Abstract

SummaryAphids are pests of chrysanthemum that employ plant volatiles to select host plants and ingest cell contents to probe host quality before engaging in prolonged feeding and reproduction. Changes in volatile and nonvolatile metabolite profiles can disrupt aphid–plant interactions and provide new methods of pest control. Chrysanthemol synthase (CHS) from Tanacetum cinerariifolium represents the first committed step in the biosynthesis of pyrethrin ester insecticides, but no biological role for the chrysanthemol product alone has yet been documented. In this study, the TcCHS gene was over‐expressed in Chrysanthemum morifolium and resulted in both the emission of volatile chrysanthemol (ca. 47 pmol/h/gFW) and accumulation of a chrysanthemol glycoside derivative, identified by NMR as chrysanthemyl‐6‐O‐malonyl‐β‐D‐glucopyranoside (ca. 1.1 mM), with no detrimental phenotypic effects. Dual‐choice assays separately assaying these compounds in pure form and as part of the headspace and extract demonstrated independent bioactivity of both components against the cotton aphid (Aphis gossypii). Performance assays showed that the TcCHS plants significantly reduced aphid reproduction, consistent with disturbance of aphid probing activities on these plants as revealed by electropenetrogram (EPG) studies. In open‐field trials, aphid population development was very strongly impaired demonstrating the robustness and high impact of the trait. The results suggest that expression of the TcCHS gene induces a dual defence system, with both repellence by chrysanthemol odour and deterrence by its nonvolatile glycoside, introducing a promising new option for engineering aphid control into plants.

Highlights

  • Aphids (Aphididae) are abundant and destructive agricultural pests causing serious economic damage to cultivated plants in the form of stunting, sooty mould and transmitted phytopathogenic viruses (Goggin, 2007)

  • Chrysanthemum (Chrysanthemum morifolium) is an important ornamental plant which is susceptible to aphid infestation

  • The aim of this study was to test whether overexpression of the TcCHS gene in chrysanthemum could produce chrysanthemol or any derivatives and improve defence against aphids

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Summary

Introduction

Aphids (Aphididae) are abundant and destructive agricultural pests causing serious economic damage to cultivated plants in the form of stunting, sooty mould and transmitted phytopathogenic viruses (Goggin, 2007). Chrysanthemum (Chrysanthemum morifolium) is an important ornamental plant which is susceptible to aphid infestation. Toxic or antinutritional plant proteins were an early lead to engineering aphid resistance into plants. Proteinase inhibitors (Rahbe et al, 2003; Stoger et al, 1999; Valizadeh et al, 2013) and plant lectins (Michiels et al, 2010) yielded significant but mild effects on aphid survival, reproduction, growth or mortality. Plant-derived secondary metabolites, such as terpenoids (Aharoni et al, 2003), alkaloids (Kim et al, 2011), hydroxamic acids (Hansen, 2006), green leaf volatiles (GLVs) (Vancanneyt et al, 2001) and methyl salicylate (Zhu and Park, 2005), were shown to be effective to various extents against aphids. The volatile terpenoids are the largest and most diverse compound family, and relevant in aphid-plant interactions, as aphids rely heavily on olfaction for host plant localization or avoiding unsuitable plants (Pickett et al, 2013)

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