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

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)-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).

ORGANISM(S): Myzus persicae

PROVIDER: GSE20445 | GEO | 2010/03/01

SECONDARY ACCESSION(S): PRJNA125099

REPOSITORIES: GEO

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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). Agilent 8x15K array previously reported by Ramsey et al., 2007 - BMC Genomics 8: 243. Two-condition experiment using Alexa Fluor 555 and 647 dyes. Biological replicates: 4 control replicates, 4 treated replicates.

Project description:The aim of this study is to identify Arabidopsis genes whose expression is altered by aphid feeding. An understanding of the plant aphid interaction at the level of the plant transcriptome will 1) consolidate current areas of investigation focused on the phloem composition (the aphid diet), 2) open up areas of plant aphid interactions for ourselves and other workers, 3) Contribute to understanding the use of new molecular technologies in an environmental context and 4) contribute to existing and development of novel control strategies.Our Arabidopsis/Myzus persicae system provides a valuable model for the study because of: a) the advantages of using Arabidopsis, b) The ability to use clonal insects, c) phloem feeding aphids facilitate focus on a specific cell type, d) aphid stylectomy allows collection of pure phloem sap to monitor ‘phloem phenotype’ of the plant and the insect diet, e) we have techniques to monitor the reproductive performance and feeding behaviour aphids.Our strategy has been to test the function of selected genes, particularly those regulating phloem composition (the feeding site of the aphid) based on current phloem models of phloem function. Gene choice is limited the simplicity of current models of phloem aphid interaction.We propose a simple two treatment (aphid infested vs control plants) experiment that will identify novel target genes for future analysis. Arabidopsis plants (variety Columbia) will be grown in 16/8 light/dark in temperature controlled growth rooms. At growth stage 3.90, when rosette growth is complete, 10 clonal adult Myzus persicae will be caged in clip cages on the two largest leaves on each plant. Control plants will be treated identically except that the cages will be empty. Leaves will be harvested 8 h after infestation. This time point is selected as we know that 90% of aphids are plugged into the sieve element within 2h and that a 6h lag phase has period has previously been used when examining gene expression affected by wounding. In subsequent experiments we will examine time courses of expression of relevant genes using other approaches. Pooling two leaves from each of ten plants will generate the RNA sample, ensuring that expression signals are representative of the population of plants. Keywords: pathogenicity_design

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

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