Salicylic Acid Mitigates Drought-Stress-Induced Oxidative Damage in Ilex rotunda Through Tissue-Specific Reprogramming of Antioxidant Phenolics and ROS Scavenging

Drought stress imposes oxidative damage on plants, yet the tissue-specific roles of salicylic acid (SA) in modulating phenolic metabolism remain poorly understood in woody species. Using Ilex rotunda seedlings, we investigated whether exogenous SA (100 µM) mitigates drought-induced oxidative damage and reshapes phenolic profiles in different tissues. Drought alone increased leaf total phenolics by 32% but depleted root phenolics by 29%, whereas combined drought + SA (DSA) treatment partially restored root phenolic levels, coinciding with elevated malondialdehyde (MDA) (2.2-fold in leaves, 2.6-fold in roots) and H2O2. Leaf antioxidant capacity increased under drought (DPPH by 73%, •OH by 33%), whereas root DPPH declined by 27% despite a 26% rise in •OH scavenging. SA alone induced mild oxidative responses and selectively upregulated caffeoylquinic and galloyl derivatives, notably 1-Caffeoylquinic acid (log2FC = 6.38) in leaves. DSA treatment mitigated oxidative damage—reducing leaf MDA by 44% and root H2O2 by 38%. Metabolomics revealed tissue-specific reprogramming leaves accumulated dicaffeoylshikimic acid (log2FC = 10.66) and trilobatin D (log2FC = 11.18) under DSA, whereas roots showed contrasting patterns with up-accumulation of vanillate (log2FC = 5.77) and suppression of 3,5-dicaffeoylquinic acid (log2FC = −7.21) under drought, with stronger metabolic reprogramming in leaves than roots. Our findings indicate that SA-mediated drought tolerance is associated with tissue-specific phenolic reprogramming, identifying candidate indicators that advance the mechanistic understanding of woody plant resilience to drought. These results provide a framework for translating metabolomic signatures into practical strategies for stress mitigation in medicinal perennials facing climate change.