Phytochemistry (v.72, #13)

Plant–insect interactions by Robert A. Raguso; Wilhelm Boland; Thomas Hartmann; John A. Pickett; Dieter Strack (1495-1496).

Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses by G. Andreas Boeckler; Jonathan Gershenzon; Sybille B. Unsicker (1497-1509).
Phenolic glycosides are major secondary metabolites in the Salicaceae and play an important role as herbivore defenses. Especially salicin (1), salicortin (2) and tremulacin (3) have been well investigated with respect to their impact on herbivores.Display Omitted► This is a review article on the role of phenolic glycosides in plant–herbivore interactions. ► Phenolic glycosides are characteristic secondary metabolites in Salicaceae. ► In this review, we summarize our current knowledge about the role of phenolic glycosides in mediating plant–herbivore interactions. ► We also review, what is known about their basic chemistry and occurrence in plants.Since the 19th century the phytochemistry of the Salicaceae has been systematically investigated, initially for pharmaceutical and later for ecological reasons. The result of these efforts is a rich knowledge about the phenolic components, especially a series of glycosylated and esterified derivatives of salicyl alcohol known as “phenolic glycosides”. These substances have received extensive attention with regard to their part in plant–herbivore interactions. The negative impact of phenolic glycosides on the performance of many generalist herbivores has been reported in numerous studies. Other more specialized feeders are less susceptible and have even been reported to sequester phenolic glycosides for their own defense. In this review, we attempt to summarize our current knowledge about the role of phenolic glycosides in mediating plant–herbivore interactions. As background, we first review what is known about their basic chemistry and occurrence in plants.
Keywords: Salicaceae; Phenolic glycoside; Salicylates; Salicin; Salicortin; Tremulacin; Plant–herbivore interactions; Defense compounds; Mode of action; Biosynthesis;

Many plant species exude latex or other exudates from damages caused by insects. Recently, it has become clear that plant latex and exudates contain various defense chemicals and proteins in highly concentrated manners. The important roles of latex and its defense substances in plant defense against herbivorous insects, as well as in the ecology and evolution of plant–insect interactions, are reviewed based on recent studies, and the mechanistic essence and unique characteristics of latex and laticifer are discussed.Display Omitted► Plant latex contains great varieties of defense chemicals and defense proteins. ► Plant latex exerts strong defense activities against herbivorous insects. ► Plant latex is a system that transports defense substances to the point of damage. ► Insects developed physiological adaptations and/or adaptive behaviors against latex. ► Plant latex plays important roles in the plant–insect interactions.Plant latex and other exudates are saps that are exuded from the points of plant damage caused either mechanically or by insect herbivory. Although many (ca. 10%) of plant species exude latex or exudates, and although the defensive roles of plant latex against herbivorous insects have long been suggested by several studies, the detailed roles and functions of various latex ingredients, proteins and chemicals, in anti-herbivore plant defenses have not been well documented despite the wide occurrence of latex in the plant kingdom. Recently, however, substantial progress has been made. Several latex proteins, including cysteine proteases and chitin-related proteins, have been shown to play important defensive roles against insect herbivory. In the mulberry (Morus spp.)–silkworm (Bombyx mori) interaction, an old and well-known model system of plant–insect interaction, plant latex and its ingredients – sugar-mimic alkaloids and defense protein MLX56 – are found to play key roles. Complicated molecular interactions between Apocynaceae species and its specialist herbivores, in which cardenolides and defense proteins in latex play key roles, are becoming more and more evident. Emerging observations suggested that plant latex, analogous to animal venom, is a treasury of useful defense proteins and chemicals that has evolved through interspecific interactions. On the other hand, specialist herbivores developed sophisticated adaptations, either molecular, physiological, or behavioral, against latex-borne defenses. The existence of various adaptations in specialist herbivores itself is evidence that latex and its ingredients function as defenses at least against generalists. Here, we review molecular and structural mechanisms, ecological roles, and evolutionary aspects of plant latex as a general defense against insect herbivory and we discuss, from recent studies, the unique characteristics of latex-borne defense systems as transport systems of defense substances are discussed based on recent studies.
Keywords: Plant–insect interactions; Plant resistance; Laticifer; Defense protein; Secondary metabolites; Physiological adaptation; Insect adaptive behavior; Coevolution; Chemical ecology; Transport duct (transport canal);

Some plant families produce non-protein amino acids such as shown in the figure. Their defensive functions against insect pests and, in some cases, insect adaptation to these toxic amino acids are reviewed in this manuscript.Display Omitted► Non-protein amino acids have been implicated in plant defense against insect pests. ► Direct toxic effects occur through interference with animal amino acid metabolism.► Nitrogen is stored in a form that is metabolically inaccessible to herbivores. ► Some specialist herbivores have specific detoxification mechanisms. ► Sequenced plant genomes provide opportunities for discovering biosynthetic enzymes.Chemical defense against herbivores is of utmost importance for plants. Primary and secondary metabolites, including non-protein amino acids, have been implicated in plant defense against insect pests. High levels of non-protein amino acids have been identified in certain plant families, including legumes and grasses, where they have been associated with resistance to insect herbivory. Non-protein amino acids can have direct toxic effects via several mechanisms, including misincorporation into proteins, obstruction of primary metabolism, and mimicking and interfering with insect neurological processes. Additionally, certain non-protein amino acids allow nitrogen to be stored in a form that is metabolically inaccessible to herbivores and, in some cases, may act as signals for further plant defense responses. Specialized insect herbivores often possess specific mechanisms to avoid or detoxify non-protein amino acids from their host plants. Although hundreds of non-protein amino acids have been found in nature, biosynthetic pathways and defensive functions have been elucidated in only a few cases. Next-generation sequencing technologies and the development of additional plant and insect model species will facilitate further research on the production of non-protein amino acids, a widespread but relatively uninvestigated plant defense mechanism.
Keywords: Legumes; Plant–insect interaction; Non-protein amino acid; Canavanine; l-DOPA; BABA; GABA; 5-Hydroxy-l-tryptophan;

Plant lectins as defense proteins against phytophagous insects by Gianni Vandenborre; Guy Smagghe; Els J.M. Van Damme (1538-1550).
Many plant lectins show entomotoxic properties against pest insects. The possible use of lectins as tools in crop protection is discussed..Display Omitted► Lectins are present in many plant species and presumably fulfill a role in plant defense. ► The expression of some novel plant lectins was shown to be induced by insect herbivory. ► Many lectins revealed entomotoxic properties when tested in vitro or when expressed in transgenic plants. ► Plant lectins can be useful tools for crop protection strategies.One of the most important direct defense responses in plants against the attack by phytophagous insects is the production of insecticidal peptides or proteins. One particular class of entomotoxic proteins present in many plant species is the group of carbohydrate-binding proteins or lectins. During the last decade a lot of progress was made in the study of a few lectins that are expressed in response to herbivory by phytophagous insects and the insecticidal properties of plant lectins in general. This review gives an overview of lectins with high potential for the use in pest control strategies based on their activity towards pest insects. In addition, potential target sites for lectins inside the insect and the mode of action are discussed. In addition, the effect of plant lectins on non-target organisms such as beneficial insects as well as on human/animal consumers is discussed. It can be concluded that some insecticidal lectins are useful tools that can contribute to the development of integrated pest management strategies with minimal effect(s) on non-target organisms.
Keywords: Agglutinins; Insecticidal proteins; Lectin; Plant defense; Pest control;

Tannins in plant–herbivore interactions by Raymond V. Barbehenn; C. Peter Constabel (1551-1565).
Tannins have variable effects on herbivores, but may negatively impact insect and mammalian herbivores via different mechanisms.Display Omitted► Tannins have diverse effects on herbivores. ► In insect guts, tannins may act as prooxidants rather than binding proteins. Insects have physiological and structural defenses and can tolerate tannins. ► Tannin effects in vertebrates may be both positive and negative and do involve protein binding. ► In the future, molecular biology tools will help define the ecological roles of tannins.Tannins are the most abundant secondary metabolites made by plants, commonly ranging from 5% to 10% dry weight of tree leaves. Tannins can defend leaves against insect herbivores by deterrence and/or toxicity. Contrary to early theories, tannins have no effect on protein digestion in insect herbivores. By contrast, in vertebrate herbivores tannins can decrease protein digestion. Tannins are especially prone to oxidize in insects with high pH guts, forming semiquinone radicals and quinones, as well as other reactive oxygen species. Tannin toxicity in insects is thought to result from the production of high levels of reactive oxygen species. Tannin structure has an important effect on biochemical activity. Ellagitannins oxidize much more readily than do gallotannins, which are more oxidatively active than most condensed tannins. The ability of insects to tolerate ingested tannins comes from a variety of biochemical and physical defenses in their guts, including surfactants, high pH, antioxidants, and a protective peritrophic envelope that lines the midgut. Most work on the ecological roles of tannins has been correlative, e.g., searching for negative associations between tannins and insect performance. A greater emphasis on manipulative experiments that control tannin levels is required to make further progress on the defensive functions of tannins. Recent advances in the use of molecular methods has permitted the production of tannin-overproducing transgenic plants and a better understanding of tannin biosynthetic pathways. Many research areas remain in need of further work, including the effects of different tannin types on different types of insects (e.g., caterpillars, grasshoppers, sap-sucking insects).
Keywords: Proanthocyanidin; Polyphenol; Phenolics; Oxidative stress; Plant defense;

The glucosinolate–myrosinase system is an activated plant defense system that can be disturbed by insect herbivores in many different ways.Display Omitted► Activated plant defense offers diverse ways of circumvention by herbivores. ► Insect counteradaptations are very specific for the system. ► Plant glucosinolate–myrosinase system is “copied” by insect herbivores. ► Insect counteradaptation illustrates “evolutionary arms race”.The glucosinolate–myrosinase system found in plants of the Brassicales order is one of the best studied plant chemical defenses. Glucosinolates and their hydrolytic enzymes, myrosinases, are stored in separate compartments in the intact plant tissue. Upon tissue disruption, bioactivation of glucosinolates is initiated, i.e. myrosinases get access to their glucosinolate substrates, and glucosinolate hydrolysis results in the formation of toxic isothiocyanates and other biologically active products. The defensive function of the glucosinolate–myrosinase system has been demonstrated in a variety of studies with different insect herbivores. However, a number of generalist as well as specialist herbivores uses glucosinolate-containing plants as hosts causing large agronomical losses in oil seed rape and other crops of the Brassicaceae. While our knowledge of counteradaptations in generalist insect herbivores is still very limited, considerable progress has been made in understanding how specialist insect herbivores overcome the glucosinolate–myrosinase system and even exploit it for their own defense. All mechanisms of counteradaptation identified to date in insect herbivores specialized on glucosinolate-containing plants ensure that glucosinolate breakdown to toxic isothiocyanates is avoided. This is accomplished in many different ways including avoidance of cell disruption, rapid absorption of intact glucosinolates, rapid metabolic conversion of glucosinolates to harmless compounds that are not substrates for myrosinases, and diversion of plant myrosinase-catalyzed glucosinolate hydrolysis. One of these counteradaptations, the nitrile-specifier protein identified in Pierid species, has been used to demonstrate mechanisms of coevolution of plants and their insect herbivores.
Keywords: Brassicaceae; Brassicales; Glucosinolates; Myrosinase; Insect counteradaptation; Detoxification; Sequestration;

Mechanisms of insect adaptation to pyrrolizidine alkaloids are reviewed with special emphasis on the most recent data concerning the evolution of a flavin-dependent monooxygenase that acts as a pyrrolizidine alkaloid N-oxygenase in adapted moths.Display Omitted► Pyrrolizidine alkaloids are among the best-studied examples of plant defense. ► Detoxification mechanisms of adapted insects are summarized focusing on N-oxidation. ► Similarities in molecular evolution of adaptations of insects and plants are likely.Pyrrolizidine alkaloids are secondary metabolites that are produced by certain plants as a chemical defense against herbivores. They represent a promising system to study the evolution of pathways in plant secondary metabolism. Recently, a specific gene of this pathway has been shown to have originated by duplication of a gene involved in primary metabolism followed by diversification and optimization for its specific function in the defense machinery of these plants. Furthermore, pyrrolizidine alkaloids are one of the best-studied examples of a plant defense system that has been recruited by several insect lineages for their own chemical defense. In each case, this recruitment requires sophisticated mechanisms of adaptations, e.g., efficient excretion, transport, suppression of toxification, or detoxification. In this review, we briefly summarize detoxification mechanism known for pyrrolizidine alkaloids and focus on pyrrolizidine alkaloid N-oxidation as one of the mechanisms allowing insects to accumulate the sequestered toxins in an inactivated protoxic form. Recent research into the evolution of pyrrolizidine alkaloid N-oxygenases of adapted arctiid moths (Lepidoptera) has shown that this enzyme originated by the duplication of a gene encoding a flavin-dependent monooxygenase of unknown function early in the arctiid lineage. The available data suggest several similarities in the molecular evolution of this adaptation strategy of insects to the mechanisms described previously for the evolution of the respective pathway in plants.
Keywords: Pyrrolizidine alkaloid N-oxidation; Flavin-dependent monooxygenase; Gene duplication; Evolution of insect adaptation mechanisms; Pyrrolizidine alkaloid sequestration;

Cyanogenic glucosides are defence compounds utilized by both plants and insects. Burnet moths sequester linamarin and lotaustralin from their food plants and also carry out de novo synthesis of these compounds and have diversified the use of the compounds.Display Omitted► Update on cyanogenesis in the Burnet moth-Birdsfoot trefoil model system. ► Identical intermediates in the biosynthetic pathways between the two kingdoms. ► New functions appearing for cyanogenic glucosides in plants and insects. ► Sequencing technologies offer opportunities to study genomics in non-model organisms.Cyanogenic glucosides are important components of plant defense against generalist herbivores due to their bitter taste and the release of toxic hydrogen cyanide upon tissue disruption. Some specialized herbivores, especially insects, preferentially feed on cyanogenic plants. Such herbivores have acquired the ability to metabolize cyanogenic glucosides or to sequester them for use in their own predator defense. Burnet moths (Zygaena) sequester the cyanogenic glucosides linamarin and lotaustralin from their food plants (Fabaceae) and, in parallel, are able to carry out de novo synthesis of the very same compounds. The ratio and content of cyanogenic glucosides is tightly regulated in the different stages of the Zygaena filipendulae lifecycle and the compounds play several important roles in addition to defense. The transfer of a nuptial gift of cyanogenic glucosides during mating of Zygaena has been demonstrated as well as the possible involvement of hydrogen cyanide in male assessment and nitrogen metabolism. As the capacity to de novo synthesize cyanogenic glucosides was developed independently in plants and insects, the great similarities of the pathways between the two kingdoms indicate that cyanogenic glucosides are produced according to a universal route providing recruitment of the enzymes required. Pyrosequencing of Z. filipendulae larvae de novo synthesizing cyanogenic glucosides served to provide a set of good candidate genes, and demonstrated that the genes encoding the pathway in plants and Z. filipendulae are not closely related phylogenetically. Identification of insect genes involved in the biosynthesis and turn-over of cyanogenic glucosides will provide new insights into biological warfare as a determinant of co-evolution between plants and insects.
Keywords: Lotus; Zygaena; Cyanogenic glucosides; De novo synthesis; Sequestration; Convergent evolution of pathways;

Insects have adapted to tolerate and use iridoid glycosides and cardenolides despite their usually toxic effects. We here review which physiological processes underlie these adaptations.Display Omitted► Iridoid glycosides in the food plant unspecifically harm insects by crosslinking dietary and tissue proteins. ► Insects may avoid toxicity by suppressing gut enzymes that activate iridoid glycosides. ► Cardenolides act much more specifically by blocking an essential ion carrier, the Na+/K+-ATPase. ► Insects on cardenolide plants have repeatedly evolved target site insensitivity to prevent this toxic effect.Specializing on host plants with toxic secondary compounds enforces specific adaptation in insect herbivores. In this review, we focus on two compound classes, iridoid glycosides and cardenolides, which can be found in the food plants of a large number of insect species that display various degrees of adaptation to them. These secondary compounds have very different modes of action: Iridoid glycosides are usually activated in the gut of the herbivores by β-glucosidases that may either stem from the food plant or be present in the gut as standard digestive enzymes. Upon cleaving, the unstable aglycone is released that unspecifically acts by crosslinking proteins and inhibiting enzymes. Cardenolides, on the other hand, are highly specific inhibitors of an essential ion carrier, the sodium pump. In insects exposed to both kinds of toxins, carriers either enabling the safe storage of the compounds away from the activating enzymes or excluding the toxins from sensitive tissues, play an important role that deserves further analysis. To avoid toxicity of iridoid glycosides, repression of activating enzymes emerges as a possible alternative strategy. Cardenolides, on the other hand, may lose their toxicity if their target site is modified and this strategy has evolved multiple times independently in cardenolide-adapted insects.
Keywords: Iridoid glycosides; Cardenolides; Insect metabolism; Sequestration; Exclusion; Excretion; Na+/K+-ATPase; Target site insensitivity;

Combinations of volatile phytochemicals are perceived by insects as having a different quality from individual compounds as they can elicit different behavioural responses.Display Omitted► Plant volatiles provide host recognition cues to insects. ► The olfactory system gives fine scale spatio-temporal resolution of these signals. ► Olfactory receptor neurons have high sensitivity and specificity to volatiles at physiologically relevant concentrations. ► Behavioural activity depends on perception of blends. ► Blends can elicit different behavioural responses compared to individual compounds.Volatile plant secondary metabolites are detected by the highly sensitive olfactory system employed by insects to locate suitable plants as hosts and to avoid unsuitable hosts. Perception of these compounds depends on olfactory receptor neurones (ORNs) in sensillae, mostly on the insect antennae, which can recognise individual molecular structures. Perception of blends of plant volatiles plays a pivotal role in host recognition, non-host avoidance and ensuing behavioural responses as different responses can occur to a whole blend compared to individual components. There are emergent properties of blend perception because components of the host blend may not be recognised as host when perceived outside the context of that blend. Often there is redundancy in the composition of blends recognised as host because certain compounds can be substituted by others. Fine spatio-temporal resolution of the synchronous firing of ORNs tuned to specific compounds enables insects to pick out relevant host odour cues against high background noise and with ephemeral exposure to the volatiles at varying concentrations. This task is challenging as they usually rely on ubiquitous plant volatiles and not those taxonomically characteristic of host plants. However, such an odour coding system has the advantage of providing flexibility; it allows for adaptation to changing environments by alterations in signal processing while maintaining the same peripheral olfactory receptors.
Keywords: Host location; Host/non-host discrimination; Olfaction; Volatile; Dose; Blend; Ratio; Behaviour;

Plants and insect eggs: How do they affect each other? by Monika Hilker; Torsten Meiners (1612-1623).
Effects of phytochemicals on the production of insect eggs, insect oviposition, egg development and, vice versa, effects of eggs on plant chemistry are reviewed and discussed.Display Omitted► Phytochemicals influence mating and the production of insect eggs. ► The leaf boundary layer may affect egg deposition behaviour and embryo development. ► Insect egg deposition changes photosynthetic activity and secondary metabolism. ► Hypersensitive responses, formation of neoplasms, ovicidal substances harm the eggs. ► Changes of plant odour/leaf surface chemistry attract/arrest egg parasitoids.Plant–insect interactions are not just influenced by interactions between plants and the actively feeding stages, but also by the close relationships between plants and insect eggs. Here, we review both effects of plants on insect eggs and, vice versa, effects of eggs on plants. We consider the influence of plants on the production of insect eggs and address the role of phytochemicals for the biosynthesis and release of insect sex pheromones, as well as for insect fecundity. Effects of plants on insect oviposition by contact and olfactory plant cues are summarised. In addition, we consider how the leaf boundary layer influences both insect egg deposition behaviour and development of the embryo inside the egg. The effects of eggs on plants involve egg-induced changes of photosynthetic activity and of the plant’s secondary metabolism. Except for gall-inducing insects, egg-induced changes of phytochemistry were so far found to be detrimental to the eggs. Egg deposition can induce hypersensitive-like plant response, formation of neoplasms or production of ovicidal plant substances; these plant responses directly harm the eggs. In addition, egg deposition can induce a change of the plant’s odour and leaf surface chemistry which serve indirect plant defence with the help of antagonists of the insect eggs. These egg-induced changes lead to attraction of egg parasitoids and their arrestance on a leaf, respectively. Finally, we summarise knowledge of the elicitors of egg-induced plant changes and address egg-induced effects on the plant’s transcriptional pattern.
Keywords: Plant volatiles; Plant surface; Plant boundary layer; Plant defence; Oviposition-induced defence; Herbivorous insect; Insect oviposition; Elicitor; Oviposition-induced transcription;

Reiterative and interruptive signaling in induced plant resistance to chewing insects by Jinwon Kim; Hélène Quaghebeur; Gary W. Felton (1624-1634).
Induced resistance represents a continuum of phenotypes that is determined by the plant’s ability to integrate multiple signal networks of plant and herbivore origin.Display Omitted► We review insect-derived cues that plants perceive as actual or impending herbivory. ► Early cues include insect walking, oviposition, and the presence of predators. ► Feeding cues from oral secretions may amplify or reduce the expression of defenses. ► Induced resistance is, in some cases, transmitted to successive generations. ► Here we present a model where plant defense level varies in response to insect cues.Our understanding of induced resistance against herbivores has grown immeasurably during the last several decades. Based upon the emerging literature, we argue that induced resistance represents a continuum of phenotypes that is determined by the plant’s ability to integrate multiple suites of signals of plant and herbivore origin. We present a model that illustrates the range of signals arising from early detection through herbivore feeding, and then through subsequent plant generations.
Keywords: Plant defense; Plant signaling; Effectors; Saliva; Elicitors; Oviposition; Transgenerational induction; Herbivory;

The biochemistry of homoterpenes – Common constituents of floral and herbivore-induced plant volatile bouquets by Dorothea Tholl; Reza Sohrabi; Jung-Hyun Huh; Sungbeom Lee (1635-1646).
This review presents a survey of the distribution of homoterpene volatiles in land plants and covers recent findings on the biosynthesis and functions of homoterpenes.Display Omitted► Homoterpenes are common floral and insect-induced volatiles in angiosperms. ► The biosynthetic pathway of the homoterpenes DMNT and TMTT has been elucidated. ► The P450 CYP82G1 from Arabidopsis thaliana was identified as a DMNT/TMTT synthase. ► Engineering the formation of homoterpenes may decipher their role in plant defense.Volatile organic compounds emitted by plants mediate a variety of interactions between plants and other organisms. The irregular acyclic homoterpenes, 4,8-dimethylnona-1,3,7-triene (DMNT) and 4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT), are among the most widespread volatiles produced by angiosperms with emissions from flowers and from vegetative tissues upon herbivore feeding. Special attention has been placed on the role of homoterpenes in attracting parasitoids and predators of herbivores and has sparked interest in engineering homoterpene formation to improve biological pest control. The biosynthesis of DMNT and TMTT proceeds in two enzymatic steps: the formation of the tertiary C15-, and C20-alcohols, (E)-nerolidol and (E,E)-geranyl linalool, respectively, catalyzed by terpene synthases, and the subsequent oxidative degradation of both alcohols by a single cytochrome P450 monooxygenase (P450). In Arabidopsis thaliana, the herbivore-induced biosynthesis of TMTT is catalyzed by the concerted activities of the (E,E)-geranyllinalool synthase, AtGES, and CYP82G1, a P450 of the so far uncharacterized plant CYP82 family. TMTT formation is in part controlled at the level of AtGES expression. Co-expression of AtGES with CYP82G1 at wound sites allows for an efficient conversion of the alcohol intermediate. The identified homoterpene biosynthesis genes in Arabidopsis and related genes from other plant species provide tools to engineer homoterpene formation and to address questions of the regulation and specific activities of homoterpenes in plant–herbivore interactions.
Keywords: Plant volatiles; Indirect defense; Floral scent; Homoterpene; Cytochrome P450; Terpene synthase;

Herbivore-induced plant volatiles should be studied in relation to the central paradigm of plant biology, i.e. the trade-off between growth/reproduction and defence.Display Omitted► Plants are exposed to many attackers and herbivorous insects take a prominent place. ► Plants have evolved a high diversity of secondary metabolites that mediate defences. ► A central paradigm in plant biology is the trade-off between growth and defence. ► Herbivore-induced plant volatiles (HIPV) mediate induced indirect defence. ► We review how HIPV affect interactions between plants and flower-visiting insects.Plants are faced with a trade-off between on the one hand growth, development and reproduction and on the other hand defence against environmental stresses. Yet, research on insect–plant interactions has addressed plant–pollinator interactions and plant–attacker interactions separately. Plants have evolved a high diversity of constitutive and induced responses to attack, including the systemic emission of herbivore-induced plant volatiles (HIPVs). The effect of HIPVs on the behaviour of carnivorous insects has received ample attention for leaf-feeding (folivorous) species and their parasitoids and predators. Here, we review whether and to what extent HIPVs affect the interaction of plants in the flowering stage with mutualistic and antagonistic insects. Whereas the role of flower volatiles in the interactions between plants and insect pollinators has received increased attention over the last decade, studies addressing both HIPVs and pollinator behaviour are rare, despite the fact that in a number of plant species herbivory is known to affect flower traits, including size, nectar secretion and composition. In addition, folivory and florivory can also result in significant changes in flower volatile emission and in most systems investigated, pollinator visitation decreased, although exceptions have been found. Negative effects of HIPVs on pollinator visitation rates likely exert negative selection pressure on HIPV emission. The systemic nature of herbivore-induced plant responses and the behavioural responses of antagonistic and mutualistic insects, requires the study of volatile emission of entire plants in the flowering stage. We conclude that approaches to integrate the study of plant defences and pollination are essential to advance plant biology, in particular in the context of the trade-off between defence and growth/reproduction.
Keywords: Induced defence; Indirect defence; Pollinators; Herbivores; Parasitoids; Terpenoids; Green leaf volatiles; Glucosinolates;

Pollination by brood-site deception by Isabella Urru; Marcus C. Stensmyr; Bill S. Hansson (1655-1666).
2-Heptanone (1), p-cresol (2), 1-decene (3) and dimethyloctadiene (4) are some of the characteristic compounds in the floral headspace of brood-site mimicking species.Pollination is often regarded as a mutualistic relationship between flowering plants and insects. In such a relationship, both partners gain a fitness benefit as a result of their interaction. The flower gets pollinated and the insect typically gets a food-related reward. However, flower–insect communication is not always a mutualistic system, as some flowers emit deceitful signals. Insects are thus fooled by irresistible stimuli and pollination is accomplished. Such deception requires very fine tuning, as insects in their typically short life span, try to find mating/feeding breeding sites as efficiently as possible, and following deceitful signals thus is both costly and time-consuming. Deceptive flowers have thus evolved the ability to emit signals that trigger obligate innate or learned responses in the targeted insects. The behavior, and thus the signals, exploited are typically involved in reproduction, from attracting pheromones to brood/food-site cues. Chemical mimicry is one of the main modalities through which flowers trick their pollen vectors, as olfaction plays a pivotal role in insect–insect and insect–plant interactions. Here we focus on floral odors that specifically mimic an oviposition substrate, i.e., brood-site mimicry. The phenomenon is wide spread across unrelated plant lineages of Angiosperm, Splachnaceae and Phallaceae. Targeted insects are mainly beetles and flies, and flowers accordingly often emit, to the human nose, highly powerful and fetid smells that are conversely extremely attractive to the duped insects. Brood-site deceptive plants often display highly elaborate flowers and have evolved a trap-release mechanism. Chemical cues often act in unison with other sensory cues to refine the imitation.
Keywords: Brood-site pollination; Mimicry;

Chemical ecology and pollinator-driven speciation in sexually deceptive orchids by Manfred Ayasse; Johannes Stökl; Wittko Francke (1667-1677).
In our paper, we describe pollinator attraction and processes of ecological speciation in sexually deceptive orchids that attract male insects for pollination.Display Omitted► Sexually deceptive orchids are ideal candidates for studies of sympatric speciation. ► Traits like the pollinator-attracting scent are associated with reproductive success. ► Minor changes in floral scent might be the driving force for speciation events. ► Pollinators act as isolation barriers towards other sympatrically occurring species. ► Hybridization occurs because of similar odour bouquets of co-occurring species.Sexually deceptive orchids mimic females of their pollinator species to attract male insects for pollination. Pollination by sexual deception has independently evolved in European, Australian, South African, and South American orchid taxa. Reproductive isolation is mainly based on pre-mating isolation barriers, the specific attraction of males of a single pollinator species, mostly bees, by mimicking the female species-specific sex-pheromone. However, in rare cases post-mating barriers have been found. Sexually deceptive orchids are ideal candidates for studies of sympatric speciation, because key adaptive traits such as the pollinator-attracting scent are associated with their reproductive success and with pre-mating isolation.During the last two decades several investigations studied processes of ecological speciation in sexually deceptive orchids of Europe and Australia. Using various methods like behavioural experiments, chemical, electrophysiological, and population-genetic analyses it was shown that minor changes in floral odour bouquets might be the driving force for pollinator shifts and speciation events. New pollinators act as an isolation barrier towards other sympatrically occurring species. Hybridization occurs because of similar odour bouquets of species and the overlap of flowering periods. Hybrid speciation can also lead to the displacement of species by the hybrid population, if its reproductive success is higher than that in the parental species.
Keywords: Sexual deception; Speciation; Orchidaceae; Floral scent; Hybridization; Chemical mimicry;

Nepenthes and other pitcher plants obtain many nutrients from caught insect. The mechanisms that are involved in trapping and retaining prey are presented. Moreover, our knowledge of the pitcher fluid composition, which is responsible for prey digestion and making nutrients available for the plant, is summarized and discussed.Display Omitted► Carnivorous Nepenthes plants attract, trap and digest insect prey for additional nutrients. ► The protein composition of the digestion fluid is reported. ► Secondary metabolites have also been described for the fluid. ► Most enzymes are employed in prey digestion but some show antimicrobial activities.Plant insect interactions are usually recognized as a scenario where herbivorous insects feed on a host plant. However, also the opposite situation is known, where plants feed on insects. Carnivorous pitcher plants of the genus Nepenthes as well as other pitcher plants obtain many nutrients from caught insect prey. Special features of the pitcher traps’ surface are responsible for attraction and trapping insects. Once caught, the prey is digested in the fluid of the pitchers to release nutrients and make them available for the plant. Nutrients are taken up by special glands localized on the inner surface of the pitchers. These glands also secrete the hydrolyzing enzymes into the digestion fluid. Although this is known for more than 100 years, our knowledge of the pitcher fluid composition is still limited. Only in recent years some enzymes have been purified from the pitcher fluid and their corresponding genes could be identified. Among them, many pathogenesis-related proteins have been identified, most of which exhibiting hydrolytic activities. The role of these proteins as well as the role of secondary metabolites, which have been identified in the pitcher fluid, is discussed in general and in the context of further studies on carnivorous plants that might give answers to basic questions in plant biology.
Keywords: Carnivorous plants; Digestion fluid; Hydrolytic enzymes; Nepenthes spp.; PR proteins; Pitcher trap;

Chemical interaction between undamaged plants – Effects on herbivores and natural enemies by Robert Glinwood; Velemir Ninkovic; Jan Pettersson (1683-1689).
Chemical interaction between undamaged plants and its effects on herbivores and natural enemiesDisplay Omitted► Chemical interactions between undamaged plants are reviewed. ► Chemical cues might give plants information about their plant neighbours. ► Plants’ responses to these cues can also affect insect herbivores and predators. ► More research is needed on trophic effects of undamaged plant chemical interaction.Most research on plant–plant chemical interactions has focussed on events following herbivore or pathogen attack. However, undamaged plants also interact chemically as a natural facet of their behaviour, and this may have consequences for insects that use the plants as hosts. In this review, the links between allelopathy and insect behaviour are outlined. Findings on how chemical interactions between different plant species and genotypes affect aphid herbivores and their natural enemies are reviewed, and the role of plant diversity and chemical interaction for trophic interactions in crops is discussed.
Keywords: Allelobiosis; Allelopathy; Tritrophic interaction; Aphids; Ladybirds;