Abstract
The aphid Myzus persicae displays high mortality on tobacco plants bearing a transgene which results in the accumulation of the ketosteroids cholestan-3-one and cholest-4-en-3-one in the phloem sap. To test whether the ketosteroids are the basis of the plant resistance to the aphids, M. persicae were reared on chemically-defined diets with different steroid contents at 0.1–10 µg ml−1. Relative to sterol-free diet and dietary supplements of the two ketosteroids and two phytosterols, dietary cholesterol significantly extended aphid lifespan and increased fecundity at one or more dietary concentrations tested. Median lifespan was 50% lower on the diet supplemented with cholest-4-en-3-one than on the cholesterol-supplemented diet. Aphid feeding rate did not vary significantly across the treatments, indicative of no anti-feedant effect of any sterol/steroid. Aphids reared on diets containing equal amounts of cholesterol and cholest-4-en-3-one showed fecundity equivalent to aphids on diets containing only cholesterol. Aphids were reared on diets that reproduced the relative steroid abundance in the phloem sap of the control and modified tobacco plants, and their performance on the two diet formulations was broadly equivalent. We conclude that, at the concentrations tested, plant ketosteroids support weaker aphid performance than cholesterol, but do not cause acute toxicity to the aphids. In plants, the ketosteroids may act synergistically with plant factors absent from artificial diets but are unlikely to be solely responsible for resistance of modified tobacco plants.
Highlights
Sterols are an essential constituent of eukaryotic membranes and contribute to other functions, notably hormones of animals and plants [1,2]
To investigate the effect of the individual sterols and steroids on the performance of M. persicae, 2-day-old aphids born on sterol-free diets were transferred to chemically-defined diets supplemented with single sterols/steroids previously identified in the phloem sap of control or modified tobacco [9]
Transgenes can affect a range of plant traits, including some that are not necessarily easy to predict from their specific function
Summary
Sterols are an essential constituent of eukaryotic membranes and contribute to other functions, notably hormones of animals (e.g. mammalian estrogens, insect ecdysteroids) and plants (e.g. brassinosteroids) [1,2]. The composition of phytosterols varies among plant species, a trait that is of special significance for phytophagous insects for two linked reasons. Insects, unlike most other animals, cannot synthesize sterols and are, dependent on a dietary supply of these nutrients; and, second, phytophagous insects vary in their capacity to utilize different phytosterols [4,5]. A mismatch between the plant sterol content and the sterol utilization traits of a particular insect is predicted to confer plant resistance to the insect of interest [1] thereby limiting the plant range of the insect [4]. Plants transformed with the bacterial gene choM (sterol oxidase) have a dramatically altered sterol profile, dominated by oxidized ketosteroids instead of phytosterols [6,7]. The central importance of the ketosteroids in the resistance of modified plants against lepidopteran caterpillars is indicated by the very poor performance of the lepidopteran Heliothis zea on diet supplemented with cholest-3-one, a dominant ketosteroid in the modified plants, relative to diets with no sterol or sterols found in control plants [9]
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