Müller Caroline, van Loon Joop, Ruschioni Sara, De Nicola Gina Rosalinda, Olsen Carl Erik, Iori Renato, Agerbirk Niels
Chemical Ecology, Bielefeld University, Universitätsstr. 25, 33615 Bielefeld, Germany.
Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.
Phytochemistry. 2015 Oct;118:139-48. doi: 10.1016/j.phytochem.2015.08.007. Epub 2015 Aug 25.
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.
异硫氰酸盐(ITCs)是十字花科植物中硫代葡萄糖苷水解后释放出来的,以其对食草动物的负面影响而闻名,但其作用机制一直难以捉摸。ITCs最初以溶解形式存在于食草动物取食部位,但挥发性ITCs随后可能进入气相,所有ITCs都可能与基质成分发生反应。因此,在人工饲养试验中局部施用挥发性ITCs对食草动物产生的威慑作用可能会导致模棱两可的结论。在本研究中,研究了非挥发性ITC辣木素(4-(α-L-鼠李糖基氧基)苄基ITC)及其硫代葡萄糖苷前体葡萄糖辣木素对十字花科专业昆虫食草动物行为和味觉生理的影响。在饲养生物测定中,葡萄糖辣木素对适应硫代葡萄糖苷的小菜蛾(鳞翅目:粉蝶科)和玫瑰三节叶蜂(膜翅目:叶蜂科)幼虫没有威慑作用。葡萄糖辣木素刺激了相关的菜粉蝶(鳞翅目:粉蝶科)幼虫的取食,并从外侧上颌味觉感器中对硫代葡萄糖苷敏感的味觉神经元引发了电生理活动。相比之下,当将ITC辣木素局部施用于直径1厘米的甘蓝叶圆片(每片叶圆片分别为12、120或1200纳摩尔辣木素)时,高浓度的辣木素对小菜蛾和菜粉蝶有威慑作用(高、低浓度均对玫瑰三节叶蜂有威慑作用)。当幼虫在经辣木素处理的叶片上饲养数天时,玫瑰三节叶蜂的存活率也显著降低。此外,辣木素在菜粉蝶内侧上颌味觉感器中对威慑敏感神经元引发了电生理活动,为威慑作用提供了一种感觉机制,这也是昆虫首次已知的ITC味觉反应。在模拟饲养试验中,根据辣木素的非挥发性性质,其回收率很高。我们的结果表明,一种非挥发性天然ITC对适应硫代葡萄糖苷的昆虫具有味觉介导的威慑作用。