insect feeding or oviposition activity. Recent studies on folivorous pine sawflies have highlighted the role of induced pine responses in herbivore attack and have demonstrated the importance of analysing the variability of pine defence and its finely tuned specificity with respect to the herbivore attacker in a multitrophic context.     

Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory

Plants defend against attack from herbivores by direct and indirect defence mechanisms mediated by the accumulation of phytoalexins and release of volatile signals, respectively. While the defensive arsenals of some plants, such as tobacco and Arabidopsis are well known, most of rice's (Oryza sativa) defence metabolites and their effectiveness against herbivores remain uncharacterized. Here, we used a non‐biassed metabolomics approach to identify many novel herbivory‐regulated metabolic signatures in rice. Most were up‐regulated by herbivore attack while only a few were suppressed. Two of the most prominent up‐regulated signatures were characterized as phenolamides (PAs), p‐coumaroylputrescine and feruloylputrescine. PAs accumulated in response to attack by both chewing insects, i.e. feeding of the lawn armyworm (Spodoptera mauritia) and the rice skipper (Parnara guttata) larvae, and the attack of the sucking insect, the brown planthopper (Nilaparvata lugens, BPH). In bioassays, BPH insects feeding on 15% sugar solution containing p‐coumaroylputrescine or feruloylputrescine, at concentrations similar to those elicited by heavy BPH attack in rice, had a higher mortality compared to those feeding on sugar diet alone. Our results highlight PAs as a rapidly expanding new group of plant defence metabolites that are elicited by herbivore attack, and deter herbivores in rice and other plants.     

Herbivore damage-induced production and specific anti-digestive function of serine and cysteine protease inhibitors in tall goldenrod, Solidago altissima L. (Asteraceae)

Plant protease inhibitors (PIs) are among the most well-studied and widely distributed resistance traits that plants use against their herbivore attackers. There are different types of plant PIs which putatively function against the different types of proteases expressed in insect guts. Serine protease inhibitors (SPIs) and cysteine protease inhibitors (CPIs) are hypothesized to differentially function against the predominant gut proteases in lepidopteran and coleopteran herbivores, respectively. Here, we test the hypothesis that tall goldenrod, Solidago altissima, can specifically respond to damage by different herbivores and differentially induce SPIs and CPIs in response to damage by lepidopteran and coleopteran herbivores. Moreover, we ask if the concerted induction of different types of PIs accounts for variation in induced resistance to herbivory. We altered and optimized a rapid and effective existing methodology to quantitatively analyze both SPI and CPI activity simultaneously from a single tissue sample and to use the same plant extracts directly for characterization of inhibitory effects on insect gut protease activity. We found that both SPIs and CPIs are induced in S. altissima in response to damage, regardless of the damaging herbivore species. However, only SPIs were effective against Spodoptera exigua gut proteases. Our data suggest that plant PI responses are not necessarily specific to the identity of the attacking organism but that different components of generally induced defense traits can specifically affect different herbivore species. While providing an efficient and broadly applicable methodology to analyze multiple PIs extracted from the same tissue, this study furthers our understanding of specificity in induced plant resistance.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Can Epichloë endophytes enhance direct and indirect plant defence?

Induced or constitutive production of secondary metabolites is a successful plant defence strategy against herbivores which can be mediated by plant associated micro-organisms. Several grass species can be associated with an endophytic fungus of the genus Epichloë which produces herbivore toxic or deterring alkaloids. Besides these direct defences, herbivorous insects are controlled via indirect plant defence mechanisms by attracting predators. Recent studies indicate that Epichloë endophytes can improve the grass emitted volatile organic compounds towards herbivore deterrence. Due to their defensive mutualistic function, we hypothesize that Epichloë altered plant volatiles can attract aphid predators and contribute to an increased indirect plant defence. With a common garden study, we show that hoverfly (Syrphidae) larvae and pupae were more abundant on endophyte-infected plants compared to uninfected plants. Our results indicate that the Epichloë endophyte provides, besides direct defence (alkaloid), indirect plant defence by improving the plant odor attracting more olfactory foraging aphid predators. Future research is needed in order to understand: (I) whether endophyte-mediated changes in plant volatiles are induced herbivore specific, (II) whether there is a trade-off between endophyte-mediated direct and indirect plant defence, (III) whether the endophyte produces volatiles or induces a change in plant-derived volatiles, (IV) the role of plant signals in endophyte-mediated plant defence.     

植物蛋白酶抑制剂基因结构、调控及其控制害虫的策略

各种不同类型的植物蛋白酶抑制剂基因已被分离,它们的特异产物(单基因或多基因组合),对昆虫体内各种生化和生理过程会产生不同程度的影响,在对昆虫和病原体防御体系中起重要作用。多种蛋白酶抑制剂重组,协同保护植物的方法,已成为害虫综合防治计划的一部分。尽管它们近期内尚不能代替化学杀虫剂,但可作为有效的替补。目前,大多数抑制剂的作用和机理正在详尽地研究中,该文综述了植物蛋白酶抑制剂的基因结构、调控与表达并讨论了培育转基因作物控制害虫的策略。     

Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions

Alkaloids produced by systemic fungal endophytes of grasses are thought to act as defensive agents against herbivores. Endophytic alkaloids may reduce arthropod herbivore abundances and diversity in agronomic grasses. Yet, accumulating evidence, particularly from native grasses, shows that herbivore preference, abundances and species richness are sometimes greater on endophyte-infected plants, even those with high alkaloids, contrary to the notion of defensive mutualism. We argue that these conflicting results are entirely consistent with well-developed concepts of plant defence theory and tri-trophic interactions. Plant secondary chemicals and endophytic alkaloids often fail to protect plants because: (1) specialist herbivores evolve to detoxify and use defensive chemicals for growth and survival; and (2) natural enemies of herbivores may be more negatively affected by alkaloids than are herbivores. Endophytes and their alkaloids may have profound, but often highly variable, effects on communities, which are also consistent with existing theories of plant defence and community genetics.     

Effects of class-specific,synthetic, and natural proteinase inhibitors on life-history traits of the cotton bollworm Helicoverpa armigera

Herbivorous insects have more difficulty obtaining proteins from their food than do predators and parasites. The scarcity of proteins in their diet requires herbivores to feed voraciously, thus heavily damaging their host plants. Plants respond to herbivory by producing defense compounds, which reduce insect growth, retard development, and increase mortality. Herbivores use both pre- and postdigestive response mechanisms to detect and avoid plant defense compounds. Proteinase inhibitors (PIs) are one example of plant compounds produced as a direct defense against herbivory. Many insects can adapt to PIs when these are incorporated into artificial diets. However, little is known about the effect of PIs on diet choice and feeding behavior. We monitored the diet choice, life-history traits, and gut proteinase activity of Helicoverpa armigera larvae using diets supplemented with synthetic and natural PIs. In choice experiments, both neonates and fourth-instar larvae preferred the control diet over PI-supplemented diets, to varying degrees. Larvae that fed on PI-supplemented diets weighed less than those that fed on the control diet and produced smaller pupae. Trypsin-specific PIs had a stronger effect on mean larval weight than did other PIs. A reduction of trypsin activity but not of chymotrypsin activity was observed in larvae fed on PI-supplemented diets. Therefore, behavioral avoidance of feeding on plant parts high in PIs could be an adaptation to minimize the impact of this plant's defensive strategy.     

Perception of insect feeding by plants

The recognition of phytophagous insects by plants induces a set of very specific responses aimed at deterring tissue consumption and reprogramming metabolism and development of the plant to tolerate the herbivore. The recognition of insects by plants requires the plant’s ability to perceive chemical cues generated by the insects and to distinguish a particular pattern of tissue disruption. Relatively little is known about the molecular basis of insect perception by plants and the signalling mechanisms directly associated with this perception. Importantly, the insect feeding behaviour (piercing‐sucking versus chewing) is a decisive determinant of the plant’s defence response, and the mechanisms used to perceive insects from different feeding guilds may be distinct. During insect feeding, components of the saliva of chewing or piercing‐sucking insects come into contact with plant cells, and elicitors or effectors present in this insect‐derived fluid are perceived by plant cells to initiate the activation of specific signalling cascades. Although receptor–ligand interactions controlling insect perception have yet not been molecularly described, a significant number of regulatory components acting downstream of receptors and involved in the activation of defence responses against insects has been reported. Some of these regulators mediate changes in the phytohormone network, while others directly control gene expression or the redox state of the cell. These processes are central in the orchestration of plant defence responses against insects.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

Contrasting patterns of herbivore and predator pressure on invasive and native plants

Invasive non-native plant species often harbor fewer herbivorous insects than related native plant species. However, little is known about how herbivorous insects on non-native plants are exposed to carnivorous insects, and even less is known on plants that have recently expanded their ranges within continents due to climate warming. In this study we examine the herbivore load (herbivore biomass per plant biomass), predator load (predator biomass per plant biomass) and predator pressure (predator biomass per herbivore biomass) on an inter-continental non-native and an intra-continental range-expanding plant species and two congeneric native species. All four plant species co-occur in riparian habitat in north-western Europe. Insects were collected in early, mid and late summer from three populations of all four species. Before counting and weighing the insects were classified to trophic guild as carnivores (predators), herbivores, and transients. Herbivores were further subdivided into leaf-miners, sap-feeders, chewers and gallers. Total herbivore loads were smaller on inter-continental non-native and intra-continental range-expanding plants than on the congeneric natives. However, the differences depended on time within growing season, as well as on the feeding guild of the herbivore. Although the predator load on non-native plants was not larger than on natives, both non-native plant species had greater predator pressure on the herbivores than the natives. We conclude that both these non-native plant species have better bottom-up as well as top-down control of herbivores, but that effects depend on time within growing season and (for the herbivore load) on herbivore feeding guild. Therefore, when evaluating insects on non-native plants, variation within season and differences among feeding guilds need to be taken into account.     

The jasmonic acid-amino acid conjugates JA-Val and JA-Leu are involved in rice resistance to herbivores

The phytohormone jasmonic acid (JA) plays a core role in plant defence against herbivores. When attacked by herbivores, JA and its bioactive derivatives are accumulated at the damage site, and subsequently perceived by the jasmonate co-receptors COI1 and JAZ proteins. The (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile) is known to be the main active JA derivative controlling vascular plant responses to herbivores as well as other JA-regulated processes. However, whether other endogenous JA-amino acid conjugates (JA-AAs) are involved in herbivore-induced defence responses remain unknown. Here, we investigated the role of herbivore-elicited JA-AAs in the crop plant rice. The levels of five JA-AAs were significantly increased under the armyworm, leaf folder and brown planthopper attack. Of the elicited JA derivatives, JA-Ile, JA-Val and JA-Leu could serve as ligands to promote the interaction between rice COI1 and JAZs, inducing OsJAZ4 degradation in vivo. JA-Val or JA-Leu treatment increased the expression of JA- and defence-related pathway genes but not JA-Ile levels, suggesting that these JA-AAs may directly function in JA signalling. Furthermore, the application of JA-Val or JA-Leu resulted in JA-mediated plant growth inhibition, while enhancing plant resistance to herbivore attack. This study uncovers that JA-Val and JA-Leu also play a role in rice defence against herbivores.     

Terrestrial plant tolerance to herbivory

Damage to plants by herbivores is ubiquitous and sometimes severe. Tolerance is the capacity of a plant to maintain its fitness through growth and reproduction after sustaining herbivore damage. Recent physiological and ecological work indicates that tolerance mechanisms are numerous and varied. Some of the plant traits involved may reflect selection by herbivores, while others are likely to be by-products of selection for other ecological functions. Similarly, some tolerance mechanisms may participate In trade-offs with plant defence, while many do not. Regardless of its ultimate origin or physiological relationship to plant defence, tolerance often may Influence the evolution of plant defence and the composition of plant communities.     

Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies

Herbivore-damaged plants emit volatile organic compounds that attract natural enemies of the herbivores. This form of indirect plant defence occurs aboveground as well as belowground, but it remains unclear how simultaneous feeding by different herbivores attacking leaves and roots may affect the production of the respective defence signals. We employed a setup that combines trapping of volatile organic signals and simultaneous measurements of the attractiveness of these signals to above and belowground natural enemies. Young maize plants were infested with either the foliar herbivore Spodoptera littoralis , the root herbivore Diabrotica virgifera virgifera , or with both these important pest insects. The parasitic wasp Cotesia marginiventris and the entomopathogenic nematode Heterorhabditis megidis were strongly attracted if their respective host was feeding on a plant, but this attraction was significantly reduced if both herbivores were on a plant. The emission of the principal root attractant was indeed reduced due to double infestation, but this was not evident for the leaf volatiles. The parasitoid showed an ability to learn the differences in odour emissions and increased its response to the odour of a doubly infested plant after experiencing this odour during an encounter with hosts. This first study to measure effects of belowground herbivory on aboveground tritrophic signalling and vice-versa reemphasizes the important role of plants in bridging interactions between spatially distinct components of the ecosystem.     

The effect of rhizosphere microbes outweighs host plant genetics in reducing insect herbivory

Rhizosphere microbes affect plant performance, including plant resistance against insect herbivores; yet, a direct comparison of the relative influence of rhizosphere microbes versus plant genetics on herbivory levels and on metabolites related to defence is lacking. In the crucifer Boechera stricta, we tested the effects of rhizosphere microbes and plant population on herbivore resistance, the primary metabolome, and select secondary metabolites. Plant populations differed significantly in the concentrations of six glucosinolates (GLS), secondary metabolites known to provide herbivore resistance in the Brassicaceae. The population with lower GLS levels experienced ~60% higher levels of aphid (Myzus persicae) attack; no association was observed between GLS and damage by a second herbivore, flea beetles (Phyllotreta cruciferae). Rhizosphere microbiome (disrupted vs. intact native microbiome) had no effect on plant GLS concentrations. However, aphid number and flea beetle damage were respectively about three‐ and seven‐fold higher among plants grown in the disrupted versus intact native microbiome treatment. These differences may be attributable to shifts in primary metabolic pathways previously implicated in host defence against herbivores, including increases in pentose and glucoronate interconversion among plants grown with an intact microbiome. Furthermore, native microbiomes with distinct community composition (as estimated from 16s rRNA amplicon sequencing) differed two‐fold in their effect on host plant susceptibility to aphids. The findings suggest that rhizosphere microbes, including distinct native microbiomes, can play a greater role than population in defence against insect herbivores, and act through metabolic mechanisms independent of population.     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.