Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes

Abstract

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)-β-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 within three generations. Whereas naive aphids are repelled by EBF, habituated aphids show no avoidance response. Similarly, 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 naive and habituated aphids treated with EBF demonstrate an almost complete desensitization in the transcriptional response to EBF. Furthermore, EBF-habituated aphids show increased progeny production relative to EBF-responsive aphids, with or without EBF treatment. Although both naive and habituated aphids emit EBF upon damage, EBF-responsive aphids have a higher survival rate in the presence of a coccinellid predator (Hippodamia convergens), and thus outperform habituated aphids that do not show an avoidance response. These results provide evidence that aphid perception of conspecific alarm pheromone aids in predator avoidance and thereby bestows fitness benefits in survivorship and fecundity. Therefore, although habituated M. persicae produce more progeny, EBF-emitting transgenic plants may have practical applications in agriculture as a result of increased predation of habituated aphids.aphid | (E)-beta-farnesene | Hippodamia convergens | microarray | sesquiterpene R apid population growth of aphids is facilitated by their parthenogenetic lifestyle, which often results in the establishment of large single-genotype colonies in the field. In agricultural settings, aphid populations can be controlled with natural enemies such as coccinellid beetles and parasitoid wasps. Despite the effectiveness of biological control, behavioral responses to the threat of predation may allow aphids to persist as pests. Aphid avoidance of predators involves the production of an alarm pheromone. Across a remarkable diversity of aphids, the alarm pheromone contains a mixture of compounds with (E)-β-Farnesene (EBF) as the predominant component (1-3). Detection of EBF results in an array of aphid escape behaviors that, depending on the species and developmental stage, can include flying, walking away, and dropping off the plant.EBF is a volatile sesquiterpene released from cornicles on the aphid's abdomen (4). When an aphid is attacked, it can release EBF in a range of concentrations, depending on the stress that is encountered, as well as the specific species, lineage, and developmental stage of the aphid itself (5-10). EBF-treated Acyrthosiphon pisum do no...

(E)-β-Farnesene synthase genes affect aphid (Myzus persicae) infestation in tobacco (Nicotiana tabacum)

“…Compared with the maize terpene synthase 1, which could produce three sesquiterpenes: (E)-β-farnesene (26%), (E)-β-nerolidol (29%), and (E, E)-farnesol (45%) (Schnee et al 2002), the above four isolated EβF synthases produced only one major sesquiterpene, EβF, indicating these genes were good candidates for manipulating crop plants for aphid control. Indeed, overexpression of a peppermint EβF synthase gene in Arabidopsis thaliana not only repelled aphids but also attracted aphid parasitoids (Beale et al 2006) and the EβF-emitting transgenic plants may have practical applications in agriculture as a result of increased predation on habituated aphids (De Vos et al 2010), demonstrating that genetically engineering of plants to consecutively emit EβF for aphid control was feasible. Although the EβF synthase gene had been isolated from sweet wormwood and in vitro analysis indeed proved that it could convert FPP to the only product of acyclic sesquiterpene EβF (Picaud et al 2005), the function of this gene in other plants remains unclear.…”

Metabolic Engineering of Plant‐derived (E)‐β‐farnesene Synthase Genes for a Novel Type of Aphid‐resistant Genetically Modified Crop PlantsF

“…Aphid populations are regulated by natural enemies such as ladybird beetles and parasitoid wasps. Despite the effectiveness of biological control, behavioral responses to the threat of predation may allow aphids to persist as pests (De Vos et al 2010). For many pest species of aphids, avoidance of predators involves the release of an alarm pheromone comprising (E)‐β‐Farnesene (EβF), a volatile sesquiterpene, released from the cornicles (aka siphunculi) on the aphids’ abdomen when attacked by its natural enemies (Bower et al 1972; Pickett and Griffiths 1980; Dixon 1998).…”

“…Unlike the majority of insects, aphids can reproduce clonally and an aphid's embryonic development begins before its mother's birth (Goggin 2007). These traits allow for rapid population growth of aphids in the field due to their parthenogenetic lifestyle, short generation times, and the fact that nymphs of certain aphid species can reach maturity in as little as 5 d (Dixon 1988; Goggin 2007; De Vos et al 2010).…”

Ecophysiological effects of predation risk; an integration across disciplines

“…Yet, we are a long way from fully understanding the impact of risk on prey physiology. For example, de Vos et al (2010) found that aphids exposed to their alarm pheromone up-or down-regulated almost 15 % of the 10,000 genes measured, yet we know little related to the control these genes exert. The field of ecophysiological effects of predation risk is in its infancy and we must move beyond simple stress hormone analysis and delve into other physiological responses and understand their interactive effects to fully appreciate how predation risk shapes system-wide changes in prey.…”