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

Abstract

Summary (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.

Methyl Salicylate and Sesquiterpene Emissions Are Indicative for Aphid Infestation on Scots Pine

“…MeSA has phytohormone properties and is functional in the plant to plant communication [7,60]. Several SQTs are related to plant insect communication [3], and (E)-β-farnesene (EBS), increased by aphid infestation in this study, is a well-known aphid alarm pheromone released by disturbed or attached aphids [61] but also produced by plants in their essential oils [61,62].…”

“…In the second year, there was a significant increase in the emission of E-β-farnesene (EBS). This compound is a well-known aphid alarm pheromone, released by aphids when disturbed by natural enemies or other factors [61]. EBS can be released by both adults and nymphs, and its release induced the escape reaction in the nearby aphids [74].…”

“…It is possible that our BVOC samplings in two successive years caused a different rate of disturbance and the release of an alarm pheromone. Plants capable of emitting EBS efficiently repelled aphids and, in addition, attracted natural enemies such as ladybird beetles [61]. However, when EBS was emitted by a genetically modified EBS-synthetizing plant, a repellent effect was found, but finally, there was not any significant effect on aphid performance [75].…”

“…Therefore, future studies should clarify how much an aphid-induced BVOC profile differs from the BVOC emissions induced by phytopathogens in their host plant. Furthermore, induced emissions of MeSA [80] and farnesenes [61,81] are known to attract predators and parasitoids of aphids and other herbivorous insects and thus affect the function of forest ecosystems.…”

New slow release mixture of (E)‐β‐farnesene with methyl salicylate to enhance aphid biocontrol efficacy in wheat ecosystem

“…12 However, the persistence of this alarm pheromone in the environment is reduced by its ease of oxidation due to the presence of several double bonds in the pheromone molecule. 13 When attacked by herbivores, plants can release specific volatile blends that attract predators and/or parasitoids. [14][15][16] Herbivoreinduced plant volatiles (HIPVs) have a key role in the tritrophic interactions among plants, herbivores and their natural enemies.…”