Systemic deterrence of aphid probing and feeding by novel β-damascone analogues

Beata Gabrys 0 1 2 3 Katarzyna Dancewicz 0 1 2 3 Anna Gliszczyn ska 0 1 2 3 Bo z_ena Kordan 0 1 2 3 Czesaw Wawrzen czyk 0 1 2 3 0 A. Gliszczyn ska C. Wawrzen czyk Department of Chemistry, Wrocaw University of Environmental and Life Sciences , Wrocaw , Poland 1 B. Gabrys (&) K. Dancewicz Department of Botany and Ecology, University of Zielona Go ra , Szafrana 1, 65-516 Zielona Go ra , Poland 2 Communicated by B. Lavandero 3 B. Kordan Department of Phytopathology and Entomology, University of Warmia and Mazury , Olsztyn , Poland b-Damascone appeared a weak attractant close to not active to Myzus persicae, but modifications of its structure caused the avoidance of treated leaves by aphids during settling and reluctance to probe in simple choice- and no-choice experiments in previous studies. Here, the electrical penetration graph (EPG) technique, which allows monitoring of aphid probing within plant tissues, was applied to explore the biological background and localisation in plant tissues of the deterrent activities of b-damascone and its analogues. Activity of b-damascone and b-damascone-derived compounds depended on their substituents, which was manifested in the variation in the potency of the behavioural effect and differences in aphid probing phases that were affected. b-Damascone appeared a behaviourally inactive compound. The moderately active b-damascone ester affected aphid activities only during the phloem phase. The highly active deterrentsdihydro-b-damascol, b-damascone acetate, d-bromo-c-lactone, and unsaturated c-lactone-affected pre-phloem and phloem aphid probing activities. The most effective structural modification that evoked the strongest negative response from M. persicae was the transformation of b-damascone into d-bromo-c-lactone. The behavioural effect of this transformation was demonstrated in frequent interruption of probing in peripheral tissues, which caused repeated failures in finding sieve elements, and reduction in the ingestion time during the phloem phase in favour of watery salivation. The inhibition of aphid probing at both the pre-phloem and phloem levels reveals the passage of the compounds studied through the plant surface and their distribution within plant tissues in a systemic way, which may reduce the risk of the transmission of non-persistent and persistent viruses. - Aphids (Homoptera: Aphididae) are responsible for at least 2 % of all losses in the annual world crops caused by insect feeding (Wellings et al. 1989). Additionally to the removal of assimilates from plant phloem-transporting vessels, aphids transfer virus diseases from infected to healthy plants. This activity, due to the specific piercing-sucking mode of feeding, is very efficient: it is estimated that more than 50 % of all insect-borne plant viruses are spread by aphids and it is believed that the indirect damage caused by aphids due to virus transmission exceeds their direct impact on crops (Katis et al. 2007; Brault et al. 2010). The peach potato aphid Myzus persicae (Sulz.) alone can transmit over 100 plant viruses among plants of over 40 families (Blackman and Eastop 1985). At the same time, M. persicae is one of 20 aphid species that developed clones resistant to one or more insecticides, and the resistance mechanisms are the most frequent and diverse (Dedryver et al. 2010). Typical probing activities known in aphids consist of two basic phases: the pre-ingestive pathway phase (intercellular within-plant stylet penetration including the uptake of small samples of contents from cells adjacent to the stylet route) and ingestive phase (active or passive uptake of xylem or phloem sap, respectively) (Pettersson et al. 2007). During the brief intracellular probes in the epidermis and parenchyma (mesophyll in leaves) that precede feeding in phloem vessels, aphids may transmit non-persistent and semi-persistent viruses, and when aphid stylets reach sieve elements, persistent viruses may be vectored (Prado and Tjallingii 1994; Tjallingii et al. 2010). The elimination or at least reduction of penetration of plant tissues by aphids may save plants from pathogen infection. Therefore, the disruption of the host plant selection strategy by interference in the fixed scheme of aphid activities through the application of various behaviour-modifying chemicals is one of the promising approaches that may result in a decline in aphid infestation (Pickett 1991). Considering the high biological activity of lower terpenoids, several attempts have been made to apply these compounds or their analogues as alternatives to conventional neurotoxic chemicals in pest insect control. In our previous studies (e.g. Gabrys et al. 2005), we found that lower terpenoids of plant origin can seriously affect aphid behaviour and prevent them from feeding and settling. Citral and linalool had repellent activity, manifested in a significant decrease in time spent on leaves, a decrease in the total and mean duration of penetration, (...truncated)