Behavioural quiescence reduces the penetration and toxicity of exogenous compounds in second-stage juveniles of Heterodera glycines

Abstract

Abstract Inactivity in nematodes is often correlated with survival of adverse environments. The non-feeding second-stage juvenile (J2) of Heterodera glycines must survive in a soil environment that may contain numerous toxins. In this report, we show that quiescent J2 of H. glycines survived higher concentrations of both ethanol and the plant-derived compound, allyl isothiocyanate, compared with actively moving nematodes. The mechanism for this quiescence-mediated resistance was investigated using fluorescein isothiocyanate (FITC). There was a reduction in the penetration of FITC in quiescent J2 of H. glycines compared with that in actively moving non-feeding J2. Furthermore, exposure of quiescent nematodes to octopamine, an invertebrate neurotransmitter, induced activity and a subsequent increase in FITC penetration compared with quiescent nematodes exposed to FITC alone. These data demonstrate that behavioural quiescence is correlated with exclusion of the compound from the body of the nematode. Finally, the entry point of FITC into the nematode was examined by the application of a veterinary cyanoacrylate adhesive to occlude either the cephalic or caudal openings of the nematodes. Nematodes glued at the anterior end showed a significant reduction in fluorescence compared with nematodes glued on the posterior end and non-glued nematodes. Thus, the entry of FITC is primarily through openings in the cephalic region. This research is the first report of behavioural quiescence correlated with reduced sensitivity to toxins in a plant-parasitic nematode, and provides insight into how these important organisms cope with stress due to exogenous toxins.