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Plasmid engineering of aphid alarm pheromone in tobacco seedlings affects the preference of aphids.

ABSTRACT: Plants producing sufficient amount of aphid alarm pheromone by expressing (E)-β-Farnesene (EβF) synthase gene may contribute to plant protection by reducing aphid populations. However, terpene biosynthesis varies among plant species and developmental stages. In the present study, volatile headspace analysis of tobacco seedlings with MaβFS1 (an EβF synthase from the Asian peppermint Mentha asiatica) failed to generate EβF. We further targeted MaβFS1 to the tobacco plastid, using a chloroplast targeting sequence, either with or without the AtFPS1 gene for the biosynthesis of the precursor farnesyl diphosphate. When both MaβFS1 and AtFPS1 genes were targeted to the chloroplast, low levels of EβF were detected in stably transformed tobacco seedlings; resulting in specific repellence of the green peach aphid, Myzus persicae. These data indicate that redirecting the EβF biosynthetic pathway from its natural cytosolic location to the chloroplast is a valid strategy. This redirecting strategy may be very useful for other crop plants that do not naturally produce EβF or other repellent volatiles.

SUBMITTER: Yu X

PROVIDER: S-EPMC6512937 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Constitutive emission of the aphid alarm pheromone, (E)-β-farnesene, from plants does not serve as a direct defense against aphids.

Project description:BackgroundThe sesquiterpene, (E)-β-farnesene (EBF), is the principal component of the alarm pheromone of many aphid species. Released when aphids are attacked by enemies, EBF leads aphids to undertake predator avoidance behaviors and to produce more winged offspring that can leave the plant. Many plants also release EBF as a volatile, and so it has been proposed that this compound could act to defend plants against aphid infestation by 1) deterring aphids from settling, 2) reducing aphid performance due to frequent interruption of feeding and 3) inducing the production of more winged offspring. Here we tested the costs and benefits of EBF as a defense against the green peach aphid, Myzus persicae, using transgenic Arabidopsis thaliana lines engineered to continuously emit EBF.ResultsNo metabolic costs of EBF synthesis could be detected in these plants as they showed no differences in growth or seed production from wild-type controls under two fertilizer regimes. Likewise, no evidence was found for the ability of EBF to directly defend the plant against aphids. EBF emission did not significantly repel winged or wingless morphs from settling on plants. Nor did EBF reduce aphid performance, measured as reproduction, or lead to an increase in the proportion of winged offspring.ConclusionsThe lack of any defensive effect of EBF in this study might be due to the fact that natural enemy attack on individual aphids leads to a pulsed emission, but the transgenic lines tested continuously produce EBF to which aphids may become habituated. Thus our results provide no support for the hypothesis that plant emission of the aphid alarm pheromone EBF is a direct defense against aphids. However, there is scattered evidence elsewhere in the literature suggesting that EBF emission might serve as an indirect defense by attracting aphid predators.

| S-EPMC3002888 | biostudies-literature

Do aphid colonies amplify their emission of alarm pheromone?

Project description:When aphids are attacked by natural enemies, they emit alarm pheromone to alert conspecifics. For most aphids tested, (E)-beta-farnesene (EBF) is the main, or only, constituent of the alarm pheromone. In response to alarm pheromone, alerted aphids drop off the plant, walk away, or attempt to elude predators. However, under natural conditions, EBF concentration might be low due to the low amounts emitted, to rapid air movement, or to oxidative degradation. To ensure that conspecifics are warned, aphids might conceivably amplify the alarm signal by emitting EBF in response to EBF emitted by other aphids. To examine whether such amplification occurs, we synthesized deuterated EBF (DEBF), which allowed us to differentiate between applied and aphid-derived chemical. Colonies of Acyrthosiphon pisum were treated with DEBF, and headspace volatiles were collected and analyzed for evidence of aphid-derived EBF. No aphid-derived EBF was detected, suggesting that amplification of the alarm signal does not occur. We discuss the disadvantages of alarm signal reinforcement.

| S-EPMC2518949 | biostudies-other

Defense of pyrethrum flowers: repelling herbivores and recruiting carnivores by producing aphid alarm pheromone.

Project description:(E)-β-Farnesene (EβF) is the predominant constituent of the alarm pheromone of most aphid pest species. Moreover, natural enemies of aphids use EβF to locate their aphid prey. Some plant species emit EβF, potentially as a defense against aphids, but field demonstrations are lacking. Here, we present field and laboratory studies of flower defense showing that ladybird beetles are predominantly attracted to young stage-2 pyrethrum flowers that emitted the highest and purest levels of EβF. By contrast, aphids were repelled by EβF emitted by S2 pyrethrum flowers. Although peach aphids can adapt to pyrethrum plants in the laboratory, aphids were not recorded in the field. Pyrethrum's (E)-β-farnesene synthase (EbFS) gene is strongly expressed in inner cortex tissue surrounding the vascular system of the aphid-preferred flower receptacle and peduncle, leading to elongated cells filled with EβF. Aphids that probe these tissues during settlement encounter and ingest plant EβF, as evidenced by the release in honeydew. These EβF concentrations in honeydew induce aphid alarm responses, suggesting an extra layer of this defense. Collectively, our data elucidate a defensive mimicry in pyrethrum flowers: the developmentally regulated and tissue-specific EβF accumulation and emission both prevents attack by aphids and recruits aphid predators as bodyguards.

| S-EPMC6772172 | biostudies-literature

Functional characterization of alkaline phosphatases involved alarm pheromone in the vetch aphid Megoura viciae

Project description: Not available

| S-EPMC10590853 | biostudies-literature

Host plants and obligate endosymbionts are not the sources for biosynthesis of the aphid alarm pheromone.

Project description:(E)-β-farnesene (EβF) is the major component of the alarm pheromone of many aphid species, but where EβF is synthesized in aphids is only partly understood. There are at least three most possible sources for the alarm pheromone: host plants, aphid obligate endosymbiont and aphids themselves. Here we eliminated the possibility of host plants and the obligate endosymbiont Buchnera aphidicola as the sources for EβF released by aphids. We excluded the possible effects of host plants on EβF biosynthesis by rearing aphids on non-plant diets. Both the diet-reared aphids, including the cotton aphid Aphis gossypii and the green peach aphid Myzus persicae, could still release EβF based on solid-phase micro-extraction combined with gas chromatography-mass spectrometer analysis. Meanwhile, we treated host aphids with antibiotics to fully eliminate Buchnera bacteria. Though the treatment seriously affected the development and fecundity of host aphids, the treated aphids could still release EβF, and there was no significant difference in the EβF concentration as per the aphid weight under different rearing conditions. Taken together, our experimental results suggest that host plants and obligate endosymbionts are not the sources for EβF released by aphids, indicating that it is most probably the aphid itself synthesizes the alarm pheromone.

| S-EPMC5519760 | biostudies-literature

Real-time analysis of alarm pheromone emission by the pea aphid (acyrthosiphon pisum) under predation.

Project description:Upon attack by predators or parasitoids, aphids emit volatile chemical alarm signals that warn other aphids of a potential risk of predation. Release rate of the major constituent of the alarm pheromone in pea aphids (Acyrthosiphon pisum), (E)-b-farnesene (EBF), was measured for all nymphal and the adult stage as aphids were attacked individually by lacewing (Chrysoperla carnae) larvae. Volatilization of EBF from aphids under attack was quantified continuously for 60 min at 2-min intervals with a rapid gas chromatography technique (zNose) to monitor headspace emissions. After an initial burst, EBF volatilization declined exponentially, and detectable amounts were still present after 30 min in most cases. Total emission of EBF averaged 16.33 +/- 1.54 ng and ranged from 1.18 to 48.85 ng. Emission was higher in nymphs as compared to adults. No differences between pea aphid life stages were detected for their speed of alarm signal emission in response to lacewing larvae attack. This is the first time that alarm pheromone emission from single aphids has been reported.

| S-EPMC2758399 | biostudies-other

Two odorant-binding proteins mediate the behavioural response of aphids to the alarm pheromone (E)-ß-farnesene and structural analogues.

Project description:BackgroundAphids are agricultural pests of great economical interest. Alternatives to insecticides, using semiochemicals, are of difficult applications. In fact, sex pheromones are of little use as aphids reproduce partenogenetically most of the time. Besides, the alarm pheromone, (E)-ß-farnesene for a great number of species, is difficult to synthesize and unstable in the environment. The search for novel semiochemicals to be used in population control can be efficiently approached through the study of the olfactory system at the biochemical level. Recently odorant-binding proteins (OBPs) have been shown to play a central role in olfactory recognition, thus becoming the target of choice for designing new semiochemicals.Methodology/principal findingsTo address the question of how the alarm message is recognised at the level of OBPs, we have tested 29 compounds, including (E)-ß-farnesene, in binding assays with 6 recombinant proteins and in behaviour experiments. We have found that good repellents bind OBP3 and/or OBP7, while non repellents present different spectra of binding. These results have been verified with two species of aphids, Acyrthosiphon pisum and Myzus persicae, both using (E)-ß-farnesene as the alarm pheromone.ConclusionsOur results represent further support to the idea (so far convincingly demonstrated only in Drosophila) that OBPs are involved in decoding the chemical information of odorants and pheromones, and for the first time provide such evidence in other insect species and using wild-type insects. Moreover, the data offer guidelines and protocols for the discovery of potential alarm pheromones, using ligand-binding assays as a preliminary screening before subjecting selected compounds to behaviour tests.

| S-EPMC3299684 | biostudies-literature

The main component of the aphid alarm pheromone (<i>E</i>)-β-farnesene affects the growth and development of <i>Spodoptera exigua</i> by mediating juvenile hormone-related genes.

Project description:The (E)-β-farnesene (EβF) is one of the most important secondary metabolites in some plants and provides indirect defense against aphids. However, the direct effect of EβF against pests is still unclear. In this study, various concentrations of EβF (0.16, 0.8, and 4 g/kg) were provided in an artificial diet to determine the direct effects of EβF on Spodoptera exigua. The results showed that an artificial diet containing 4 g/kg of EβF reduced the final survival of the S. exigua larvae and per female fecundity of adults significantly when compared with CK and SC controls (p < 0.05), then ultimately it also significantly affected the intrinsic rate of increase (p < 0.05). Furthermore, the results of the EβF bioassay in an artificial diet also indicated that the proliferation of the S. exigua population was inhibited by the ingestion of EβF in a dose-dependent manner. Combined differential RNA-seq data and RT-qPCR analysis, it was found that four key genes involved in juvenile hormone degradation significantly upregulated in S. exigua larvae treated by EβF at a dose of 0.8 and 4 g/kg when compared with two controls (p < 0.05). This indicated that EβF could disturb the normal function of juvenile hormones and reduce the survival rate of S. exigua larvae. Additionally, two key genes that regulate per fecundity of S. exigua females, including SeVg and SeVgR, were significantly downregulated in adult females (p < 0.05) when they were treated with 0.8 and 4 g/kg of EβF at the larval stage, relative to the expression of these genes after treatment with controls. These findings suggested that EβF first disturbed the normal function of juvenile hormone by upregulating key degradation genes, and then inhibited the expression of SeVg/SeVgR genes and proteins, thus reducing the population size of S. exigua by increasing larval mortality and inhibiting per female fecundity.

| S-EPMC9445801 | biostudies-literature

Alarm Pheromone Responses Depend on Genotype, but Not on the Presence of Facultative Endosymbionts in the Pea Aphid Acyrthosiphon pisum.

Project description:Aphids use an alarm pheromone, E-β farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, Acyrthosiphon pisum, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not Hamiltonella defensa, a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with H. defensa did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont H. defensa does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.

| S-EPMC7826508 | biostudies-literature

Alarm pheromone habituation in Myzus persicae: Fitness consequences and the transcriptome of fear

Project description:In most aphid species, facultative parthenogenetic reproduction allows rapid growth and formation of large single-genotype colonies. Upon predator attack, individual aphids emit an alarm pheromone to warn the colony of this danger. (E)-beta-farnesene (EBF) is the predominant constituent of the alarm pheromone in Myzus persicae (green peach aphid) and many other aphid species. Continuous exposure to alarm pheromone in aphid colonies raised on transgenic Arabidopsis thaliana plants that produce EBF leads to habituation of the aphid population. Whereas naïve aphids are repelled by EBF, habituated aphids show no avoidance response. Individual aphids from the habituated colony can revert back to being EBF-sensitive in three generations, indicating that this behavioral change is not caused by a genetic mutation. Instead, DNA microarray experiments comparing gene expression in naïve and habituated aphids treated with EBF demonstrate an almost complete desensitization in the transcriptional response to EBF. Furthermore, EBF-responsive aphids, but not habituated aphids show significantly lower reproduction in the presence of EBF. Although both naïve and habituated aphids emit EBF upon damage, EBF-responsive aphids display a higher survival rate in the presence of coccinellid predators and thus outperform habituated aphids that do not show an avoidance response. These results provide direct evidence that aphid perception of conspecific alarm pheromone aids in predator avoidance and thereby bestows fitness benefits in survivorship and fecundity. Although habituated M. persicae have equal fecundity on control and EBF-producing plants, such transgenics may have practical applications in agriculture because of increased predation of habituated aphids. Log fold-changes (LogFC) were computed and contigs with P-values ≤ 0.05 were considered to be differentially expressed (see Supplementary file at foot of this record).

2010-03-01 | GSE20445 | GEO

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