Characterization of the detrimental effects of type IV glandular trichomes on the aphid Macrosiphum euphorbiae in tomato

Abstract

BACKGROUND Glandular trichomes are essential in plants' defence against pests however, the mechanisms of action are not completely understood. While there is considerable evidence of feeding and movement impairment by trichomes, the effect on other traits is less clear. We combined laboratory and greenhouse experiments with molecular analysis to understand how glandular trichomes affect the behavior, population growth, and the expression of biomarkers involved in detoxification, primary metabolism, and developmental pathways of the aphid Macrosiphum euphorbiae. We used two isogenic tomato lines that differ in the presence of type IV glandular trichomes and production of acylsucroses; i.e.,Solanum lycopersicum cv. ‘Moneymaker’ and an introgressed line from Solanum pimpinellifolium (with trichomes type IV). RESULTS Type IV glandular trichomes affected host selection and aphid proliferation with aphids avoiding, and showing impaired multiplication on the genotype with trichomes. The exposure to type IV glandular trichomes resulted in the overexpression of detoxication markers (i.e., Hsp70, Hsp17, Hsp10); the repression of the energetic metabolism (GAPDH), and the activation of the ecdysone pathway; all these, underlying the key adaptations and metabolic trade‐offs in aphids exposed to glandular trichomes. CONCLUSION Our results demonstrate the detrimental effect of glandular trichomes (type IV) on the aphid and put forward their mode of action. Given the prevalence of glandular trichomes in wild and cultivated Solanaceae; and of the investigated molecular biomarkers in insects in general, our results provide relevant mechanisms to understand the effect of trichomes not only on herbivorous insects but also on other trophic levels.

Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses

“…Data of no-choice assay performed under the same conditions described the preference of aphid choice for MM (70%) comparing to that of aphid choosing an ABL 10–4 plant (30%) 40 . A clear effect of plant genotype on the selection rate was also observed under free-choice conditions, when aphids could choose either MM or ABL 10–4 42 . Since aphids seem not to feed on ABL10-4 plants as regularly as on MM plants, they might not induce the secretion of detoxification proteins located in saliva to response to oxidative stress provoked by plants.…”

“…The level of reserves accumulated in the fat body modulates several essential aspects of the insect's life, such as the rate of insect growth, the timing of metamorphosis, and egg development 65 . The observed results at the transcriptomic level on carbohydrate, energy and lipid metabolism genes show the inhibition of the corresponding metabolic pathways and, consequently, point at the metabolic basis for the impairment observed in feeding, growth, oviposition in aphids reared on ABL10-4 plants 42 .…”

“…For each sample, RNA was extracted from 25 apterous and viviparous females using TRIzol Reagent (Invitrogen, USA) following the manufacturer's instructions as described in previously 42 .…”

“…Further, low-quality (Phred value < 33) and adaptor sequences from the raw data were removed using the Trimmomatic (v0.32) tool. Assembly and annotation were performed as described previously 42 .…”

“…Secondary metabolites also contribute to defence against a variety of insects, including whiteflies 34 – 37 , aphids 38 , spider mites 25 , and leaf miners 39 . Cultivated tomato (in contrast to wild species) lacks many of these secondary metabolites and its glandular trichomes, making them relatively susceptible to a wide range of pests 31 , 40 – 42 .…”