Tephritis Angustipennis-Induced Flavonoid Dynamics Drive Cross-Species Pest Resistance in Aster spp.

Abstract

Flowering Aster species (Aster spp.) native to the high-altitude (3753 m on average) Three Rivers Source Region are frequently damaged by Tephritis angustipennis, imposing significant stress that negatively impacts their survival and productivity. This study reveals that pest stress enhances antioxidant enzyme activity (CAT, POD, SOD, and PPO) and increases secondary metabolites, particularly flavonoids, in Aster flowers. Integrated transcriptomic and metabolomic analyses identified differential responses among three Aster varieties exhibiting distinct resistance levels. We found that increasing pest stress, particularly under serious-hazard (HH) conditions, upregulates resistance-related genes and promotes the accumulation of phenolic and terpenoid compounds. Pest feeding activates the flavonoid biosynthesis pathway, with key enzyme genes (PAL, CAD, HCT, FLS, and CYP) being upregulated, reflecting a rapid physiological response that enhances resistance. Notably, flavonoid synthesis is dynamically regulated in response to stress. Under HH conditions, quercetin and kaempferol levels decrease, while phlorizin, kaempferide, sakuranetin, and isosakuranetin increase, indicating a complex defense strategy. Overall, pest-induced flavonoid accumulation helps delay the process of flower aging and deterioration, thereby enhancing seed yield. These findings provide valuable insights into the molecular defense mechanisms of Aster spp., offering potential targets for breeding pest-resistant varieties and developing effective pest management strategies.