Taste detection of the non-volatile isothiocyanate moringin results in deterrence to glucosinolate-adapted insect larvae

Phytochemistry. 2015 Oct:118:139-48. doi: 10.1016/j.phytochem.2015.08.007. Epub 2015 Aug 25.

Abstract

Isothiocyanates (ITCs), released from Brassicales plants after hydrolysis of glucosinolates, are known for their negative effects on herbivores but mechanisms have been elusive. The ITCs are initially present in dissolved form at the site of herbivore feeding, but volatile ITCs may subsequently enter the gas phase and all ITCs may react with matrix components. Deterrence to herbivores resulting from topically applied volatile ITCs in artificial feeding assays may hence lead to ambiguous conclusions. In the present study, the non-volatile ITC moringin (4-(α-L-rhamnopyranosyloxy)benzyl ITC) and its glucosinolate precursor glucomoringin were examined for effects on behaviour and taste physiology of specialist insect herbivores of Brassicales. In feeding bioassays, glucomoringin was not deterrent to larvae of Pieris napi (Lepidoptera: Pieridae) and Athalia rosae (Hymenoptera: Tenthredinidae), which are adapted to glucosinolates. Glucomoringin stimulated feeding of larvae of the related Pieris brassicae (Lepidoptera: Pieridae) and also elicited electrophysiological activity from a glucosinolate-sensitive gustatory neuron in the lateral maxillary taste sensilla. In contrast, the ITC moringin was deterrent to P. napi and P. brassicae at high levels and to A. rosae at both high and low levels when topically applied to cabbage leaf discs (either 12, 120 or 1200 nmol moringin per leaf disc of 1cm diameter). Survival of A. rosae was also significantly reduced when larvae were kept on leaves treated with moringin for several days. Furthermore, moringin elicited electrophysiological activity in a deterrent-sensitive neuron in the medial maxillary taste sensillum of P. brassicae, providing a sensory mechanism for the deterrence and the first known ITC taste response of an insect. In simulated feeding assays, recovery of moringin was high, in accordance with its non-volatile nature. Our results demonstrate taste-mediated deterrence of a non-volatile, natural ITC to glucosinolate-adapted insects.

Keywords: Brassicales; Deterrent; Glucosinolate; HPLC–MS/MS; Isothiocyanate; NMR; Neuron; Sensory physiology; Specialist herbivores; Stimulant; Taste.

MeSH terms

  • Animals
  • Brassicaceae / chemistry*
  • Choline / analogs & derivatives
  • Choline / chemistry
  • Feeding Behavior / physiology
  • Glucosinolates / chemistry*
  • Herbivory / physiology
  • Hymenoptera / physiology
  • Isothiocyanates / analysis*
  • Isothiocyanates / chemistry
  • Isothiocyanates / isolation & purification
  • Isothiocyanates / pharmacology*
  • Larva / drug effects*
  • Lepidoptera / physiology
  • Nuclear Magnetic Resonance, Biomolecular
  • Plant Leaves
  • Rhamnose / analogs & derivatives*
  • Rhamnose / chemistry
  • Rhamnose / pharmacology
  • Taste / physiology*

Substances

  • 4-((alpha-L-rhamnosyloxy)benzyl)isothiocyanate
  • Glucosinolates
  • Isothiocyanates
  • isothiocyanate moringin
  • isothiocyanic acid
  • Choline
  • Rhamnose
  • sinalbin