Physiological response of Colorado potato beetle and beet armyworm larvae to depletion of wound-inducible proteinase inhibitors in transgenic potato plants

Larvae of Colorado potato beetle (CPB), Leptinotarsa decemlineata, and beet armyworm (BAW), Spodoptera exigua, reared on potato plants in which wound-induced accumulation of proteinase inhibitors (PIs) was largely reduced through antisense-mediated depletion of a specific lipoxygenase (LOX H3) had significantly larger weight gains than those fed on non-transformed plants. The midgut endoproteolytic activities of CPB larvae fed on non-transformed potato were significantly higher than those from larvae fed on LOX-H3-deficient plants. However, none of these proteolytic activities was inhibited by potato leaf extracts, regardless of the plant that they were fed on. Taken together, these data suggest that CPB, a leaf-feeding specialist of solanaceous plants, is largely adapted to the inducible PIs of potato, though the metabolic cost associated with the hyperproduction of digestive proteases may account for the 14–31% lower weight gain of larvae fed on non-transformed plants. The effect of LOX-H3 depletion on insect performance was more evident with larvae of the polyphagous BAW (52–63% higher weight gain and 73% higher fecundity when reared on LOX-H3-deficient plants). The poorer larval performance of BAW on non-transformed plants may be due to the susceptibility to inhibition by potato leaf tissues of most BAW digestive proteases. Indeed, BAW larvae fed on non-transformed potato showed a significant reduction in most endoproteolytic activities compared to larvae fed on LOX-H3-deficient plants, suggesting a that these insects deal poorly with induced plant defences in potato.