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1.
Sci Adv ; 4(5): eaar4767, 2018 05.
Article in English | MEDLINE | ID: mdl-29774237

ABSTRACT

Herbivore-induced plant volatiles (HIPVs) can mediate tritrophic interactions by attracting natural enemies of insect herbivores such as predators and parasitoids. Whether HIPVs can also mediate tritrophic interactions by influencing the attractiveness of the herbivores themselves remains unknown. We explored this question by studying the role of indole, a common HIPV in the plant kingdom. We found that herbivory-induced indole increases the recruitment of the solitary endoparasitoid Microplitis rufiventris to maize plants that are induced by Spodoptera littoralis caterpillars. Surprisingly, however, indole reduces parasitoid recruitment when the caterpillars themselves are present on the plants. Further experiments revealed that indole exposure renders S. littoralis caterpillars unattractive to M. rufiventris, leading to an overall reduction in attractiveness of plant-herbivore complexes. Furthermore, indole increases S. littoralis resistance and decreases M. rufiventris parasitization success. S. littoralis caterpillars are repelled by indole in the absence of M. rufiventris but specifically stop avoiding the volatile in the presence of the parasitoid. Our study shows how an HIPV can undermine tritrophic interactions by reducing the suitability and attractiveness of caterpillars to parasitoids.


Subject(s)
Herbivory , Host-Parasite Interactions , Smell , Volatile Organic Compounds , Disease Resistance , Indoles , Insect Repellents , Odorants , Plant Diseases/parasitology , Plant Physiological Phenomena , Plants/chemistry , Plants/parasitology
2.
Nat Commun ; 6: 6273, 2015 Feb 16.
Article in English | MEDLINE | ID: mdl-25683900

ABSTRACT

Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.


Subject(s)
Herbivory/drug effects , Indoles/pharmacology , Volatile Organic Compounds/pharmacology , Zea mays/physiology , Abscisic Acid/biosynthesis , Animals , Cyclopentanes/metabolism , Mutation/genetics , Oxylipins/metabolism , Plant Growth Regulators/pharmacology , Terpenes/pharmacology , Zea mays/drug effects
3.
Plant Cell Environ ; 38(6): 1081-93, 2015 Jun.
Article in English | MEDLINE | ID: mdl-25293400

ABSTRACT

Plant defences vary in space and time, which may translate into specific herbivore-foraging patterns and feeding niche differentiation. To date, little is known about the effect of secondary metabolite patterning on within-plant herbivore foraging. We investigated how variation in the major maize secondary metabolites, 1,4-benzoxazin-3-one derivatives (BXDs), affects the foraging behaviour of two leaf-chewing herbivores. BXD levels varied substantially within plants. Older leaves had higher levels of constitutive BXDs while younger leaves were consistently more inducible. These differences were observed independently of plant age, even though the concentrations of most BXDs declined markedly in older plants. Larvae of the well-adapted maize pest Spodoptera frugiperda preferred and grew better on young inducible leaves irrespective of plant age, while larvae of the generalist Spodoptera littoralis preferred and tended to grow better on old leaves. In BXD-free mutants, the differences in herbivore weight gain between old and young leaves were absent for both species, and leaf preferences of S. frugiperda were attenuated. In contrast, S. littoralis foraging patterns were not affected. In summary, our study shows that plant secondary metabolites differentially affect performance and foraging of adapted and non-adapted herbivores and thereby likely contribute to feeding niche differentiation.


Subject(s)
Benzoxazines/analysis , Herbivory , Zea mays/chemistry , Age Factors , Animals , Benzoxazines/metabolism , Ecosystem , Larva , Plant Leaves/chemistry , Plant Leaves/metabolism , Spodoptera/physiology , Zea mays/metabolism
4.
Insects ; 5(3): 499-512, 2014 Jun 30.
Article in English | MEDLINE | ID: mdl-26462821

ABSTRACT

Sex pheromones have rarely been studied in parasitoids, and it remains largely unknown how male and female parasitoids locate each other. We investigated possible attraction (and repellency) between the sexes of two braconid wasps belonging to the same genus, the gregarious parasitoid, Cotesia glomerata (L.), and the solitary parasitoid, Cotesia marginiventris (Cresson). Males of both species were strongly attracted to conspecific virgin females. Interestingly, in C. glomerata, the males were repelled by mated females, as well as by males of their own species. This repellency of mated females was only evident hours after mating, implying a change in pheromone composition. Males of C. marginiventris were also no longer attracted, but not repelled, by mated females. Females of both species showed no attraction to the odors of conspecific individuals, male or female, and C. glomerata females even appeared to be repelled by mated males. Moreover, the pheromones were found to be highly specific, as males were not attracted by females of the other species. Males of Cotesia glomerata even avoided the pheromones of female Cotesia marginiventris, indicating the recognition of non-conspecific pheromones. We discuss these unique responses in the context of optimal mate finding strategies in parasitoids.

5.
Front Plant Sci ; 4: 209, 2013.
Article in English | MEDLINE | ID: mdl-23825475

ABSTRACT

Plants under herbivore attack emit volatile organic compounds (VOCs) that can serve as foraging cues for natural enemies. Adult females of Lepidoptera, when foraging for host plants to deposit eggs, are commonly repelled by herbivore-induced VOCs, probably to avoid competition and natural enemies. Their larval stages, on the other hand, have been shown to be attracted to inducible VOCs. We speculate that this contradicting behavior of lepidopteran larvae is due to a need to quickly find a new suitable host plant if they have fallen to the ground. However, once they are on a plant they might avoid the sites with fresh damage to limit competition and risk of cannibalism by conspecifics, as well as exposure to natural enemies. To test this we studied the effect of herbivore-induced VOCs on the attraction of larvae of the moth Spodoptera littoralis and on their feeding behavior. The experiments further considered the importance of previous feeding experience on the responses of the larvae. It was confirmed that herbivore-induced VOCs emitted by maize plants are attractive to the larvae, but exposure to the volatiles decreased the growth rate of caterpillars at early developmental stages. Larvae that had fed on maize previously were more attracted by VOCs of induced maize than larvae that had fed on artificial diet. At relatively high concentrations synthetic green leaf volatiles, indicative of fresh damage, also negatively affected the growth rate of caterpillars, but not at low concentrations. In all cases, feeding by the later stages of the larvae was not affected by the VOCs. The results are discussed in the context of larval foraging behavior under natural conditions, where there may be a trade-off between using available host plant signals and avoiding competitors and natural enemies.

6.
PLoS One ; 8(6): e62299, 2013.
Article in English | MEDLINE | ID: mdl-23840295

ABSTRACT

cis-Jasmone (CJ) is a natural plant product that activates defence against herbivores in model and crop plants. In this study, we investigated whether CJ could prime defence in maize, Zea mays, against the leafhopper, Cicadulina storeyi, responsible for the transmission of maize streak virus (MSV). Priming occurs when a pre-treatment, in this case CJ, increases the potency and speed of a defence response upon subsequent attack on the plant. Here, we tested insect responses to plant volatile organic compounds (VOCs) using a Y-tube olfactometer bioassay. Our initial experiments showed that, in this system, there was no significant response of the herbivore to CJ itself and no difference in response to VOCs collected from unexposed plants compared to CJ exposed plants, both without insects. VOCs were then collected from C. storeyi-infested maize seedlings with and without CJ pre-treatment. The bioassay revealed a significant preference by this pest for VOCs from infested seedlings without the CJ pre-treatment. A timed series of VOC collections and bioassays showed that the effect was strongest in the first 22 h of insect infestation, i.e. before the insects had themselves induced a change in VOC emission. Chemical analysis showed that treatment of maize seedlings with CJ, followed by exposure to C. storeyi, led to a significant increase in emission of the defensive sesquiterpenes (E)-(1R,9S)-caryophyllene, (E)-α-bergamotene, (E)-ß-farnesene and (E)-4,8-dimethyl-1,3,7-nonatriene, known to act as herbivore repellents. The chemical analysis explains the behavioural effects observed in the olfactometer, as the CJ treatment caused plants to emit a blend of VOCs comprising more of the repellent components in the first 22 h of insect infestation than control plants. The speed and potency of VOC emission was increased by the CJ pre-treatment. This is the first indication that CJ can prime plants for enhanced production of defensive VOCs antagonist towards herbivores.


Subject(s)
Cyclopentanes/pharmacology , Oxylipins/pharmacology , Volatile Organic Compounds/metabolism , Zea mays/drug effects , Zea mays/metabolism , Animals , Hemiptera/physiology , Zea mays/physiology
7.
Proc Natl Acad Sci U S A ; 110(14): 5707-12, 2013 Apr 02.
Article in English | MEDLINE | ID: mdl-23509266

ABSTRACT

Insect-induced defenses occur in nearly all plants and are regulated by conserved signaling pathways. As the first described plant peptide signal, systemin regulates antiherbivore defenses in the Solanaceae, but in other plant families, peptides with analogous activity have remained elusive. In the current study, we demonstrate that a member of the maize (Zea mays) plant elicitor peptide (Pep) family, ZmPep3, regulates responses against herbivores. Consistent with being a signal, expression of the ZmPROPEP3 precursor gene is rapidly induced by Spodoptera exigua oral secretions. At concentrations starting at 5 pmol per leaf, ZmPep3 stimulates production of jasmonic acid, ethylene, and increased expression of genes encoding proteins associated with herbivory defense. These include proteinase inhibitors and biosynthetic enzymes for production of volatile terpenes and benzoxazinoids. In accordance with gene expression data, plants treated with ZmPep3 emit volatiles similar to those from plants subjected to herbivory. ZmPep3-treated plants also exhibit induced accumulation of the benzoxazinoid phytoalexin 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside. Direct and indirect defenses induced by ZmPep3 contribute to resistance against S. exigua through significant reduction of larval growth and attraction of Cotesia marginiventris parasitoids. ZmPep3 activity is specific to Poaceous species; however, peptides derived from PROPEP orthologs identified in Solanaceous and Fabaceous plants also induce herbivory-associated volatiles in their respective species. These studies demonstrate that Peps are conserved signals across diverse plant families regulating antiherbivore defenses and are likely to be the missing functional homologs of systemin outside of the Solanaceae.


Subject(s)
Gene Expression Regulation, Plant/drug effects , Immunity, Innate/immunology , Protein Precursors/metabolism , Signal Transduction/immunology , Zea mays/chemistry , Zea mays/immunology , Animals , Bodily Secretions/metabolism , Cyclopentanes/metabolism , Ethylenes/metabolism , Gene Expression Regulation, Plant/immunology , Herbivory/immunology , Host-Parasite Interactions , Oxylipins/metabolism , Protease Inhibitors/metabolism , Signal Transduction/genetics , Spodoptera/chemistry
8.
J Chromatogr A ; 1292: 151-9, 2013 May 31.
Article in English | MEDLINE | ID: mdl-23274073

ABSTRACT

The response of Arabidopsis to stress caused by mechanical wounding was chosen as a model to compare the performances of high resolution quadrupole-time-of-flight (Q-TOF) and single stage Orbitrap (Exactive Plus) mass spectrometers in untargeted metabolomics. Both instruments were coupled to ultra-high pressure liquid chromatography (UHPLC) systems set under identical conditions. The experiment was divided in two steps: the first analyses involved sixteen unwounded plants, half of which were spiked with pure standards that are not present in Arabidopsis. The second analyses compared the metabolomes of mechanically wounded plants to unwounded plants. Data from both systems were extracted using the same feature detection software and submitted to unsupervised and supervised multivariate analysis methods. Both mass spectrometers were compared in terms of number and identity of detected features, capacity to discriminate between samples, repeatability and sensitivity. Although analytical variability was lower for the UHPLC-Q-TOF, generally the results for the two detectors were quite similar, both of them proving to be highly efficient at detecting even subtle differences between plant groups. Overall, sensitivity was found to be comparable, although the Exactive Plus Orbitrap provided slightly lower detection limits for specific compounds. Finally, to evaluate the potential of the two mass spectrometers for the identification of unknown markers, mass and spectral accuracies were calculated on selected identified compounds. While both instruments showed excellent mass accuracy (<2.5ppm for all measured compounds), better spectral accuracy was recorded on the Q-TOF. Taken together, our results demonstrate that comparable performances can be obtained at acquisition frequencies compatible with UHPLC on Q-TOF and Exactive Plus MS, which may thus be equivalently used for plant metabolomics.


Subject(s)
Arabidopsis/metabolism , Chromatography, High Pressure Liquid/instrumentation , Mass Spectrometry/instrumentation , Metabolomics/instrumentation , Arabidopsis/chemistry , Multivariate Analysis
9.
Ecol Lett ; 15(1): 55-64, 2012 Jan.
Article in English | MEDLINE | ID: mdl-22070646

ABSTRACT

The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.


Subject(s)
Coleoptera/physiology , Zea mays/metabolism , Adaptation, Physiological , Animals , Feeding Behavior , Nutritive Value , Phenols/metabolism , Plant Roots/metabolism
10.
Plant Physiol ; 157(1): 317-27, 2011 Sep.
Article in English | MEDLINE | ID: mdl-21730199

ABSTRACT

Benzoxazinoids (BXs), such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. The first step in BX biosynthesis converts indole-3-glycerol phosphate into indole. In maize (Zea mays), this reaction is catalyzed by either BENZOXAZINELESS1 (BX1) or INDOLE GLYCEROL PHOSPHATE LYASE (IGL). The Bx1 gene is under developmental control and is mainly responsible for BX production, whereas the Igl gene is inducible by stress signals, such as wounding, herbivory, or jasmonates. To determine the role of BXs in defense against aphids and fungi, we compared basal resistance between Bx1 wild-type and bx1 mutant lines in the igl mutant background, thereby preventing BX production from IGL. Compared to Bx1 wild-type plants, BX-deficient bx1 mutant plants allowed better development of the cereal aphid Rhopalosiphum padi, and were affected in penetration resistance against the fungus Setosphaeria turtica. At stages preceding major tissue disruption, R. padi and S. turtica elicited increased accumulation of DIMBOA-glucoside, DIMBOA, and 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one-glucoside (HDMBOA-glc), which was most pronounced in apoplastic leaf extracts. Treatment with the defense elicitor chitosan similarly enhanced apoplastic accumulation of DIMBOA and HDMBOA-glc, but repressed transcription of genes controlling BX biosynthesis downstream of BX1. This repression was also obtained after treatment with the BX precursor indole and DIMBOA, but not with HDMBOA-glc. Furthermore, BX-deficient bx1 mutant lines deposited less chitosan-induced callose than Bx1 wild-type lines, whereas apoplast infiltration with DIMBOA, but not HDMBOA-glc, mimicked chitosan-induced callose. Hence, DIMBOA functions as a defense regulatory signal in maize innate immunity, which acts in addition to its well-characterized activity as a biocidal defense metabolite.


Subject(s)
Aphids/physiology , Benzoxazines/metabolism , Fungi/physiology , Immunity, Innate , Zea mays/immunology , Animals , DNA, Complementary/genetics , Genes, Plant , RNA, Plant/isolation & purification , Real-Time Polymerase Chain Reaction , Transcription, Genetic , Zea mays/genetics , Zea mays/parasitology
11.
Phytochemistry ; 72(14-15): 1838-47, 2011 Oct.
Article in English | MEDLINE | ID: mdl-21658734

ABSTRACT

Maize plants respond to feeding by arthropod herbivores by producing a number of secondary plant compounds, including volatile organic compounds (VOCs). These herbivore-induced VOCs are not only known to attract natural enemies of the herbivores, but they may also prime inducible defences in neighbouring plants, resulting in stronger and faster defence responses in these VOC-exposed plants. Among the compounds that cause this priming effect, green leaf volatiles (GLVs) have received particular attention, as they are ubiquitous and rapidly emitted upon damage. In this study, we investigated their effects under realistic conditions by applying specially devised dispensers to release four synthetic GLVs at physiologically relevant concentrations in a series of experiments in maize fields. We compared the VOC emission of GLV-exposed maize plants to non-exposed plants and monitored the attraction of herbivores and predators, as well as parasitism of the caterpillar Spodoptera frugiperda, the most common herbivore in the experimental maize fields. We found that maize plants that were exposed to GLVs emitted increased quantities of sesquiterpenes compared to non-exposed plants. In several replicates, herbivorous insects, such as adult Diabrotica beetles and S. frugiperda larvae, were observed more frequently in GLV-treated plots and caused more damage to GLV-exposed plants than to non-exposed plants. Parasitism of S. frugiperda was only weakly affected by GLVs and overall parasitism rates of S. frugiperda were similar in GLV-exposed and non-exposed plots. The effects on insect presence depended on the distance from the GLV-dispensers at which the plants were located. The results are discussed in the context of strategies to improve biological control by enhancing plant-mediated attraction of natural enemies.


Subject(s)
Coleoptera/drug effects , Oils, Volatile/pharmacology , Pest Control, Biological/methods , Sesquiterpenes/metabolism , Spodoptera/drug effects , Zea mays/drug effects , Animals , Coleoptera/physiology , Herbivory/drug effects , Mexico , Oils, Volatile/chemistry , Plant Diseases/parasitology , Plant Leaves/chemistry , Spodoptera/physiology , Volatilization , Zea mays/chemistry , Zea mays/parasitology , Zea mays/physiology
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