Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies
Graphical abstract
Wild tomato (Solanum habrochaites) emits mainly 7-epizingiberene and R-curcumene. Adult whiteflies are repelled by these two sesquiterpenes, but not by the stereoisomers zingiberene and S-curcumene.
Introduction
By deciding which host plant to select for laying their eggs, flying adults of polyphagous insects determine a great deal of the developmental success of their relatively less mobile offspring. Here, we study these decisions for the case of the sweetpotato whitefly, Bemisia tabaci Gennadius, a polyphagous insect, first described as a plant pest in 1889 and continuing to be a threat to various horticultural and agricultural crops worldwide, mostly due to vectoring various devastating plant viruses (Jones, 2003). Prior to landing on a plant these insects may use a combination of vision and olfaction, to scan for cues that inform them on plant quality (Visser, 1988). Post-landing, they may also use gustatory or other sensory and metabolic cues to perceive host quality and to decide whether or not to oviposit. For B. tabaci post-landing behaviour consists of labial dabbing, probing and, finally, feeding, whereas pre-landing responses to colour, especially yellow-green (wavelength 500–600 nm), have been described by van Lenteren and Noldus (1990). Recently, we found that, in addition to visual cues, whiteflies use semiochemicals for selecting a host plant from a distance. They display avoidance behaviour to a selection of tomato terpenes, in particular the sesquiterpenes zingiberene and curcumene (Bleeker et al., 2009). Tomato zingiberene is known to be toxic and to have a negative effect on whitefly feeding and oviposition (Freitas et al., 2002, Muigai et al., 2002); ginger oil, which contains mostly zingiberene, has a similar impact (Zhang et al., 2004). However, the repellency in response to these compounds has not been elucidated so far.
In this study we isolated and purified zingiberene and curcumene focussing on the effect of these sesquiterpenes on the initial decision making process of whiteflies and addressed the following questions: (a) whether B. tabaci antennae can perceive these volatiles; (b) how specific perception is for different stereoisomers purified from tomato and ginger and; (c) how different stereoisomers influence whiteflies in deciding to land on a plant.
Section snippets
Results
When given a choice between cultivated tomato (Solanum lycopersicum cv. Moneymaker) and wild tomato Solanum habrochaites PI127826, more than 90% of the whiteflies choose cultivated tomato (Fig. 1a; P < 0.000). However, in a no-choice assay, approximately 60% of the whiteflies will still land on the wild tomato (Fig. 1b), which is not significantly different from the numbers found on the cultivated tomato (P = 0.267). On the wild tomato, all whiteflies subsequently die (Fig. 1c), whereas >75% will
Discussion
When given no other option, whiteflies will find and settle on a host displaying toxic properties, even if chances for survival are poor, indicating that visual cues dominate the response under the conditions of this assay (Fig. 1b and c). Since visual and odour cues can interact when processed in the insect brain (Balkenius et al., 2009), it is important to perform olfactory preference tests against the same visual background. Our host-choice assays show that, when given the choice between
Concluding remarks
Besides dominant visual cues, B. tabaci makes use of volatile semiochemicals prior to choosing a host. Only tomato-derived 7-epizingiberene and R-curcumene prompted a modified behaviour in whiteflies under free-choice conditions, although their respective stereoisomers, zingiberene and S-curcumene, from ginger elicited a similar response in antennae, as determined by electroantennography. Thus 7-epizingiberene and R-curcumene most likely signal the presence of a hostile environment on the site
General experimental procedures
A detailed description of the isolation of zingiberene, 7-epizingiberene, (S)-curcumene and (R)-curcumene can be found in Supplementary information. In short; 7-epizingiberene 2 was isolated from leaf and stem material of S. habrochaites (PI127826) by hexane extraction of tissue ground in liquid nitrogen. The crude tomato plant extract was filtered with pentane over a plug of silica gel from which almost pure (>90%) 7-epizingiberene was obtained. This was dissolved in 10 ml tetrahydrofuran (THF)
Acknowledgements
This work was supported by Senter Novem, Enza Zaden, Vilmorin & Cie, Takii & Co., and De Ruiter Seeds.
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