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.     

植食性昆虫唾液效应子和激发子的研究进展

植食性昆虫与寄主植物通过协同进化形成了复杂的防御和反防御机制.本文系统综述了昆虫唾液效应子和激发子在植物与昆虫互作中的作用及机理.昆虫取食中释放的唾液激发子被植物识别而激活植物早期免疫反应,昆虫也能从口腔分泌效应子到植物体内抑制免疫;抗性植物则利用抗性(R)蛋白识别昆虫无毒效应子,启动效应子诱导的免疫反应,而昆虫又进化...     

The Myriad Plant Responses to Herbivores

Abstract Plant responses to herbivores are complex. Genes activated on herbivore attack are strongly correlated with the mode of herbivore feeding and the degree of tissue damage at the feeding site. Phloem-feeding whiteflies and aphids that produce little injury to plant foliage are perceived as pathogens and activate the salicylic acid (SA)-dependent and jasmonic acid (JA)/ethylene-dependent signaling pathways. Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage. Other elicitors for defense-gene activation are likely to be more ubiquitous. Analogies to the pathogen-incompatible reactions are found. Chewing insects such as caterpillars and beetles and cell-content feeders such as mites and thrips cause more extensive tissue damage and activate wound-signaling pathways. Herbivore feeding is not equivalent to mechanical wounding. Wound responses are a part of the induced responses that accompany herbivore feeding. Herbivores induce direct defenses that interfere with herbivore feeding, growth and development, fecundity, and fertility. In addition, herbivores induce an array of volatiles that creates an indirect mechanism of defense. Volatile blends provide specific cues to attract herbivore parasites and predators to infested plants. The nature of the elicitors for volatile production is discussed.     

Physiological function and ecological aspects of fatty acid-amino acid conjugates in insects†

In tritrophic interactions, plants recognize herbivore-produced elicitors and release a blend of volatile compounds (VOCs), which work as chemical cues for parasitoids or predators to locate their hosts. From detection of elicitors to VOC emissions, plants utilize sophisticated systems that resemble the plant–microbe interaction system. Fatty acid–amino acid conjugates (FACs), a class of insect elicitors, resemble compounds synthesized by microbes in nature. Recent evidence suggests that the recognition of insect elicitors by an ancestral microbe-associated defense system may be the origin of tritrophic interactions mediated by FACs. Here we discuss our findings in light of how plants have customized this defense to be effective against insect herbivores, and how some insects have successfully adapted to these defenses.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

How do insect herbivores cope with the extreme oxidative stress of phototoxic host plants?

Plants of the Asteraceae and Hypericaceae possess secondary compounds that induce photooxidation in insect herbivores that consume them. One of the well-established modes of action of these substances is peroxidation of membrane lipids. Some herbivores counteract these defences by avoidance of light and tissues rich in phototoxins or the ability to detoxify these secondary substances. The cytochrome P-450 polysubstrate monooxygenase systems involved, the metabolic products, and a new putative toxin pump have been described. Dietary antioxidants (β-carotene, vitamin E, ascorbate) are additional defences against phototoxicity. They reduce mortality in herbivores exposed to phototoxins and some specialist herbivores have high constitutive levels. Adapted specialist insects also have higher constitutive levels of superoxide dismutase (SOD) and respond to phototoxins in their diet by the induction of catalase (CAT), glutathione reductase (GR), and increased levels of reduced glutathione (GSH). Artificial inhibition of the enzymes SOD and CAT had little effect on phototoxicity but inhibition of GSH synthesis in herbivores enhanced photooxidative effects of administered phototoxins on lipid peroxidation. While insects have many mechanisms to overcome plant photooxidants, the Asteraceae appear to have adopted a strategy of counterattack. We suggest and provide preliminary evidence that a second group of secondary substances, the sesquiterpene lactones, occurring in the Asteraceae can attack key antioxidant defences to synergise phototoxins. © 1995 Wiley-Liss, Inc.     

Quantitative comparison of chemical, biological and mechanical induction of secondary compounds in Pinus pinaster seedlings

Chemical elicitors and mechanical treatments simulating real insect herbivory have been increasingly used to study induced defensive responses in woody plants. However, simultaneous quantitative comparisons of plant chemical defences elicited by real and simulated herbivory have received little attention. In this paper we compared the effects of real herbivory, simulated herbivory using two chemical elicitors, and mechanical damage treatments on the quantitative secondary chemistry of Pinus pinaster juveniles (namely on non-volatile resin in the stem and total phenolics in the needles). The real herbivory involved phloem wounding by Hylobius abietis and defoliation by Brachyderes lusitanicus (two pine weevils); the chemical elicitors to simulate herbivory induction were 40 mM methyl jasmonate (MJ) and 20 μM benzothiadiazole (BTH); and the mechanical treatments included phloem wounding and needle clipping. We also performed an additional experiment for assessing at what extent insect extracts could increase plant responses over mechanical damage. Chemical induction with MJ, mechanical wounding and real phloem herbivory by H. abietis all produced quantitatively similar results, increasing the concentration of resin in the stem and total phenolics in the needles by equivalent magnitudes. Exogenous application of BTH increased the concentration of phenolic compounds in pine needles, but did not show the same effect on stem resin. Contrastingly, we did not find significant changes in the concentration of resin in the stem or phenolics in the needles after needle clipping and B. lusitanicus feeding. Mechanical damage followed by the application of extracts from the insects B. lusitanicus and H. abietis on the injured tissues did not increase the responses in comparison to mechanical damage alone. The fact that strong induced responses elicited by phloem wounding insects are equally elicited by phloem injuries suggests that defences in pine trees are raised with low specificity regarding biotic enemies. Results from this paper support future methodological approaches using chemical elicitors and mechanical damage as simulated herbivory treatments for the experimental induction of conifer defences.     

Perception, signaling and molecular basis of oviposition-mediated plant responses

Eggs deposited on plants by herbivorous insects represent a threat as they develop into feeding larvae. Plants are not a passive substrate and have evolved sophisticated mechanisms to detect eggs and induce direct and indirect defenses. Recent years have seen exciting development in molecular aspects of egg-induced responses. Some egg-associated elicitors have been identified, and signaling pathways and egg-induced expression profiles are being uncovered. Depending on the mode of oviposition, both the jasmonic acid and salicylic acid pathways seem to play a role in the induction of defense responses. An emerging concept is that eggs are recognized like microbial pathogens and innate immune responses are triggered. In addition, some eggs contain elicitors that induce highly specific defenses in plants. Examples of egg-induced suppression of defense or, on the contrary, egg-induced resistance highlight the complexity of plant–egg interactions in an on-going arms race between herbivores and their hosts. A major challenge is to identify plant receptors for egg-associated elicitors, to assess the specificity of these elicitors and to identify molecular components that underlie various responses to oviposition.     

A porin-like protein from oral secretions of Spodoptera littoralis larvae induces defense-related early events in plant leaves

Insect herbivory on plants is a complex incident consisting of at least two different aspects, namely mechanical damage and chemical challenge, as feeding insects introduce oral secretions (OS) into the wounded tissue of the attacked plant. Mechanical wounding alone is sufficient to induce a set of defense-related reactions in host plants, but some early events such as membrane potential (Vm) changes and cytosolic Ca²⁺-elevations can be triggered only by herbivores suggesting that OS-derived molecules are involved in those processes. Following an assay-guided purification based on planar lipid bilayer membrane technique in combination with proteomic analysis, a porin-like protein (PLP) of most likely bacterial origin was determined from collected OS of Spodoptera littoralis larvae. PLP exhibited channel-forming activity. Further, early defense-related events in plant–insect interaction were evaluated by using a purified fraction and α-hemolysin (α-HL) as a commercial pore-forming compound. Both up-regulated the calmodulin-like CML42 in Arabidopsis thaliana, which only responds to oral secretion and not to wounding. An elevation of in vivo [Ca²⁺]_cyt was not observed. Because membrane channel formation is a widespread phenomenon in plant–insect interactions, this PLP might represent an example for microbial compounds from the insect gut which are initially involved in plant–insect interactions.     

Generalist insects behave in a jasmonate-dependent manner on their host plants,leaving induced areas quickly and staying longer on distant parts

Plants are sessile, so have evolved sensitive ways to detect attacking herbivores and sophisticated strategies to effectively defend themselves. Insect herbivory induces synthesis of the phytohormone jasmonic acid which activates downstream metabolic pathways for various chemical defences such as toxins and digestion inhibitors. Insects are also sophisticated animals, and many have coevolved physiological adaptations that negate this induced plant defence. Insect behaviour has rarely been studied in the context of induced plant defence, although behavioural adaptation to induced plant chemistry may allow insects to bypass the host''s defence system. By visualizing jasmonate-responsive gene expression within whole plants, we uncovered spatial and temporal limits to the systemic spread of plant chemical defence following herbivory. By carefully tracking insect movement, we found induced changes in plant chemistry were detected by generalist Helicoverpa armigera insects which then modified their behaviour in response, moving away from induced parts and staying longer on uninduced parts of the same plant. This study reveals that there are plant-wide signals rapidly generated following herbivory that allow insects to detect the heterogeneity of plant chemical defences. Some insects use these signals to move around the plant, avoiding localized sites of induction and staying ahead of induced toxic metabolites.     

Resistance and response of <Emphasis Type="Italic">Pinus pinaster</Emphasis> seedlings to <Emphasis Type="Italic">Hylobius abietis</Emphasis> after induction with methyl jasmonate

Experimental induction of plant chemical defences with methyl jasmonate (MeJa) is a valuable tool for understanding the ecology of plant defensive responses. However, few studies have examined whether MeJa-induced defences in conifers are effective against insect herbivores. We studied, in 17 half-sib Pinus pinaster families, (i) the effect of MeJa application on plant growth and on the induction of diterpenoid resin in different sections of the stem; (ii) whether MeJa-induced defences increase the resistance of living pine juveniles against the large pine weevil Hylobius abietis in an in vivo bioassay and (iii) the induction of resin content after weevil wounding. Resin concentration was greater in the upper section of the stem compared with basal sections in both MeJa-induced and non-induced seedlings. Sixty days after MeJa application, treated plants showed 40% greater resin content all along the stem, but reduced height growth compared to control plants. MeJa-induction was effective against the pine weevil, as induced seedlings were 21% less damaged than control plants. Wounding activity by H. abietis produced a strong local defensive response after 48 h, where resin concentration was double that observed in the basal and apical sections not exposed to the insects.     

Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.     

Insect herbivory and ontogeny: How do growth and development influence feeding behaviour,morphology and host use?

Herbivorous insects exploit many different plants and plant parts and often adopt different feeding strategies throughout their life cycle. The conceptual framework for investigating insect–plant interactions relies heavily on explanations invoking plant chemistry, neglecting a suite of competing and interacting pressures that may also limit herbivory. In the present paper, the methods by which ontogeny, feeding strategies and morphological characters inhibit herbivory by mandibulate holometabolous insects are examined. The emphasis on mechanical disruption of plant cells in the insect digestive strategy changes the relative importance of plant ‘defences’, increasing the importance of leaf structure in inhibiting herbivory. Coupled with the implications of substantial morphological and behavioural changes in ontogeny, herbivores adopt a range of approaches to herbivory that are independent of plant chemistry alone. Many insect herbivores exhibit substantial ontogenetic character displacement in mandibular morphology. This is tightly correlated with changes in feeding strategy, with changes to the cutting edges of mandibles increasing the efficiency of feeding. The changes in feeding strategy are also characterized by changes in feeding behaviour, with many larvae feeding gregariously in early instars. Non‐nutritive hypotheses considering the importance of natural enemies, shelter‐building and thermoregulation may also be invoked to explain the ontogenetic consequences of changes to feeding behaviour. There is a need to integrate these factors into a framework considering the gamut of potential explanations of insect herbivory, recognizing that ontogenetic constraints are not only viable explanations but a logical starting point. The interrelations between ontogeny, size, morphology and behaviour highlight the complexity of insect–plant relationships. Given the many methods used by insect herbivores to overcome the challenges of consuming foliage, the need for species‐specific and stage‐ specific research investigating ontogeny and host use by insect herbivores is critical for developing general theories of insect–plant interactions.     

Multiple calmodulin-like proteins in Arabidopsis are induced by insect-derived (Spodoptera littoralis) oral secretion

In plant cells, diverse environmental changes often induce transient elevation in the intracellular calcium concentrations, which are involved in signaling pathways leading to the respective cellular reactions. Therefore, these calcium elevations need to be deciphered into specific downstream responses. Calmodulin-like-proteins (CMLs) are calcium-sensing proteins present only in higher plants. They are involved in signaling processes induced by both abiotic as well as biotic stress factors. However, the role of CMLs in the interaction of plants with herbivorous insects is almost unknown. Here we show that in Arabidopsis thaliana a number of CMLs genes (CML9, 11,12,16,17 and 23) are upregulated due to treatments with oral secretion of larvae of the herbivorous insect Spodoptera littoralis. We identified that these genes belong to two groups that respond with different kinetics to the treatment with oral secretion. Our data indicate that signaling networks involving multiple CMLs very likely have important functions in plant defense against insect herbivores, in addition to their involvement in many other stress-induced processes in plants.     

Realised toxicity of plant defences to an insect herbivore depends more on insect dehydration than on energy reserves

1. Climate effects on plant defences, and subsequently insect herbivores, have received considerable attention. However, climate also directly affects the physiological condition of insects that may influence their ability to combat plant defences. 2. This study tested the effects of body fat and water content on the ability of mountain pine beetles, Dendroctonus ponderosae Hopkins, to tolerate monoterpenes, the primary defences of their host pine trees. To manipulate their physiological condition, we exposed beetles to one of three environmental treatments: cold (4 °C, 30% RH), humid (21 °C, 70% RH) or dry (21 °C, 30% RH). Beetles had the highest fat and water content in the cold treatment, followed by lower fat but the same water content in the humid treatment, and the lowest of both in the dry treatment. Following environmental treatments, beetles were exposed to 0, 312.5 or 625 ppm vapours of monoterpenes (−)-α-pinene or (R)-(+)-limonene. 3. Survival during both environmental and monoterpene treatments was highest for the cold treatment, less for the humid treatment, and lowest for the dry treatment. Fat and water content positively predicted survival. In response to increasing monoterpene concentration, survival, body condition and water content, but not fat, declined. 4. These results indicate that water content of insect herbivores was important for the realised toxicity of plant defences, presumably due to the process of excreting detoxified compounds. Energetic costs of detoxification were less evident. Dehydration of insects has not been widely considered in insect–plant interactions, but effects of climate change on humidity may become increasingly important for these interactions.     

Anthropogenic increase in carbon dioxide modifies plant–insect interactions

Industrialisation has elevated atmospheric levels of CO₂ from original 280 ppm to current levels at 400 ppm, which is estimated to double by 2050. Although high atmospheric CO₂ levels affect insect interactions with host plants, the impact of global change on plant defences in response to insect attack is not completely understood. Recent studies have made advances in elucidating the mechanisms of the effects of high CO₂ levels in plant–insect interactions. New studies have proposed that gene regulation and phytohormones regulate resource allocation from photosynthesis to plant defences against insects. Biochemical and molecular studies demonstrated that both defensive hormones jasmonic acid (JA) and ethylene (ET) participate in modulating chemical defences against herbivores in plants grown under elevated CO₂ atmosphere rather than changes in C:N ratio. High atmospheric CO₂ levels increase vulnerability to insect damage by down‐regulating both inducive and constitutive chemical defences regulated by JA and ET. However, elevated CO₂ levels increase the JA antagonistic hormone salicylic acid that increases other chemical defences. How plants grown under elevated CO₂ environment allocate primary metabolites from photosynthesis to secondary metabolism would help to understand innate defences and prevent future herbivory in field crops. We present evidence demonstrating that changes in chemical defences in plants grown under elevated CO₂ environment are hormonal regulated and reject the C:N hypothesis. In addition, we discuss current knowledge of the mechanisms that regulate plants defences against insects in elevated CO₂ atmospheres.