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1.  Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid 
Oecologia  2007;152(2):257-264.
The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.
doi:10.1007/s00442-006-0649-z
PMCID: PMC1915602  PMID: 17334787
Above-/below-ground interactions; Delia radicum; Glucosinolates; Plant–insect interactions; Trybliographa rapae
2.  Belowground induction by Delia radicum or phytohormones affect aboveground herbivore communities on field-grown broccoli 
Induced plant defence in response to phytophagous insects is a well described phenomenon. However, so far little is known about the effect of induced plant responses on subsequently colonizing herbivores in the field. Broccoli plants were induced in the belowground compartment using (i) infestation by the root-herbivore Delia radicum, (ii) root application of jasmonic acid (JA) or (iii) root application of salicylic acid (SA). The abundance of D. radicum and six aboveground herbivores displaying contrasting levels of host specialization were surveyed for 5 weeks. Our study showed that the response of herbivores was found to differ from one another, depending on the herbivore species, its degree of specialization and the root treatment. The abundance of the root herbivore D. radicum and particularly the number of emerging adults was decreased by both phytohormone treatments, while the number of D. radicum eggs was increased on conspecific infested plants. The root infestation exhibited moderate effects on the aboveground community. The abundance of the aphid Brevicoryne brassicae was strongly increased on D. radicum infested plants, but the other species were not impacted. Root hormone applications exhibited a strong effect on the abundance of specialist foliar herbivores. A higher number of B. brassicae and Pieris brassicae and a lower number of Plutella xylostella were found on JA treated plants. On SA treated plants we observed a decrease of the abundance of B. brassicae, Pi. rapae, and P. xylostella. Surprisingly, generalist species, Mamestra brassicae and Myzus persicae were not affected by root induction treatments. Finally, root treatments had no significant effect on either glucosinolate (GLS) profiles of the heads or on plant quality parameters. These results are discussed from the perspective of below- aboveground interactions and adaptations of phytophagous insects to induced plant responses according to their trophic specialization level.
doi:10.3389/fpls.2013.00305
PMCID: PMC3748748  PMID: 23970888
plant-mediated above-belowground interactions; induced plant defence; Brassica spp; root herbivory; phytohormones
3.  Identification of Biologically Relevant Compounds in Aboveground and Belowground Induced Volatile Blends 
Journal of Chemical Ecology  2010;36(9):1006-1016.
Plants under attack by aboveground herbivores emit complex blends of volatile organic compounds (VOCs). Specific compounds in these blends are used by parasitic wasps to find their hosts. Belowground induction causes shifts in the composition of aboveground induced VOC blends, which affect the preference of parasitic wasps. To identify which of the many volatiles in the complex VOC blends may explain parasitoid preference poses a challenge to ecologists. Here, we present a case study in which we use a novel bioinformatics approach to identify biologically relevant differences between VOC blends of feral cabbage (Brassica oleracea L.). The plants were induced aboveground or belowground with jasmonic acid (JA) and shoot feeding caterpillars (Pieris brassicae or P. rapae). We used Partial Least Squares—Discriminant Analysis (PLSDA) to integrate and visualize the relation between plant-emitted VOCs and the preference of female Cotesia glomerata. Overall, female wasps preferred JA-induced plants over controls, but they strongly preferred aboveground JA-induced plants over belowground JA-induced plants. PLSDA revealed that the emission of several monoterpenes was enhanced similarly in all JA-treated plants, whereas homoterpenes and sesquiterpenes increased exclusively in aboveground JA-induced plants. Wasps may use the ratio between these two classes of terpenes to discriminate between aboveground and belowground induced plants. Additionally, it shows that aboveground applied JA induces different VOC biosynthetic pathways than JA applied to the root. Our bioinformatic approach, thus, successfully identified which VOCs matched the preferences of the wasps in the various choice tests. Additionally, the analysis generated novel hypotheses about the role of JA as a signaling compound in aboveground and belowground induced responses in plants.
doi:10.1007/s10886-010-9844-9
PMCID: PMC2941087  PMID: 20737198
Aboveground-belowground interactions; Volatile organic compounds; Indirect defenses; Multivariate analysis; Terpenes; Jasmonic acid; Parasitoid preference; PLSDA
4.  Tracing Hidden Herbivores: Time-Resolved Non-Invasive Analysis of Belowground Volatiles by Proton-Transfer-Reaction Mass Spectrometry (PTR-MS) 
Journal of Chemical Ecology  2012;38(6):785-794.
Root herbivores are notoriously difficult to study, as they feed hidden in the soil. However, root herbivores may be traced by analyzing specific volatile organic compounds (VOCs) that are produced by damaged roots. These VOCs not only support parasitoids in the localization of their host, but also may help scientists study belowground plant-herbivore interactions. Herbivore-induced VOCs are usually analyzed by gas-chromatography mass spectrometry (GC-MS), but with this off-line method, the gases of interest need to be preconcentrated, and destructive sampling is required to assess the level of damage to the roots. In contrast to this, proton-transfer-reaction mass spectrometry (PTR-MS) is a very sensitive on-line, non-invasive method. PTR-MS already has been successfully applied to analyze VOCs produced by aboveground (infested) plant parts. In this review, we provide a brief overview of PTR-MS and illustrate how this technology can be applied to detect specific root-herbivore induced VOCs from Brassica plants. We also specify the advantages and disadvantages of PTR-MS analyses and new technological developments to overcome their limitations.
doi:10.1007/s10886-012-0129-3
PMCID: PMC3375075  PMID: 22592334
Chemical ecology; Root herbivory; Trace gas analysis; Induced indirect defense; Mass spectrometry; Volatile organic compound (VOC)
5.  Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles 
Plants produce volatile organic compounds (VOCs) in response to herbivore attack, and these VOCs can be used by parasitoids of the herbivore as host location cues. We investigated the behavioural responses of the parasitoid Cotesia vestalis to VOCs from a plant–herbivore complex consisting of cabbage plants (Brassica oleracea) and the parasitoids host caterpillar, Plutella xylostella. A Y-tube olfactometer was used to compare the parasitoids' responses to VOCs produced as a result of different levels of attack by the caterpillar and equivalent levels of mechanical damage. Headspace VOC production by these plant treatments was examined using gas chromatography–mass spectrometry. Cotesia vestalis were able to exploit quantitative and qualitative differences in volatile emissions, from the plant–herbivore complex, produced as a result of different numbers of herbivores feeding. Cotesia vestalis showed a preference for plants with more herbivores and herbivore damage, but did not distinguish between different levels of mechanical damage. Volatile profiles of plants with different levels of herbivores/herbivore damage could also be separated by canonical discriminant analyses. Analyses revealed a number of compounds whose emission increased significantly with herbivore load, and these VOCs may be particularly good indicators of herbivore number, as the parasitoid processes cues from its external environment.
doi:10.1098/rspb.2010.2725
PMCID: PMC3136836  PMID: 21270031
herbivore-induced plant volatiles; Hymenoptera; Lepidoptera; parasitoid host location; tritrophic; volatile organic compounds
6.  Flower vs. Leaf Feeding by Pieris brassicae: Glucosinolate-Rich Flower Tissues are Preferred and Sustain Higher Growth Rate 
Journal of Chemical Ecology  2007;33(10):1831-1844.
Interactions between butterflies and caterpillars in the genus Pieris and plants in the family Brassicaceae are among the best explored in the field of insect–plant biology. However, we report here for the first time that Pieris brassicae, commonly assumed to be a typical folivore, actually prefers to feed on flowers of three Brassica nigra genotypes rather than on their leaves. First- and second-instar caterpillars were observed to feed primarily on leaves, whereas late second and early third instars migrated via the small leaves of the flower branches to the flower buds and flowers. Once flower feeding began, no further leaf feeding was observed. We investigated growth rates of caterpillars having access exclusively to either leaves of flowering plants or flowers. In addition, we analyzed glucosinolate concentrations in leaves and flowers. Late-second- and early-third-instar P. brassicae caterpillars moved upward into the inflorescences of B. nigra and fed on buds and flowers until the end of the final (fifth) instar, after which they entered into the wandering stage, leaving the plant in search of a pupation site. Flower feeding sustained a significantly higher growth rate than leaf feeding. Flowers contained levels of glucosinolates up to five times higher than those of leaves. Five glucosinolates were identified: the aliphatic sinigrin, the aromatic phenyethylglucosinolate, and three indole glucosinolates: glucobrassicin, 4-methoxyglucobrassicin, and 4-hydroxyglucobrassicin. Tissue type and genotype were the most important factors affecting levels of identified glucosinolates. Sinigrin was by far the most abundant compound in all three genotypes. Sinigrin, 4-hydroxyglucobrassicin, and phenylethylglucosinolate were present at significantly higher levels in flowers than in leaves. In response to caterpillar feeding, sinigrin levels in both leaves and flowers were significantly higher than in undamaged plants, whereas 4-hydroxyglucobrassicin leaf levels were lower. Our results show that feeding on flower tissues, containing higher concentrations of glucosinolates, provides P. brassicae with a nutritional benefit in terms of higher growth rate. This preference appears to be in contrast to published negative effects of volatile glucosinolate breakdown products on the closely related Pieris rapae.
doi:10.1007/s10886-007-9350-x
PMCID: PMC2039843  PMID: 17828429
Herbivory; Lepidoptera; Pieridae; Myrosinase; Isothiocyanates; Nutrition; Brassica nigra
7.  Herbivore-induced maize leaf volatiles affect attraction and feeding behavior of Spodoptera littoralis caterpillars 
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.
doi:10.3389/fpls.2013.00209
PMCID: PMC3695448  PMID: 23825475
Spodoptera littoralis; green leaf volatiles; maize; larval foraging behavior; host plant suitability
8.  Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth 
Plant Signaling & Behavior  2008;3(2):91-98.
Many induced responses in plants are systemic. Therefore, root-induced responses may alter leaf quality for shoot herbivores. Previously, we found that root and shoot application of jasmonic acid (JA) to feral Brassica oleracea both induced glucosinolates in the leaves. However, the types of glucosinolates that increased in root- and shoot induced plants were different. Here we analyse whether primary metabolites, such as sugars and amino acids, are also differentially affected. Moreover, we test whether chemical differences in root- and shoot-induced plants differentially affect growth of the generalist Mamestra brassicae and the specialist Pieris rapae. Comprehensive analysis of glucosinolates, amino acid and sugars with principal component analysis revealed that leaf chemical profiles were affected both by JA application and by the organ that was induced. Shoot-induction increased indole glucosinolates, whereas root-induction induced aliphatic glucosinolates in the leaves. Leaves of shoot-induced plants had lower total sugar and total amino acid levels, whereas in root-induced plants only total sugar levels were significantly decreased. (Iso)leucine responded significantly different from the general trend, which allowed us to discuss the potential role of Myb transcription factors which are coordinating JA-induced glucosinolate and amino acid responses in Arabidopsis thaliana. Both M. brassicae and P. rapae grew the slowest on leaves of shoot-induced plants. M. brassicae growth and survival was also reduced on root-induced plants, whereas P. rapae growth on these plants was similar to that on controls. Specialist and generalist herbivores thus are differentially affected by the chemical changes after root and shoot-JA application.
PMCID: PMC2633990  PMID: 19516980
above-below ground interactions; amino acids; Brassica oleracea; glucosinolates; induced responses; jasmonic acid; Mamestra brassicae; Pieris rapae; sugars
9.  Priming of Production in Maize of Volatile Organic Defence Compounds by the Natural Plant Activator cis-Jasmone 
PLoS ONE  2013;8(6):e62299.
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)-β-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.
doi:10.1371/journal.pone.0062299
PMCID: PMC3694093  PMID: 23840295
10.  Degree of herbivore feeding damage as an important contributor to multitrophic plant-parasitoid signaling under climate change 
Plant Signaling & Behavior  2009;4(3):249-251.
Biogenic volatile organic compounds (VOCs) serve as signals mediating information between plants and their higher trophic level beneficials, such as parasitoids and predators of herbivores. We recently demonstrated with oilseed rape (Brassica napus L.) plants, herbivorous diamond-back moth (Plutella xylostella L. (Lepidoptera: Yponomeutidae)) larvae and Cotesia vestalis (Haliday) (Hymenoptera: Braconidae) parasitoids that atmospheric pollution, i.e., elevated ozone (O3), can disturb attraction of natural enemies by plant-emitted host-induced volatile cues. Additionally, we found that the degree of herbivore feeding damage is an important contributor to this O3 interference. Low feeding damage in herbivore-resistant plants was sufficient to attract C. vestalis females to host-damaged plants under ambient air, but this tritrophic signaling turned non-functional in the combination of low feeding damage and high O3 concentration. Here we present some additional data of how climate change factors may modify feeding patterns and growth of herbivores. We further discuss how the degree of herbivore feeding damage and the tritrophic signaling interaction relaying on the herbivore-induced VOCs from attacked plants might change through direct and indirect effects of increased levels of carbon dioxide, temperature and O3.
PMCID: PMC2652544  PMID: 19721765
volatile organic compounds; carbon dioxide; ozone; herbivore feeding; tritrophic interactions; oilseed rape; Lepidoptera; parasitoids; climate change
11.  Heterodera schachtii Nematodes Interfere with Aphid-Plant Relations on Brassica oleracea 
Journal of Chemical Ecology  2013;39:1193-1203.
Aboveground and belowground herbivore species modify plant defense responses differently. Simultaneous attack can lead to non-additive effects on primary and secondary metabolite composition in roots and shoots. We previously found that aphid (Brevicoryne brassicae) population growth on Brassica oleracea was reduced on plants that were infested with nematodes (Heterodera schachtii) prior (4 weeks) to aphid infestation. Here, we examined how infection with root-feeding nematodes affected primary and secondary metabolites in the host plant and whether this could explain the increase in aphid doubling time from 3.8 to 6.7 days. We hypothesized that the effects of herbivores on plant metabolites would depend on the presence of the other herbivore and that nematode-induced changes in primary metabolites would correlate with reduced aphid performance. Total glucosinolate concentration in the leaves was not affected by nematode presence, but the composition of glucosinolates shifted, as gluconapin concentrations were reduced, while gluconapoleiferin concentrations increased in plants exposed to nematodes. Aphid presence increased 4-methoxyglucobrassicin concentrations in leaves, which correlated positively with the number of aphids per plant. Nematodes decreased amino acid and sugar concentrations in the phloem. Aphid population doubling time correlated negatively with amino acids and glucosinolate levels in leaves, whereas these correlations were non-significant when nematodes were present. In conclusion, the effects of an herbivore on plant metabolites were independent of the presence of another herbivore. Nematode presence reduced aphid population growth and disturbed feeding relations between plants and aphids.
Electronic supplementary material
The online version of this article (doi:10.1007/s10886-013-0338-4) contains supplementary material, which is available to authorized users.
doi:10.1007/s10886-013-0338-4
PMCID: PMC3790247  PMID: 24014097
Heterodera; Brevicoryne; Brassica; Glucosinolates; Phloem; EDTA
12.  The role of spatial scale and intraspecific variation in secondary chemistry in host-plant location by Ceutorhynchus assimilis (Coleoptera: Curculionidae). 
To understand the ecological role of secondary plant compounds in host location by phytophagous insects it is important to consider attraction at different scales in natural populations. The cabbage seed weevil, Ceutorhynchus assimilis, which lays eggs in pods of crucifers where the larvae feed on seed, is attracted to purified extracts of specific glucosinolate-derived volatiles. We considered the possibility that C. assimilis adults are attracted to and preferentially attack patches of plants and/or individual plants producing these volatiles. Using discrete natural populations of Brassica oleracea and Brassica nigra, we found that oviposition was highest in populations of B. oleracea producing high amounts of 3-butenylglucosinolate. No links were found between the other glucosinolates, 2-propenylglucosinolate, 2-hydroxy-3-butenylglucosinolate, 1-indolylmethylglucosinolate or 1-methoxy-3-indolylmethylglucosinolate, and oviposition in B. oleracea. B. nigra, which contains only 2-propenylglucosinolate, was not attacked by C. assimilis. Within populations of B. oleracea, neither oviposition nor the number of seeds eaten was related to the glucosinolate profiles of individual plants. We suggest that C. assimilis adults use 3-butenylglucosinolate-derived volatiles to locate host populations, whereas other cues determine oviposition on individual plants. The consequences of these results for natural selection of glucosinolate phenotypes are discussed.
doi:10.1098/rspb.2001.1685
PMCID: PMC1088779  PMID: 11487403
13.  The cabbage aphid: a walking mustard oil bomb 
The cabbage aphid, Brevicoryne brassicae, has developed a chemical defence system that exploits and mimics that of its host plants, involving sequestration of the major plant secondary metabolites (glucosinolates). Like its host plants, the aphid produces a myrosinase (β-thioglucoside glucohydrolase) to catalyse the hydrolysis of glucosinolates, yielding biologically active products. Here, we demonstrate that aphid myrosinase expression in head/thoracic muscle starts during embryonic development and protein levels continue to accumulate after the nymphs are born. However, aphids are entirely dependent on the host plant for the glucosinolate substrate, which they store in the haemolymph. Uptake of a glucosinolate (sinigrin) was investigated when aphids fed on plants or an in vitro system and followed a different developmental pattern in winged and wingless aphid morphs. In nymphs of the wingless aphid morph, glucosinolate level continued to increase throughout the development to the adult stage, but the quantity in nymphs of the winged form peaked before eclosion (at day 7) and subsequently declined. Winged aphids excreted significantly higher amounts of glucosinolate in the honeydew when compared with wingless aphids, suggesting regulated transport across the gut. The higher level of sinigrin in wingless aphids had a significant negative impact on survival of a ladybird predator. Larvae of Adalia bipunctata were unable to survive when fed adult wingless aphids from a 1% sinigrin diet, but survived successfully when fed aphids from a glucosinolate-free diet (wingless or winged), or winged aphids from 1% sinigrin. The apparent lack of an effective chemical defence system in adult winged aphids possibly reflects their energetic investment in flight as an alternative predator avoidance mechanism.
doi:10.1098/rspb.2007.0237
PMCID: PMC2288485  PMID: 17623639
tritrophic interactions; chemical defences; convergent evolution; glucosinates
14.  Field Application of Entomopathogenic Nematodes for Control of Delia radicum in Collards 
Journal of Nematology  1992;24(3):374-378.
Control of Delia radicum (cabbage maggot) in field collards (Brassica oleracea) was compared after one or two applications of entomopathogenic nematodes, Steinernema carpocapsae (All strain) and Heterorhabditis bacterophora (HP88 strain), a single application of granular chlorpyrifos, and a water-only treatment. Nematodes were applied with a sprayer during the egg stage of first-generation D. radicum, and chlorpyrifos was hand placed around collard stems during the same period. A second nematode application was made 10 days later. Chlorpyrifos treatment resulted in fewer puparia per plant, less root damage and higher yield than all other treatments, including the control. Collard yield from nematode-treated beds did not differ from controls. These data indicate that, under these field conditions, the species or strains of entomopathogenic nematodes tested did not reduce the number of active cabbage maggots, nor did they prevent collard root damage.
PMCID: PMC2619292  PMID: 19283012
biological control; cabbage maggot; chlorpyrifos; collards; Delia radicum; entomopathogenic nematode; Heterorhabditis bacteriophora; nematode; Steinernema carpocapsae
15.  Crosstalk between above- and belowground herbivores is mediated by minute metabolic responses of the host Arabidopsis thaliana 
Journal of Experimental Botany  2012;63(17):6199-6210.
Plants are frequently under attack by multiple herbivores and can be infested at their shoots as well as their roots. As a consequence, plant metabolites are readily induced, mediated by phytohormones such as salicylic acid and jasmonic acid. Thereby, cross-talk between signal transduction pathways may occur if different herbivores attack the plant simultaneously. In turn, modifications in the plant metabolic pattern can affect herbivores infesting local and systemic tissue. Here, an integrative approach combining metabolomics and performance experiments was used to study the induction of plant metabolites in Arabidopsis thaliana by the specialist aphid Brevicoryne brassicae feeding on shoots and the generalist nematode Heterodera schachtii infesting root tissue. In contrast to most other studies, low infestation rates typical for the decisive early stages of infestation were used. Moreover, the consequences of induction responses on plant-mediated indirect interactions between these herbivores were investigated. In aphid-treated plants, several metabolites including glucosinolates, important defence compounds of Brassicaceae, were reduced in the shoot, but only minute changes took part in the systemic root tissue. Primary metabolites as well as phytohormones were not altered 3 days post infestation. In contrast, nematodes did not evoke significant metabolic alterations locally or systemically. In accordance, nematode presence did not affect aphid population growth, whereas aphids mediated a considerably reduced nematode infestation. These results demonstrate that plants respond in a very fine-tuned way to different challenges. Although they show only minute systemic responses to low herbivore stress, these changes can have pronounced effects on plant-mediated interactions between herbivores.
doi:10.1093/jxb/ers274
PMCID: PMC3481212  PMID: 23045608
Aphids; glucosinolates; induction; metabolomics; nematodes; phytohormones
16.  Egg Laying of Cabbage White Butterfly (Pieris brassicae) on Arabidopsis thaliana Affects Subsequent Performance of the Larvae 
PLoS ONE  2013;8(3):e59661.
Plant resistance to the feeding by herbivorous insects has recently been found to be positively or negatively influenced by prior egg deposition. Here we show how crucial it is to conduct experiments on plant responses to herbivory under conditions that simulate natural insect behaviour. We used a well-studied plant – herbivore system, Arabidopsis thaliana and the cabbage white butterfly Pieris brassicae, testing the effects of naturally laid eggs (rather than egg extracts) and allowing larvae to feed gregariously as they do naturally (rather than placing single larvae on plants). Under natural conditions, newly hatched larvae start feeding on their egg shells before they consume leaf tissue, but access to egg shells had no effect on subsequent larval performance in our experiments. However, young larvae feeding gregariously on leaves previously laden with eggs caused less feeding damage, gained less weight during the first 2 days, and suffered twice as high a mortality until pupation compared to larvae feeding on plants that had never had eggs. The concentration of the major anti-herbivore defences of A. thaliana, the glucosinolates, was not significantly increased by oviposition, but the amount of the most abundant member of this class, 4-methylsulfinylbutyl glucosinolate was 1.8-fold lower in larval-damaged leaves with prior egg deposition compared to damaged leaves that had never had eggs. There were also few significant changes in the transcript levels of glucosinolate metabolic genes, except that egg deposition suppressed the feeding-induced up-regulation of FMOGS-OX2, a gene encoding a flavin monooxygenase involved in the last step of 4-methylsulfinylbutyl glucosinolate biosynthesis. Hence, our study demonstrates that oviposition does increase A. thaliana resistance to feeding by subsequently hatching larvae, but this cannot be attributed simply to changes in glucosinolate content.
doi:10.1371/journal.pone.0059661
PMCID: PMC3602411  PMID: 23527243
17.  From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory 
PLoS ONE  2008;3(7):e2832.
Background
An understanding of the evolution of potential signals from plants to the predators of their herbivores may provide exciting examples of co-evolution among multiple trophic levels. Understanding the mechanism behind the attraction of predators to plants is crucial to conclusions about co-evolution. For example, insectivorous birds are attracted to herbivore-damaged trees without seeing the herbivores or the defoliated parts, but it is not known whether birds use cues from herbivore-damaged plants with a specific adaptation of plants for this purpose.
Methodology
We examined whether signals from damaged trees attract avian predators in the wild and whether birds could use volatile organic compound (VOC) emissions or net photosynthesis of leaves as cues to detect herbivore-rich trees. We conducted a field experiment with mountain birches (Betula pubescens ssp. czerepanovii), their main herbivore (Epirrita autumnata) and insectivorous birds. Half of the trees had herbivore larvae defoliating trees hidden inside branch bags and half had empty bags as controls. We measured predation rate of birds towards artificial larvae on tree branches, and VOC emissions and net photosynthesis of leaves.
Principal Findings and Significance
The predation rate was higher in the herbivore trees than in the control trees. This confirms that birds use cues from trees to locate insect-rich trees in the wild. The herbivore trees had decreased photosynthesis and elevated emissions of many VOCs, which suggests that birds could use either one, or both, as cues. There was, however, large variation in how the VOC emission correlated with predation rate. Emissions of (E)-DMNT [(E)-4,8-dimethyl-1,3,7-nonatriene], β-ocimene and linalool were positively correlated with predation rate, while those of highly inducible green leaf volatiles were not. These three VOCs are also involved in the attraction of insect parasitoids and predatory mites to herbivore-damaged plants, which suggests that plants may not have specific adaptations to signal only to birds.
doi:10.1371/journal.pone.0002832
PMCID: PMC2475509  PMID: 18665271
18.  The Impact of the Absence of Aliphatic Glucosinolates on Insect Herbivory in Arabidopsis 
PLoS ONE  2008;3(4):e2068.
Aliphatic glucosinolates are compounds which occur in high concentrations in Arabidopsis thaliana and other Brassicaceae species. They are important for the resistance of the plant to pest insects. Previously, the biosynthesis of these compounds was shown to be regulated by transcription factors MYB28 and MYB29. We now show that MYB28 and MYB29 are partially redundant, but in the absence of both, the synthesis of all aliphatic glucosinolates is blocked. Untargeted and targeted biochemical analyses of leaf metabolites showed that differences between single and double knock-out mutants and wild type plants were restricted to glucosinolates. Biosynthesis of long-chain aliphatic glucosinolates was blocked by the myb28 mutation, while short-chain aliphatic glucosinolates were reduced by about 50% in both the myb28 and the myb29 single mutants. Most remarkably, all aliphatic glucosinolates were completely absent in the double mutant. Expression of glucosinolate biosynthetic genes was slightly but significantly reduced by the single myb mutations, while the double mutation resulted in a drastic decrease in expression of these genes. Since the myb28myb29 double mutant is the first Arabidopsis genotype without any aliphatic glucosinolates, we used it to establish the relevance of aliphatic glucosinolate biosynthesis to herbivory by larvae of the lepidopteran insect Mamestra brassicae. Plant damage correlated inversely to the levels of aliphatic glucosinolates observed in those plants: Larval weight gain was 2.6 fold higher on the double myb28myb29 mutant completely lacking aliphatic glucosinolates and 1.8 higher on the single mutants with intermediate levels of aliphatic glucosinolates compared to wild type plants.
doi:10.1371/journal.pone.0002068
PMCID: PMC2323576  PMID: 18446225
19.  Odor Uniformity among Tomato Individuals in Response to Herbivore Depends on Insect Species 
PLoS ONE  2013;8(10):e77199.
Plants produce specific volatile organic compound (VOC) blends in response to herbivory. Herbivore-induced blends may prime the plant for future attack or attract carnivorous insects; these responses have been considered adaptive for plants. If herbivores differentially modify the VOC emission among individuals within a group of plants they feed upon, then plant responses to herbivores will not only produce specific blends but also variation in odor among individuals, i.e. individuals smell the same, then having a uniform odor. We investigated the VOC emission variation or uniformity among tomato individuals (Solanum lycopersicum L. cv. Castlemart) in response to moderate wounding by (1) nymphs of the psyllid Bactericera cockerelli (Sulc.) (TP); (2) Lepidoptera chewing-feeding larvae of Fall Armyworm (Spodoptera frugiperda Smith) (FAW) and (3) of Cabbage Looper (Trichoplusia ni Hübner) (CL), and (4) mechanical damage (MD). We used a ratio-based analysis to compare the fold-change in concentration from constitutive to induced VOC emission. We also used size and shape analysis to compare the emission of damaged and non-damaged individuals. Aside of finding herbivore-specific blends in line with other studies, we found patterns not described previously. We detected constitutive and induced odor variation among individuals attacked by the same herbivore, with the induced odor uniformity depending on the herbivore identity. We also showed that the fold-change of VOCs from constitutive to induced state differed among individuals independently of the uniformity of the blends before herbivore attack. We discuss our findings in the context of the ecological roles of VOCs in plant-plant and plant-carnivore insects’ interactions.
doi:10.1371/journal.pone.0077199
PMCID: PMC3793962  PMID: 24130855
20.  Barbarea vulgaris Glucosinolate Phenotypes Differentially Affect Performance and Preference of Two Different Species of Lepidopteran Herbivores 
Journal of Chemical Ecology  2008;34(2):121-131.
The composition of secondary metabolites and the nutritional value of a plant both determine herbivore preference and performance. The genetically determined glucosinolate pattern of Barbarea vulgaris can be dominated by either glucobarbarin (BAR-type) or by gluconasturtiin (NAS-type). Because of the structural differences, these glucosinolates may have different effects on herbivores. We compared the two Barbarea chemotypes with regards to the preference and performance of two lepidopteran herbivores, using Mamestra brassicae as a generalist and Pieris rapae as a specialist. The generalist and specialist herbivores did not prefer either chemotype for oviposition. However, larvae of the generalist M. brassicae preferred to feed and performed best on NAS-type plants. On NAS-type plants, 100% of the M. brassicae larvae survived while growing exponentially, whereas on BAR-type plants, M. brassicae larvae showed little growth and a mortality of 37.5%. In contrast to M. brassicae, the larval preference and performance of the specialist P. rapae was unaffected by plant chemotype. Total levels of glucosinolates, water soluble sugars, and amino acids of B. vulgaris could not explain the poor preference and performance of M. brassicae on BAR-type plants. Our results suggest that difference in glucosinolate chemical structure is responsible for the differential effects of the B. vulgaris chemotypes on the generalist herbivore.
Electronic supplementary material
The online version of this article (doi:10.1007/s10886-007-9424-9) contains supplementary material, which is available to authorized users.
doi:10.1007/s10886-007-9424-9
PMCID: PMC2239252  PMID: 18213497
Glucosinolates; Oviposition; Performance; Polymorphism; Barbarea vulgaris; Pieris rapae; Mamestra brassicae; Co-evolution
21.  Comparative mapping of Brassica juncea and Arabidopsis thaliana using Intron Polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes 
BMC Genomics  2008;9:113.
Background
Extensive mapping efforts are currently underway for the establishment of comparative genomics between the model plant, Arabidopsis thaliana and various Brassica species. Most of these studies have deployed RFLP markers, the use of which is a laborious and time-consuming process. We therefore tested the efficacy of PCR-based Intron Polymorphism (IP) markers to analyze genome-wide synteny between the oilseed crop, Brassica juncea (AABB genome) and A. thaliana and analyzed the arrangement of 24 (previously described) genomic block segments in the A, B and C Brassica genomes to study the evolutionary events contributing to karyotype variations in the three diploid Brassica genomes.
Results
IP markers were highly efficient and generated easily discernable polymorphisms on agarose gels. Comparative analysis of the segmental organization of the A and B genomes of B. juncea (present study) with the A and B genomes of B. napus and B. nigra respectively (described earlier), revealed a high degree of colinearity suggesting minimal macro-level changes after polyploidization. The ancestral block arrangements that remained unaltered during evolution and the karyotype rearrangements that originated in the Oleracea lineage after its divergence from Rapa lineage were identified. Genomic rearrangements leading to the gain or loss of one chromosome each between the A-B and A-C lineages were deciphered. Complete homoeology in terms of block organization was found between three linkage groups (LG) each for the A-B and A-C genomes. Based on the homoeology shared between the A, B and C genomes, a new nomenclature for the B genome LGs was assigned to establish uniformity in the international Brassica LG nomenclature code.
Conclusion
IP markers were highly effective in generating comparative relationships between Arabidopsis and various Brassica species. Comparative genomics between the three Brassica lineages established the major rearrangements, translocations and fusions pivotal to karyotype diversification between the A, B and C genomes of Brassica species. The inter-relationships established between the Brassica lineages vis-à-vis Arabidopsis would facilitate the identification and isolation of candidate genes contributing to traits of agronomic value in crop Brassicas and the development of unified tools for Brassica genomics.
doi:10.1186/1471-2164-9-113
PMCID: PMC2277410  PMID: 18315867
22.  The Venus flytrap attracts insects by the release of volatile organic compounds 
Journal of Experimental Botany  2014;65(2):755-766.
Does Dionaea muscipula, the Venus flytrap, use a particular mechanism to attract animal prey? This question was raised by Charles Darwin 140 years ago, but it remains unanswered. This study tested the hypothesis that Dionaea releases volatile organic compounds (VOCs) to allure prey insects. For this purpose, olfactory choice bioassays were performed to elucidate if Dionaea attracts Drosophila melanogaster. The VOCs emitted by the plant were further analysed by GC-MS and proton transfer reaction-mass spectrometry (PTR-MS). The bioassays documented that Drosophila was strongly attracted by the carnivorous plant. Over 60 VOCs, including terpenes, benzenoids, and aliphatics, were emitted by Dionaea, predominantly in the light. This work further tested whether attraction of animal prey is affected by the nutritional status of the plant. For this purpose, Dionaea plants were fed with insect biomass to improve plant N status. However, although such feeding altered the VOC emission pattern by reducing terpene release, the attraction of Drosophila was not affected. From these results it is concluded that Dionaea attracts insects on the basis of food smell mimicry because the scent released has strong similarity to the bouquet of fruits and plant flowers. Such a volatile blend is emitted to attract insects searching for food to visit the deadly capture organ of the Venus flytrap.
doi:10.1093/jxb/ert455
PMCID: PMC3904726  PMID: 24420576
Carnivorous plants; Dionaea muscipula; Drosophila melanogaster; nitrogen status; olfactory bioassay; plant–animal interaction; VOC emissions.
23.  Drought and Root Herbivory Interact to Alter the Response of Above-Ground Parasitoids to Aphid Infested Plants and Associated Plant Volatile Signals 
PLoS ONE  2013;8(7):e69013.
Multitrophic interactions are likely to be altered by climate change but there is little empirical evidence relating the responses of herbivores and parasitoids to abiotic factors. Here we investigated the effects of drought on an above/below-ground system comprising a generalist and a specialist aphid species (foliar herbivores), their parasitoids, and a dipteran species (root herbivore).We tested the hypotheses that: (1) high levels of drought stress and below-ground herbivory interact to reduce the performance of parasitoids developing in aphids; (2) drought stress and root herbivory change the profile of volatile organic chemicals (VOCs) emitted by the host plant; (3) parasitoids avoid ovipositing in aphids feeding on plants under drought stress and root herbivory. We examined the effect of drought, with and without root herbivory, on the olfactory response of parasitoids (preference), plant volatile emissions, parasitism success (performance), and the effect of drought on root herbivory. Under drought, percentage parasitism of aphids was reduced by about 40–55% compared with well watered plants. There was a significant interaction between drought and root herbivory on the efficacy of the two parasitoid species, drought stress partially reversing the negative effect of root herbivory on percent parasitism. In the absence of drought, root herbivory significantly reduced the performance (e.g. fecundity) of both parasitoid species developing in foliar herbivores. Plant emissions of VOCs were reduced by drought and root herbivores, and in olfactometer experiments parasitoids preferred the odour from well-watered plants compared with other treatments. The present work demonstrates that drought stress can change the outcome of interactions between herbivores feeding above- and below-ground and their parasitoids, mediated by changes in the chemical signals from plants to parasitoids. This provides a new insight into how the structure of terrestrial communities may be affected by drought.
doi:10.1371/journal.pone.0069013
PMCID: PMC3716814  PMID: 23894394
24.  Subterranean, Herbivore-Induced Plant Volatile Increases Biological Control Activity of Multiple Beneficial Nematode Species in Distinct Habitats 
PLoS ONE  2012;7(6):e38146.
While the role of herbivore-induced volatiles in plant-herbivore-natural enemy interactions is well documented aboveground, new evidence suggests that belowground volatile emissions can protect plants by attracting entomopathogenic nematodes (EPNs). However, due to methodological limitations, no study has previously detected belowground herbivore-induced volatiles in the field or quantified their impact on attraction of diverse EPN species. Here we show how a belowground herbivore-induced volatile can enhance mortality of agriculturally significant root pests. First, in real time, we identified pregeijerene (1,5-dimethylcyclodeca-1,5,7-triene) from citrus roots 9–12 hours after initiation of larval Diaprepes abbreviatus feeding. This compound was also detected in the root zone of mature citrus trees in the field. Application of collected volatiles from weevil-damaged citrus roots attracted native EPNs and increased mortality of beetle larvae (D. abbreviatus) compared to controls in a citrus orchard. In addition, field applications of isolated pregeijerene caused similar results. Quantitative real-time PCR revealed that pregeijerene increased pest mortality by attracting four species of naturally occurring EPNs in the field. Finally, we tested the generality of this root-zone signal by application of pregeijerene in blueberry fields; mortality of larvae (Galleria mellonella and Anomala orientalis) again increased by attracting naturally occurring populations of an EPN. Thus, this specific belowground signal attracts natural enemies of widespread root pests in distinct agricultural systems and may have broad potential in biological control of root pests.
doi:10.1371/journal.pone.0038146
PMCID: PMC3384653  PMID: 22761668
25.  Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host 
PLoS Biology  2012;10(11):e1001435.
Parasitic wasps that develop inside herbivorous hosts alter the volatiles produced by plants in response to the damage, thus giving away the presence of the parasitoid larvae to their hyperparasitoid enemies.
Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.
Author Summary
In nature, plants often release volatiles in response to damage by herbivores (e.g., by caterpillars), and these can indirectly help defend the plants. Indeed, it is well documented that volatiles can recruit the natural enemies of herbivores, such as predators and parasitoid wasps, whose offspring feed on and develop within their caterpillar hosts. However, such induced plant odours can also be detected by other organisms. One important group of organisms, hyperparasitoids, the enemies of the parasitoids that indirectly benefit the plants, have not been included in this trophic web because so little is known about their foraging behaviour. Here, using a combination of laboratory and field experiments, we demonstrate that hyperparasitoid wasps also take advantage of the odours that plants produce in response to the feeding by caterpillars. The larvae of parasitic wasps developing inside the caterpillar alter the composition of the oral secretions of their herbivorous host and thereby affect the cocktail of volatiles the plant produces. The hyperparasitoids on the lookout for their parasitoid prey can preferentially detect infected caterpillars, although not all parasitoid wasps gave away their presence through this host–plant interaction. We conclude that herbivore-induced plant volatiles can affect the interaction among parasitoids and their enemies and thereby may reduce the indirect defence accrued for the plant.
doi:10.1371/journal.pbio.1001435
PMCID: PMC3507920  PMID: 23209379

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