Ecdysteroid biosynthesis and embryonic development are disturbed in insects ( Locusta migratoria ) reared on plant diet ( Triticum sativum ) with a selectively modified sterol profile

Abstract

Wheat seedlings germinating in the presence of the systemic fungicide fenpropimorph accumulate 9.8,19-cyclopropylsterols (95% of total sterols) in place of A5-sterols, which are normally produced in these plants. Adult females of the phytophagous insect Locusta migratoria show a dramatic decrease in their cholesterol content when reared on fenpropimorph-treated wheat. These females lay eggs with the ecdysteroid concentration reduced by up to 80% as compared to controls. Injection of fenpropimorph to the insects or feeding them on wheat coated with the fungicide (normal sterol composition) does not affect their sterol or ecdysteroid profiles; addition of cholesterol to fenpropimorph-treated wheat prior to feeding restores normal ecdysteroid titers in the insects. The severe reduction of the ecdysteroid content in eggs laid by females reared on fenpropimorph-treated wheat is associated with a series of developmental arrests and/or abnormalities. The results show that the dietary 9,3,19-cyclopropylsterols cannot be used by Locusta in place of A5-sterols for ecdysteroid biosynthesis. They suggest that the selective inhibition of specific enzymes in the sterol biosynthetic pathway of the plants can be used as a strategy to control insect development.Insects are unable to synthesize de novo the steroid nucleus and depend on an exogenous source for their steroid economy. In particular, the biosynthesis of the molting hormone family, the ecdysteroids, which are polyhydroxylated steroids, is dependent on the uptake of sterols from the diet. The phytophagous grasshopper Locusta migratoria uses phytosterols such as sitosterol, stigmasterol, and campesterol, which it dealkylates to cholesterol, the most common precursor for ecdysone biosynthesis ( Fig. 1) (1, 2). We have recently shown that long-term treatment of maize seedlings with low concentrations of the systemic fungicides tridemorph or fenpropimorph leads to an almost complete replacement in these plants of the A5-sterols by the 9P,19-cyclopropylsterols [>95% of total sterols (3-5)]. This replacement could be traced back to a selective inhibition by the fungicide of two enzymes in the biosynthetic pathway of plant sterols: cycloeucalenolobtusifoliol isomerase and A8 A7-sterol isomerase (6).We have investigated the effect of abnormal sterol diet on the sterol economy of Locusta and have focused on possible interferences with ecdysteroid titers. This study was prompted by previous reports showing that lanosterol could not meet the sterol requirements of Dermestes vulpinus (7) and that some species of Drosophila were unable to complete development when raised on yeast mutants lacking A8 A7-sterol isomerase (8). MATERIALS AND METHODSChemicals. Fenpropimorph {4-[3-(4-t-butylphenyl)-2-methyl]propyl-2,6-dimethylmorpholine} was a gift of H. Pommer (BASF, Limburgerhof, F.R.G.). The cyclopropyl sterols used as standards were extracted from maize seedlings treated with tridemorph (3).Plant Material and Insects. Wheat (Triticum sativum) caryopses were purchased locally. ...

Effects of modifying the phytosterol profile of canola, Brassica napus L., on growth, development, and survival of the bertha armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae), the flea beetle, Phyllotreta cruciferae (Goeze) (Coleoptera: Chrysomelidae) and the aphids, Lipaphis erysimi (Kaltenbach) and Myzus persicae (Sulzer) (Homoptera: Aphididae)

“…Mortality at pupation, an event that is critically dependent on the moulting hormone, may be due in part to a deficiency in ecdysteroids. Locusts are unable to use 9β-19-cyclopropyl sterols in place of ∆ 5 -phytosterols for ecdysteroid biosynthesis (Costet et al 1987;Corio-Costet et al 1989) and a similar situation may exist for the bertha armyworm.…”

“…Wheat seedlings, Triticum aestivum L., treated with fenpropimorph, show a drastically reduced level of their usual ∆ 5 -phytosterols and replacement by 9β, 19-cyclopropyl and ∆ 8 -sterols. Larvae of locusts, Locusta migratoria, fed fenpropimorph-treated wheat displayed delayed development, morphogenic alterations and adults laid eggs in which embryonic development was disturbed (Costet et al 1987;Charlet et al 1988). There have been few other studies on insect utilization of plants with an altered sterol profile, in particular studies on holometabolous insect pests and on insects that harbour symbionts.…”

Metabolism of dietary Δ8‐sterols and 9β, 19‐cyclopropyl sterols by Locusta migratoria

“…In conclusion, the changes in sterol content of experimental animals or eggs are stronger in the ester than in the free sterol fraction. Previous analyses performed on the hemolymph of females reared on experimental and normal wheat have shown that the major difference between the two was a 90% reduction of the titer of cholesterol and an accumulation of 5a-cholest-8-en-3P-01 and of 24-methyl pollinastanol (18) in the experimental hemolymph [23]. The present studies show an addition that steryl esters are absent in the blood from control animals and present in trace amounts in experimental animals.…”

Distribution and Biosynthesis of 20-Hydroxyecdysone in Plants ofAchyranthes japonicaNakai

“…This level was expected to be sufficient because 20E in insects is known to be present at about 10 mg/g DW. [28][29][30] The high level of PEs in these vital plant organs, requiring intensive protection, is well-documented in previous reports. 2,17,20,31) Thus, many of the plants containing PEs appear to be able to accumulate PEs in organs at high levels for protection against non-adapted insects.…”