As the largest class of natural products, terpenes have a variety of roles in mediating antagonistic and beneficial interactions among organisms. They defend many species of plants, animals and ...microorganisms against predators, pathogens and competitors, and they are involved in conveying messages to conspecifics and mutualists regarding the presence of food, mates and enemies. Despite the diversity of terpenes known, it is striking how phylogenetically distant organisms have come to use similar structures for common purposes. New natural roles undoubtedly remain to be discovered for this large class of compounds, given that such a small percentage of terpenes has been investigated so far.
Individual biotic and abiotic stresses, such as high temperature, high light and herbivore attack, are well known to increase the emission of volatile organic compounds from plants. Much less is ...known about the effect of multiple, co-occurring stress factors, despite the fact that multiple stresses are probably the rule under natural conditions. Here, after briefly summarizing the basic effects of single stress factors on the volatile emission of plants, we survey the influence of multiple stresses. When two or more stresses co-occur their effects are sometimes additive, while in other cases the influence of one stress has priority. Further investigations on the effects of multiple stress factors will improve our understanding of the patterns and functions of plant volatile emission.
Glucosinolates are sulfur-rich, anionic natural products that upon hydrolysis by endogenous thioglucosidases called myrosinases produce several different products (e.g., isothiocyanates, ...thiocyanates, and nitriles). The hydrolysis products have many different biological activities, e.g., as defense compounds and attractants. For humans these compounds function as cancer-preventing agents, biopesticides, and flavor compounds. Since the completion of the Arabidopsis genome, glucosinolate research has made significant progress, resulting in near-complete elucidation of the core biosynthetic pathway, identification of the first regulators of the pathway, metabolic engineering of specific glucosinolate profiles to study function, as well as identification of evolutionary links to related pathways. Although much has been learned in recent years, much more awaits discovery before we fully understand how and why plants synthesize glucosinolates. This may enable us to more fully exploit the potential of these compounds in agriculture and medicine.
Summary
The phenylpropanoid pathway leads to the production of many important plant secondary metabolites including lignin, chlorogenic acids, flavonoids, and phenolic glycosides. Early studies have ...demonstrated that flavonoid biosynthesis is transcriptionally regulated, often by a MYB, bHLH, and WDR transcription factor complex. In poplar, several R2R3 MYB transcription factors are known to be involved in flavonoid biosynthesis. Previous work determined that poplar MYB134 and MYB115 are major activators of the proanthocyanidin pathway, and also induce the expression of repressor‐like MYB transcription factors. Here we characterize two new repressor MYBs, poplar MYB165 and MYB194, paralogs which comprise a subgroup of R2R3‐MYBs distinct from previously reported poplar repressors. Both MYB165 and MYB194 repressed the activation of flavonoid promoters by MYB134 in transient activation assays, and both interacted with a co‐expressed bHLH transcription factor, bHLH131, in yeast two‐hybrid assays. Overexpression of MYB165 and MYB194 in hybrid poplar resulted in greatly reduced accumulation of several phenylpropanoids including anthocyanins, proanthocyanidins, phenolic glycosides, and hydroxycinnamic acid esters. Transcriptome analysis of MYB165‐ and MYB194‐overexpressing poplars confirmed repression of many phenylpropanoid enzyme genes. In addition, other MYB genes as well as several shikimate pathway enzyme genes were downregulated by MYB165‐overexpression. By contrast, leaf aromatic amino acid concentrations were greater in MYB165‐overexpressing poplars. Our findings indicate that MYB165 is a major repressor of the flavonoid and phenylpropanoid pathway in poplar, and may also affect the shikimate pathway. The coordinated action of repressor and activator MYBs could be important for the fine tuning of proanthocyanidin biosynthesis during development or following stress.
Significance Statement
Proanthocyanidins are important phenolic plant metabolites with key adaptive roles, and that can be both developmentally regulated and stress‐induced. We describe two poplar MYB proteins that directly repress biosynthesis of proanthocyanidins and also influence other phenolic pathways in poplar, contributing more complexity to the network of transcriptional regulators of poplar phenolic secondary metabolism.
Despite the phylogenetic distance between plants and insects, these two groups of organisms produce some secondary metabolites in common. Identical structures belonging to chemical classes such as ...the simple monoterpenes and sesquiterpenes, iridoid monoterpenes, cyanogenic glycosides, benzoic acid derivatives, benzoquinones and naphthoquinones are sometimes found in both plants and insects. In addition, very similar glucohydrolases involved in activating two-component defenses, such as glucosinolates and cyanogenic glycosides, occur in both plants and insects. Although this trend was first noted many years ago, researchers have long struggled to find convincing explanations for such co-occurrence. In some cases, identical compounds may be produced by plants to interfere with their function in insects. In others, plant and insect compounds may simply have parallel functions, probably in defense or attraction, and their co-occurrence is a coincidence. The biosynthetic origin of such co-occurring metabolites may be very different in insects as compared to plants. Plants and insects may have different pathways to the same metabolite, or similar sequences of intermediates, but different enzymes. Further knowledge of the ecological roles and biosynthetic pathways of secondary metabolites may shed more light on why plants and insects produce identical substances.
The pine weevil (Hylobius abietis), a major pest of conifer forests throughout Europe, feeds on the bark and cambium, tissues rich in terpenoid resins that are toxic to many insect herbivores. Here, ...we report the ability of the pine weevil gut microbiota to degrade the diterpene acids of Norway spruce. The diterpene acid levels present in ingested bark were substantially reduced on passage through the pine weevil gut. This reduction was significantly less upon antibiotic treatment, and supplementing the diet with gut suspensions from untreated insects restored the ability to degrade diterpenes. In addition, cultured bacteria isolated from pine weevil guts were shown to degrade a Norway spruce diterpene acid. In a metagenomic survey of the insect's bacterial community, we were able to annotate several genes of a previously described diterpene degradation (dit) gene cluster. Antibiotic treatment disrupted the core bacterial community of H. abietis guts and eliminated nearly all dit genes concordant with its reduction in diterpene degradation. Pine weevils reared on an artificial diet spiked with diterpenes, but without antibiotics, were found to lay more eggs with a higher hatching rate than weevils raised on diets with antibiotics or without diterpenes. These results suggest that gut symbionts contribute towards host fitness, but not by detoxification of diterpenes, as these compounds do not show toxic effects with or without antibiotics. Rather the ability to thrive in a terpene‐rich environment appears to allow gut microbes to benefit the weevil in other ways, such as increasing the nutritional properties of their diet.
Plants respond to herbivore attack by emitting complex mixtures of volatile compounds that attract herbivore enemies, both predators and parasitoids. Here, we explore whether these mixtures provide ...significant value as information cues in herbivore enemy attraction. Our survey indicates that blends of volatiles released from damaged plants are frequently specific depending on the type of herbivore and its age, abundance and feeding guild. The sensory perception of plant volatiles by herbivore enemies is also specific, according to the latest evidence from studies of insect olfaction. Thus, enemies do exploit the detailed information provided by plant volatile mixtures in searching for their prey or hosts, but this varies with the diet breadth of the enemy.
Like many other plant defense compounds, glucosinolates are present constitutively in plant tissues, but are also induced to higher levels by herbivore attack. Of the major glucosinolate types, ...indolic glucosinolates are most frequently induced regardless of the type of herbivore involved. Over 90% of previous studies found that herbivore damage to glucosinolate-containing plants led to an increased accumulation of indolic glucosinolates at levels ranging up to 20-fold. Aliphatic and aromatic glucosinolates are also commonly induced by herbivores, though usually at much lower magnitudes than indolic glucosinolates, and aliphatic and aromatic glucosinolates may even undergo declines following herbivory. The glucosinolate defense system also requires another partner, the enzyme myrosinase, to hydrolyze the parent glucosinolates into biologically active derivatives. Much less is known about myrosinase induction after herbivory compared to glucosinolate induction, and no general trends are evident. However, it is clear that insect feeding stimulates the formation of various myrosinase associated proteins whose function is not yet understood. The biochemical mechanism of glucosinolate induction involves a jasmonate signaling cascade that leads eventually to increases in the transcript levels of glucosinolate biosynthetic genes. Several recently described transcription factors controlling glucosinolate biosynthesis are activated by herbivory or wounding. Herbivore induction of glucosinolates has sometimes been demonstrated to increase protection against subsequent herbivore attack, but more research is needed to evaluate the costs and benefits of this phenomenon.
• Poplar trees synthesize flavan-3-ols (catechin and proanthocyanidins) as a defense against foliar rust fungi, but the regulation of this defense response is poorly understood. Here, we investigated ...the role of hormones in regulating flavan-3-ol accumulation in poplar during rust infection.
• We profiled levels of defense hormones, signaling genes, and flavan-3-ol metabolites in black poplar leaves at different stages of rust infection. Hormone levels were manipulated by external sprays, genetic engineering, and drought to reveal their role in rust fungal defenses.
• Levels of salicylic acid (SA), jasmonic acid, and abscisic acid increased in rust-infected leaves and activated downstream signaling, with SA levels correlating closely with those of flavan-3-ols. Pretreatment with the SA analog benzothiadiazole increased flavan-3-ol accumulation by activating the MYB–bHLH–WD40 complex and reduced rust proliferation. Furthermore, transgenic poplar lines overproducing SA exhibited higher amounts of flavan-3-ols constitutively via the same transcriptional activation mechanism. These findings suggest a strong association among SA, flavan-3-ol biosynthesis, and rust resistance in poplars. Abscisic acid also promoted poplar defense against rust infection, but likely through stomatal immunity independent of flavan-3-ols. Jasmonic acid did not confer any apparent defense responses to the fungal pathogen.
• We conclude that SA activates flavan-3-ol biosynthesis in poplar against rust infection.
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