Cooccurring gall morphotypes reveal organ-specific shifts in phenolic metabolism and antioxidant activity in Schinus polygama (Cav.) Cabrera (Anacardiaceae)

Abstract

Gall-inducing insects are modulators of plant metabolism, yet the combined effects of different inducer species on secondary metabolite distribution and function across host organs remain poorly understood. We predicted that (i) branches bearing the three gall morphotypes would exhibit higher overall phenolic and flavonoid accumulation and greater antioxidant activity than nongalled branches, and (ii) this response would not be uniform among organs. To test these predictions, we analyzed total phenols and flavonoids, phenolic composition, histochemical localization, and antioxidant activity in leaves, stems, and three gall morphotypes induced by Calophya mammifex, C. rubra, and Andescecidium parrai on Schinus polygama. Branches bearing galls presented higher total phenol contents than nongalled branches did, although organ-level responses contrasted, with reduced phenols in leaves but increased levels in stems. Gall tissues consistently presented the highest phenolic and flavonoid concentrations. Beyond these quantitative changes, clustering analyses revealed organ-dependent patterns, with leaf galls retaining the phenolic framework of leaf tissues, whereas stem galls showed pronounced divergence and distinctive phenolic signatures. Histochemical analyses further demonstrated marked spatial compartmentalization, with phenolics and flavonols preferentially accumulating in outer tissues but being excluded from feeding sites. These metabolic changes were reflected in antioxidant performance, which was greater in galled organs and more closely associated with qualitative phenolic composition than with total phenolic content alone. Taken together, these results show that the co-occurrence of multiple gall-inducing species is associated with distinct patterns of metabolic and functional organization in S. polygama. Gall induction drives organ-dependent and spatially structured reorganization of secondary metabolism, balancing gall defense and insect performance, and underscores the importance of metabolite compartmentalization in plant–insect interactions.