Periodic outbreaks of spruce budworm (SBW) affect large areas of ecologically and economically important conifer forests in North America, causing tree mortality and reduced forest productivity. Host resistance against SBW has been linked to growth phenology and the chemical composition of foliage, but the underlying molecular mechanisms and population variation are largely unknown. Using a genomics approach, we discovered a β-glucosidase gene, Pgβglu-1, whose expression levels and function underpin natural resistance to SBW in mature white spruce (Picea glauca) trees. In phenotypically resistant trees, Pgβglu-1 transcripts were up to 1000 times more abundant than in non-resistant trees and were highly enriched in foliage. The encoded PgβGLU-1 enzyme catalysed the cleavage of acetophenone sugar conjugates to release the aglycons piceol and pungenol. These aglycons were previously shown to be active against SBW. Levels of Pgβglu-1 transcripts and biologically active acetophenone aglycons were substantially different between resistant and non-resistant trees over time, were positively correlated with each other and were highly variable in a natural white spruce population. These results suggest that expression of Pgβglu-1 and accumulation of acetophenone aglycons is a constitutive defence mechanism in white spruce. The progeny of resistant trees had higher Pgβglu-1 gene expression than non-resistant progeny, indicating that the trait is heritable. With reported increases in the intensity of SBW outbreaks, influenced by climate, variation of Pgβglu-1 transcript expression, PgβGLU-1 enzyme activity and acetophenone accumulation may serve as resistance markers to better predict impacts of SBW in both managed and wild spruce populations.

Phenolic compounds are apparently important in the defence mechanisms of conifers. To test the hypothesis that phenolic compounds in resistant white spruce [Picea glauca (Moench) Voss (Pinaceae)] impart resistance against spruce budworm [Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae)], we performed aqueous extractions of current-year shoots of white spruce that were tolerant of varying levels of budworm defoliation. High-performance liquid chromatographic profiles of water extracts of P. glauca needles differed between resistant and susceptible trees. Further nuclear magnetic resonance analyses identified two phenolic glucosides in susceptible white spruce, picein [3-(b-D-glucosyloxy)-hydroxy-acetophenone] and pungenin [3-(b-D-glucosyloxy)-4-hydroxy-acetophenone], and two phenolics in resistant white spruce, pungenol (3¢,4¢-hydroxy-acetophenone) and piceol (4¢-hydroxyacetophenone). We focused on the performance of spruce budworm when piceol and pungenol were added to the diet. These two compounds significantly reduced larval survival, retarded development, and reduced pupal mass. Food consumption by sixth-instar spruce budworms was affected by a combination of the phenolic compounds. These results suggest that the two phenolic compounds reduce the pressure of spruce budworm herbivory on specific host tree phenotypes. Thus, the mechanism of defence in P. glauca apparently reflects a strategy of constitutive resistance.

The pattern of feeding of Eastern spruce budworm Choristoneura fumiferana (Clem.) (Lepidoptera, Tortricidae) is compared on foliage from white spruce Picea glauca (Moench) Voss. (Pinaceae) trees previously determined to be susceptible and resistant to defoliation by budworm. No differences are observed in electrophysiological responses from taste sensilla to aqueous extracts of the two foliage types, nor is there a preference for either extract type in a choice test. Acetone extracts from the two foliage types are both preferred to a control sucrose solution, although neither elicits a preference relative to the other. These results suggest that there is no difference in phagostimulatory power of internal leaf contents of the two foliage types. Longer‐term observation of feeding behaviour in a no‐choice situation shows no difference in meal duration, confirming the lack of difference in phagostimulatory power. However, on average, intermeal intervals are twice as long on the resistant foliage, leading to an overall lower food consumption during the assay. This result suggests an anti‐digestive or toxic effect of the resistant foliage that slows behaviour and limits food intake. Previous research has shown that waxes of the resistant foliage deter initiation of feeding by the spruce budworm and that this foliage contains higher levels of tannins and monoterpenes. The data suggest that the resistant foliage contains a post‐ingestive second line of defence against the spruce budworm.