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1.
Plant Cell Environ ; 42(12): 3308-3325, 2019 12.
Article in English | MEDLINE | ID: mdl-31330571

ABSTRACT

Plants that are subject to insect herbivory emit a blend of so-called herbivore-induced plant volatiles (HIPVs), of which only a few serve as cues for the carnivorous enemies to locate their host. We lack understanding which HIPVs are reliable indicators of insect herbivory. Here, we take a modelling approach to elucidate which physicochemical and physiological properties contribute to the information value of a HIPV. A leaf-level HIPV synthesis and emission model is developed and parameterized to poplar. Next, HIPV concentrations within the canopy are inferred as a function of dispersion, transport and chemical degradation of the compounds. We show that the ability of HIPVs to reveal herbivory varies from almost perfect to no better than chance and interacts with canopy conditions. Model predictions matched well with leaf-emission measurements and field and laboratory assays. The chemical class a compound belongs to predicted the signalling ability of a compound only to a minor extent, whereas compound characteristics such as its reaction rate with atmospheric oxidants, biosynthesis rate upon herbivory and volatility were much more important predictors. This study shows the power of merging fields of plant-insect interactions and atmospheric chemistry research to increase our understanding of the ecological significance of HIPVs.


Subject(s)
Herbivory/physiology , Insecta/physiology , Volatile Organic Compounds/metabolism , Animals , Models, Biological , Plant Leaves/physiology , Populus/physiology
2.
Sci Rep ; 9(1): 7714, 2019 05 22.
Article in English | MEDLINE | ID: mdl-31118456

ABSTRACT

Herbivory is well known to trigger increased emission of volatile organic compounds (VOCs) from plants, but we know little about the responses of mature trees. We measured the volatiles emitted by leaves of old-growth black poplar (Populus nigra) trees after experimental damage by gypsy moth (Lymantria dispar) caterpillars in a floodplain forest, and studied the effect of herbivory on the transcript abundance of two genes involved in the biosynthesis of VOCs, and the accumulation of defence phytohormones. Herbivory significantly increased volatile emission from the experimentally damaged foliage, but not from adjacent undamaged leaves in the damaged branches (i.e., no systemic response). Methylbutyraldoximes, 4,8-dimethyl-1,3,7-nonatriene (DMNT), (Z)-3-hexenol and (E)-ß-ocimene, amongst other compounds, were found to be important in distinguishing the blend of herbivore-damaged vs. undamaged leaves. Herbivory also increased expression of PnTPS3 (described here for the first time) and PnCYP79D6-v4 genes at the damaged sites, these genes encode for an (E)-ß-ocimene synthase and a P450 enzyme involved in aldoxime formation, respectively, demonstrating de novo biosynthesis of the volatiles produced. Herbivore-damaged leaves had significantly higher levels of jasmonic acid and its conjugate (-)-jasmonic acid-isoleucine. This study shows that mature trees in the field have a robust response to herbivory, producing induced volatiles at the damaged sites even after previous natural herbivory and under changing environmental conditions, however, further studies are needed to establish whether the observed absence of systemic responses is typical of mature poplar trees or if specific conditions are required for their induction.


Subject(s)
Herbivory , Populus/physiology , Volatile Organic Compounds/analysis , Animals , Cyclopentanes/analysis , Feeding Behavior , Genes, Plant , Larva , Moths/growth & development , Oxylipins/analysis , Plant Leaves/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , Populus/genetics
3.
Insect Biochem Mol Biol ; 78: 39-49, 2016 11.
Article in English | MEDLINE | ID: mdl-27503687

ABSTRACT

The survival of insect herbivores on chemically defended plants may often depend on their ability to metabolize these defense compounds. However, only little knowledge is available on how insects actually process most plant defense compounds. We investigated the metabolism of salicinoids, a major group of phenolic glycosides in poplar and willow species, by a generalist herbivore, the gypsy moth (Lymantria dispar). Seven salicinoid metabolites identified in gypsy moth caterpillar feces were mostly conjugates with glucose, cysteine or glycine. Two of the glucosides were phosphorylated, a feature not previously reported for insect metabolites of plant defense compounds. The origins of these metabolites were traced to specific moieties of three major poplar salicinoids ingested, salicin, salicortin and tremulacin. Based on the observed metabolite patterns we were able to deduce the initial steps of salicinoid breakdown in L. dispar guts, which involves cleavage of ester bonds. The conjugated molecules were effectively eliminated within 24 h after ingestion. Some of the initial breakdown products (salicin and catechol) demonstrated negative effects on insect growth and survival in bioassays on artificial diets. Gypsy moth caterpillars with prior feeding experience on salicinoid-containing poplar foliage converted salicinoids to the identified metabolites more efficiently than caterpillars pre-fed an artificial diet. The majority of the metabolites we identified were also produced by other common poplar-feeding insects. The conversion of plant defenses like salicinoids to a variety of water-soluble sugar, phosphate and amino acid conjugates and their subsequent excretion fits the general detoxification strategy found in insect herbivores and other animals.


Subject(s)
Benzyl Alcohols/metabolism , Glucosides/metabolism , Herbivory , Moths/physiology , Populus/chemistry , Animals , Feeding Behavior , Larva/growth & development , Larva/metabolism , Moths/growth & development , Plant Leaves/chemistry , Tissue Distribution
4.
BMC Plant Biol ; 14: 304, 2014 Nov 28.
Article in English | MEDLINE | ID: mdl-25429804

ABSTRACT

BACKGROUND: The role of herbivore-induced plant volatiles as signals mediating the attraction of herbivore enemies is a well-known phenomenon. Studies with short-lived herbaceous plant species have shown that various biotic and abiotic factors can strongly affect the quantity, composition and timing of volatile emission dynamics. However, there is little knowledge on how these factors influence the volatile emission of long-lived woody perennials. The aim of this study was to investigate the temporal dynamics of herbivore-induced volatile emission of black poplar (Populus nigra) through several day-night cycles following the onset of herbivory. We also determined the influence of different herbivore species, caterpillars of the gypsy moth (Lymantria dispar) and poplar hawkmoth (Laothoe populi), and different herbivore developmental stages on emission. RESULTS: The emission dynamics of major groups of volatile compounds differed strikingly in response to the timing of herbivory and the day-night cycle. The emission of aldoximes, salicyl aldehyde, and to a lesser extent, green leaf volatiles began shortly after herbivore attack and ceased quickly after herbivore removal, irrespective of the day-night cycle. However, the emission of most terpenes showed a more delayed reaction to the start and end of herbivory, and emission was significantly greater during the day compared to the night. The identity of the caterpillar species caused only slight changes in emission, but variation in developmental stage had a strong impact on volatile emission with early instar L. dispar inducing more nitrogenous volatiles and terpenoids than late instar caterpillars of the same species. CONCLUSIONS: The results indicate that only a few of the many herbivore-induced black poplar volatiles are released in tight correlation with the timing of herbivory. These may represent the most reliable cues for herbivore enemies and, interestingly, have been shown in a recent study to be the best attractants for an herbivore enemy that parasitizes gypsy moth larvae feeding on black poplar.


Subject(s)
Moths/physiology , Populus/chemistry , Volatile Organic Compounds/metabolism , Animals , Circadian Rhythm , Cues , Herbivory , Larva , Plant Leaves/chemistry , Plant Leaves/physiology , Populus/immunology , Populus/physiology , Signal Transduction , Terpenes/isolation & purification , Terpenes/metabolism , Trees , Volatile Organic Compounds/isolation & purification
5.
J Chem Ecol ; 40(2): 150-8, 2014 Feb.
Article in English | MEDLINE | ID: mdl-24496605

ABSTRACT

Transgenic hybrid aspen (Populus tremula x tremuloides) overexpressing the MYB134 tannin regulatory gene show dramatically enhanced condensed tannin (proanthocyanidin) levels, as well as shifts in other phenolic metabolites. A series of insect bioassays with forest tent caterpillars (Malacosoma disstria) and gypsy moth (Lymantria dispar) caterpillars was carried out to determine how this metabolic shift affects food preference and performance of generalist tree-feeding lepidopterans. Both species showed a distinct preference for the high-tannin MYB134 overexpressor plants, and L. dispar performance was enhanced relative to controls. L. dispar reached greater pupal weight and showed reduced time to pupation when reared on the MYB134 overexpressing poplar. These results were unexpected since enhanced condensed tannin levels were predicted to act as feeding deterrents. However, the data may be explained by the observed decrease in the salicinoids (phenolic glycosides) salicortin and tremulacin that accompanied the upregulation of the condensed tannins in the transgenics. We conclude that for these two lepidopteran species, condensed tannin levels are unlikely to be a major determinant of caterpillar food preference or performance. However, our experiments show that overexpression of a single regulatory gene in transgenic aspen can have a significant impact on herbivorous insects.


Subject(s)
Herbivory , Lepidoptera/physiology , Plants, Genetically Modified/genetics , Populus/genetics , Tannins/genetics , Animals , Gene Expression Regulation, Plant , Genes, Plant , Plant Leaves/genetics , Plant Leaves/physiology , Plants, Genetically Modified/physiology , Populus/physiology , Tannins/metabolism , Trees/genetics , Trees/physiology , Up-Regulation
6.
Plant Cell Environ ; 37(8): 1909-23, 2014 Aug.
Article in English | MEDLINE | ID: mdl-24471487

ABSTRACT

After herbivory, plants release volatile organic compounds from damaged foliage as well as from nearby undamaged leaves that attract herbivore enemies. Little is known about what controls the volatile emission differences between damaged and undamaged tissues and how these affect the orientation of herbivore enemies. We investigated volatile emission from damaged and adjacent undamaged foliage of black poplar (Populus nigra) after herbivory by gypsy moth (Lymantria dispar) caterpillars and determined the compounds mediating the attraction of the gypsy moth parasitoid Glyptapanteles liparidis (Braconidae). Female parasitoids were more attracted to gypsy moth-damaged leaves than to adjacent non-damaged leaves. The most characteristic volatiles of damaged versus neighbouring undamaged leaves included terpenes, green leaf volatiles and nitrogen-containing compounds, such as aldoximes and nitriles. Electrophysiological recordings and olfactometer bioassays demonstrated the importance of nitrogenous volatiles. Under field conditions, parasitic Hymenoptera were more attracted to traps baited with these substances than most other compounds. The differences in volatile emission profiles between damaged and undamaged foliage appear to be regulated by jasmonate signalling and the local activation of volatile biosynthesis. We conclude that characteristic volatiles from damaged black poplar foliage are essential cues enabling parasitoids to find their hosts.


Subject(s)
Herbivory , Moths/physiology , Populus/chemistry , Volatile Organic Compounds/chemistry , Wasps/physiology , Animals , Female , Genes, Plant , Genotype , Larva , Moths/parasitology , Pheromones/chemistry , Plant Leaves/chemistry , Plant Leaves/physiology , Populus/genetics , Populus/physiology , Terpenes/chemistry
7.
Plant Cell ; 25(11): 4737-54, 2013 Nov.
Article in English | MEDLINE | ID: mdl-24220631

ABSTRACT

Aldoximes are known as floral and vegetative plant volatiles but also as biosynthetic intermediates for other plant defense compounds. While the cytochrome P450 monooxygenases (CYP) from the CYP79 family forming aldoximes as biosynthetic intermediates have been intensively studied, little is known about the enzymology of volatile aldoxime formation. We characterized two P450 enzymes, CYP79D6v3 and CYP79D7v2, which are involved in herbivore-induced aldoxime formation in western balsam poplar (Populus trichocarpa). Heterologous expression in Saccharomyces cerevisiae revealed that both enzymes produce a mixture of different aldoximes. Knockdown lines of CYP79D6/7 in gray poplar (Populus × canescens) exhibited a decreased emission of aldoximes, nitriles, and alcohols, emphasizing that the CYP79s catalyze the first step in the formation of a complex volatile blend. Aldoxime emission was found to be restricted to herbivore-damaged leaves and is closely correlated with CYP79D6 and CYP79D7 gene expression. The semi-volatile phenylacetaldoxime decreased survival and weight gain of gypsy moth (Lymantria dispar) caterpillars, suggesting that aldoximes may be involved in direct defense. The wide distribution of volatile aldoximes throughout the plant kingdom and the presence of CYP79 genes in all sequenced genomes of angiosperms suggest that volatile formation mediated by CYP79s is a general phenomenon in the plant kingdom.


Subject(s)
Cytochrome P-450 Enzyme System/metabolism , Herbivory , Populus/physiology , Volatile Organic Compounds/metabolism , Alcohols/metabolism , Animals , Cytochrome P-450 Enzyme System/genetics , Gene Expression Regulation, Plant , Gene Knockdown Techniques , Genome, Plant , Mortality , Moths/drug effects , Moths/growth & development , Moths/physiology , Nitriles/metabolism , Oximes/metabolism , Oximes/pharmacology , Phenylalanine/metabolism , Plant Leaves/genetics , Plant Leaves/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified , Populus/genetics , Populus/metabolism , Nicotiana/genetics , Nicotiana/metabolism , Volatile Organic Compounds/analysis
8.
J Chem Ecol ; 39(10): 1301-12, 2013 Oct.
Article in English | MEDLINE | ID: mdl-24154955

ABSTRACT

Species of the Salicaceae produce phenolic compounds that may function as anti-herbivore defenses. Levels of these compounds have been reported to increase upon herbivory, but only rarely have these changes in phenolics been studied under natural conditions. We profiled the phenolics of old-growth black poplar (Populus nigra L.) and studied the response to gypsy moth (Lymantria dispar L.) herbivory in two separate field experiments. In a first experiment, foliar phenolics of 20 trees were monitored over 4 weeks after caterpillar infestation, and in a second experiment the bark and foliar phenolics of a single tree were measured over a week. Of the major groups of phenolics, salicinoids (phenolic glycosides) showed no short term response to caterpillar feeding, but after 4 weeks they declined up to 40 % in herbivore damaged and adjacent undamaged leaves on the same branch when compared to leaves of control branches. Flavonol glycosides, low molecular weight flavan-3-ols, and condensed tannins were not affected by herbivory in the first experiment. However, in the single-tree experiment, foliar condensed tannins increased by 10-20 % after herbivory, and low molecular weight flavan-3-ols decreased by 10 % in the leaves but increased by 10 % in the bark. Despite 15 % experimental leaf area loss followed by a 5-fold increase in foliar jasmonate defense hormones, we found no evidence for substantial induction of phenolic defense compounds in old growth black poplar trees growing in a native stand. Thus, if phenolics in these trees function as defenses against herbivory, our results suggest that they act mainly as constitutive defenses.


Subject(s)
Herbivory , Moths/physiology , Phenols/metabolism , Populus/metabolism , Animals , Phenols/chemistry , Populus/chemistry
9.
Phytochemistry ; 72(9): 897-908, 2011 Jun.
Article in English | MEDLINE | ID: mdl-21492885

ABSTRACT

After herbivore damage, many plants increase their emission of volatile compounds, with terpenes usually comprising the major group of induced volatiles. Populus trichocarpa is the first woody species with a fully sequenced genome, enabling rapid molecular approaches towards characterization of volatile terpene biosynthesis in this and other poplar species. We identified and characterized four terpene synthases (PtTPS1-4) from P. trichocarpa which form major terpene compounds of the volatile blend induced by gypsy moth (Lymantria dispar) feeding. The enzymes were heterologously expressed and assayed with potential prenyl diphosphate substrates. PtTPS1 and PtTPS2 accepted only farnesyl diphosphate and produced (-)-germacrene D and (E,E)-α-farnesene as their major products, respectively. In contrast, PtTPS3 and PtTPS4 showed both mono- and sesquiterpene synthase activity. They produce the acyclic terpene alcohols linalool and nerolidol but exhibited opposite stereospecificity. qRT-PCR analysis revealed that the expression of the respective terpene synthase genes was induced after feeding of gypsy moth caterpillars. The TPS enzyme products may play important roles in indirect defense of poplar to herbivores and in mediating intra- and inter-plant signaling.


Subject(s)
Alkyl and Aryl Transferases/metabolism , Herbivory , Populus/enzymology , Terpenes/chemistry , Volatile Organic Compounds/chemistry , Amino Acid Sequence , Animals , Gene Expression Regulation, Plant , Molecular Sequence Data , Moths , Plant Leaves/chemistry , Plant Proteins/metabolism , Populus/chemistry
10.
Phytochemistry ; 72(13): 1497-509, 2011 Sep.
Article in English | MEDLINE | ID: mdl-21376356

ABSTRACT

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.


Subject(s)
Adaptation, Physiological , Glycosides , Phenols , Plant Diseases , Salicaceae/chemistry , Animals , Disease Resistance , Plant Leaves , Salicaceae/physiology
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