Plants Attract Parasitic Wasps to Defend Themselves against Insect Pests by Releasing Hexenol

Plant volatiles play an important role in defending plants against insect attacks by attracting their natural enemies. For example, green leaf volatiles (GLVs) and terpenoids emitted from herbivore-damaged plants were found to be important in the host location of parasitic wasps. However, evidence of the functional roles and mechanisms of these semio-chemicals from a system of multiple plants in prey location by the parasitoid is limited. Little is known about the potential evolutionary trends between herbivore-induced host plant volatiles and the host location of their parasitoids.. Specifically, we found that volatile profiles from healthy plants revealed a partly phylogenetic signal, while the inducible compounds of the infested-plants did not result from the fact that the induced plant volatiles dominate most of the volatile blends of the host and non-host plants of the leafminer pests. We further show that the parasitoids are capable of distinguishing the damaged host plant from the non-host plant of the leafminers.Our results suggest that, as the most passive scenario of plant involvement, leafminers and mechanical damages evoke similar semio-chemicals. Using ubiquitous compounds, such as hexenol, for host location by general parasitoids could be an adaptation of the most conservative evolution of tritrophic interaction. Although for this, other compounds may be used to improve the precision of the host location by the parasitoids

Do Leaf Cutting Ants Cut Undetected? Testing the Effect of Ant-Induced Plant Defences on Foraging Decisions in Atta colombica

Leaf-cutting ants (LCAs) are polyphagous, yet highly selective herbivores. The factors that govern their selection of food plants, however, remain poorly understood. We hypothesized that the induction of anti-herbivore defences by attacked food plants, which are toxic to either ants or their mutualistic fungus, should significantly affect the ants' foraging behaviour. To test this “induced defence hypothesis,” we used lima bean (Phaseolus lunatus), a plant that emits many volatile organic compounds (VOCs) upon herbivore attack with known anti-fungal or ant-repellent effects. Our results provide three important insights into the foraging ecology of LCAs. First, leaf-cutting by Atta ants can induce plant defences: Lima bean plants that were repeatedly exposed to foraging workers of Atta colombica over a period of three days emitted significantly more VOCs than undamaged control plants. Second, the level to which a plant has induced its anti-herbivore defences can affect the LCAs' foraging behaviour: In dual choice bioassays, foragers discriminated control plants from plants that have been damaged mechanically or by LCAs 24 h ago. In contrast, strong induction levels of plants after treatment with the plant hormone jasmonic acid or three days of LCA feeding strongly repelled LCA foragers relative to undamaged control plants. Third, the LCA-specific mode of damaging leaves allows them to remove larger quantities of leaf material before being recognized by the plant: While leaf loss of approximately 15% due to a chewing herbivore (coccinelid beetle) was sufficient to significantly increase VOC emission levels after 24 h, the removal of even 20% of a plant's leaf area within 20 min by LCAs did not affect its VOC emission rate after 24 h. Taken together, our results support the “induced defence hypothesis” and provide first empirical evidence that the foraging behaviour of LCAs is affected by the induction of plant defence responses

Eavesdropping on Plant Volatiles by a Specialist Moth: Significance of Ratio and Concentration

We investigated the role that the ratio and concentration of ubiquitous plant volatiles play in providing host specificity for the diet specialist grape berry moth Paralobesia viteana (Clemens) in the process of locating its primary host plant Vitis sp. In the first flight tunnel experiment, using a previously identified attractive blend with seven common but essential components (“optimized blend”), we found that doubling the amount of six compounds singly [(E)- & (Z)-linalool oxides, nonanal, decanal, β-caryophyllene, or germacrene-D], while keeping the concentration of other compounds constant, significantly reduced female attraction (average 76% full and 59% partial upwind flight reduction) to the synthetic blends. However, doubling (E)-4,8-dimethyl 1,3,7-nonatriene had no effect on female response. In the second experiment, we manipulated the volatile profile more naturally by exposing clonal grapevines to Japanese beetle feeding. In the flight tunnel, foliar damage significantly reduced female landing on grape shoots by 72% and full upwind flight by 24%. The reduction was associated with two changes: (1) more than a two-fold increase in total amount of the seven essential volatile compounds, and (2) changes in their relative ratios. Compared to the optimized blend, synthetic blends mimicking the volatile ratio emitted by damaged grapevines resulted in an average of 87% and 32% reduction in full and partial upwind orientation, respectively, and the level of reduction was similar at both high and low doses. Taken together, these results demonstrate that the specificity of a ubiquitous volatile blend is determined, in part, by the ratio of key volatile compounds for this diet specialist. However, P. viteana was also able to accommodate significant variation in the ratio of some compounds as well as the concentration of the overall mixture. Such plasticity may be critical for phytophagous insects to successfully eavesdrop on variable host plant volatile signals

Does egg deposition by herbivorous pine sawflies affect transcription of sesquiterpene synthases in pine?

Scots pine (Pinus sylvestris; Pinaceae, Pinales) is known to defend against egg deposition by herbivorous sawflies by changing its terpenoid volatile blend. The oviposition-induced pine odor attracts egg parasitoids that kill the sawfly eggs. Here, we investigated whether sawfly egg deposition activates genes encoding pine terpene synthases by extracting mRNA from oviposition-induced P. sylvestris. Three new sesquiterpene synthases, PsTPS 1, PsTPS 2, and PsTPS 3, were isolated that were shown on heterologous expression in Escherichia coli to produce (E)-β-caryophyllene and α-humulene (PsTPS 1), 1(10),5-germacradiene-4-ol (PsTPS 2), and longifolene and α-longipinene (PsTPS 3) as their principal products. Quantitative RT-PCR analyses revealed that transcript levels of PsTPS 1 and PsTPS 2 were significantly higher in oviposition-induced twigs that were attractive to the parasitoids than in non-attractive, artificially damaged twigs. Thus, our results demonstrate a specific transcription response to egg deposition, distinct from that caused by artificial wounding. Transcripts of PsTPS 3 did not change in response to egg deposition. The transcript levels of PsTPS 1, PsTPS 2, and PsTPS 3 were also determined in relation to time after egg deposition, since pine odor is attractive to the parasitoid only 72 h after egg deposition. Transcription rates of PsTPS 1 and PsTPS 2 were significantly enhanced only 72 h after egg deposition, thus matching the timing of odor attractiveness, while for PsTPS 3, enhanced transcription was not detected at any time period studied after egg deposition. The ecological significance of the oviposition-induced increase of sesquiterpene synthase transcripts is discussed

Different Transcript Patterns in Response to Specialist and Generalist Herbivores in the Wild Arabidopsis Relative Boechera divaricarpa

BACKGROUND: Plants defend themselves against herbivorous insects, utilizing both constitutive and inducible defenses. Induced defenses are controlled by several phytohormone-mediated signaling pathways. Here, we analyze transcriptional changes in the North American Arabidopsis relative Boechera divaricarpa in response to larval herbivory by the crucifer specialist lepidopteran Plutella xylostella (diamondback moth) and by the generalist lepidopteran Trichoplusia ni (cabbage semilooper), and compare them to wounding and exogenous phytohormone application. METHODOLOGY/PRINCIPAL FINDINGS: We use a custom macroarray constructed from B. divaricarpa herbivory-regulated cDNAs identified by suppression subtractive hybridization and from known stress-responsive A. thaliana genes for transcript profiling after insect herbivory, wounding and in response to jasmonate, salicylate and ethylene. In addition, we introduce path analysis as a novel approach to analyze transcript profiles. Path analyses reveal that transcriptional responses to the crucifer specialist P. xylostella are primarily determined by direct effects of the ethylene and salicylate pathways, whereas responses to the generalist T. ni are influenced by the ethylene and jasmonate pathways. Wound-induced transcriptional changes are influenced by all three pathways, with jasmonate having the strongest effect. CONCLUSIONS/SIGNIFICANCE: Our results show that insect herbivory is distinct from simple mechanical plant damage, and that different lepidopteran herbivores elicit different transcriptional responses

Chrysolina herbacea Modulates Terpenoid Biosynthesis of Mentha aquatica L.

Interactions between herbivorous insects and plants storing terpenoids are poorly understood. This study describes the ability of Chrysolina herbacea to use volatiles emitted by undamaged Mentha aquatica plants as attractants and the plant's response to herbivory, which involves the production of deterrent molecules. Emitted plant volatiles were analyzed by GC-MS. The insect's response to plant volatiles was tested by Y-tube olfactometer bioassays. Total RNA was extracted from control plants, mechanically damaged leaves, and leaves damaged by herbivores. The terpenoid quantitative gene expressions (qPCR) were then assayed. Upon herbivory, M. aquatica synthesizes and emits (+)-menthofuran, which acts as a deterrent to C. herbacea. Herbivory was found to up-regulate the expression of genes involved in terpenoid biosynthesis. The increased emission of (+)-menthofuran was correlated with the upregulation of (+)-menthofuran synthase

Ranking and characterization of established BMI and lipid associated loci as candidates for gene-environment interactions

Phenotypic variance heterogeneity across genotypes at a single nucleotide polymorphism (SNP) may reflect underlying gene-environment (G×E) or gene-gene interactions. We modeled variance heterogeneity for blood lipids and BMI in up to 44,211 participants and investigated relationships between variance effects (P$_v$), G×E interaction effects (with smoking and physical activity), and marginal genetic effects (P$_m$). Correlations between P$_v$ and P$_m$ were stronger for SNPs with established marginal effects (Spearman's ρ = 0.401 for triglycerides, and ρ = 0.236 for BMI) compared to all SNPs. When P$_v$ and P$_m$ were compared for all pruned SNPs, only BMI was statistically significant (Spearman's ρ = 0.010). Overall, SNPs with established marginal effects were overrepresented in the nominally significant part of the P$_v$ distribution (P$_{binomial}$ <0.05). SNPs from the top 1% of the P$_m$ distribution for BMI had more significant Pv values (P$_{Mann-Whitney}$ = 1.46×10$^{-5}$), and the odds ratio of SNPs with nominally significant (<0.05) P$_m$ and P$_v$ was 1.33 (95% CI: 1.12, 1.57) for BMI. Moreover, BMI SNPs with nominally significant G×E interaction P-values (P$_{int}$<0.05) were enriched with nominally significant P$_v$ values (P$_{binomial}$ = 8.63×10$^{-9}$ and 8.52×10$^{-7}$ for SNP × smoking and SNP × physical activity, respectively). We conclude that some loci with strong marginal effects may be good candidates for G×E, and variance-based prioritization can be used to identify them.This research was undertaken as part of a research program supported by the European Commission (CoG-2015_681742_NASCENT), Swedish Research Council (Distinguished Young Researchers Award in Medicine), Swedish HeartLung Foundation, and the Novo Nordisk Foundation, all grants to PWF. DS is supported by the Swedish Research Council International Postdoc Fellowship (4.1-2016-00416). TVV is supported by the Novo Nordisk Foundation Postdoctoral Fellowship within Endocrinology/ Metabolism at International Elite Research Environments via NNF16OC0020698. TWW was supported by the grants "Bundesministerium fur Bildung und Forschung": BMBF-01ER1206, BMBF- 01ER1507. APM is a Wellcome Trust Senior Fellow in Basic Biomedical Science (grant WT098017). LAC acknowledges funding for the Framingham Heart Study: This research was conducted in part using data and resources from the Framingham Heart Study of the National Heart Lung and Blood Institute of the National Institutes of Health and Boston University School of Medicine. The analyses reflect intellectual input and resource development from the Framingham Heart Study investigators participating in the SNP Health Association Resource (SHARe) project. This work was partially supported by the National Heart, Lung and Blood Institute’s Framingham Heart Study (Contract No. N01-HC-25195 and Contract No. HHSN268201500001I) and its contract with Affymetrix, Inc for genotyping services (Contract No. N02-HL-6-4278). A portion of this research utilized the Linux Cluster for Genetic Analysis (LinGA-II) funded by the Robert Dawson Evans Endowment of the Department of Medicine at Boston University School of Medicine and Boston Medical Center. This research was partially supported by grant R01-DK089256 from the National Institute of Diabetes and Digestive and Kidney Diseases (MPIs: I.B. Borecki, LAC, K. North). TOK was supported by the Danish Council for Independent Research (DFF—1333-00124) and Sapere Aude program grant (DFF—1331-00730B). RM would like to acknowledge the High Performance Computing Center of University of Tartu. EGCUT was supported by EU H2020 grants 692145, 676550, 654248, 692065, Estonian Research Council Grant IUT20-60, and PerMed I NIASC, EIT—Health and European Union through the European Regional Development Fund (Project No, 2014-2020.4.01.15-0012 GENTRANSMED)