Ozone-induced alterations in multi-element nutrient resorption reveal three interacting control strategies in poplar

Abstract

Tropospheric ozone (O₃) pollution is increasingly recognized as a major stressor to forest ecosystems, particularly through its interference with plant nutrient cycling processes. However, the mechanistic basis by which O₃ influences the resorption of multiple essential nutrients remains inadequately characterized. In this study, we conducted a controlled open-top chamber experiment using hybrid poplar ‘107’ (Populus euramericana cv. ‘74/76’) to systematically assess the effects of elevated O₃ exposure (ranging from 19.2 to 99.0 ppb) on the resorption efficiency (RE) of six key macronutrients: nitrogen (N), phosphorus (P), sulfur (S), potassium (K), calcium (Ca), and magnesium (Mg). Elevated O₃ consistently enhanced the RE of N and S that are fundamental to core metabolic processes while reducing the RE of K, Mg, P, and Ca. Notably, K and Mg accumulated in senesced foliage at high O₃ doses, with critical thresholds observed at 46.0 and 41.7 ppm·h, respectively. These results suggest a trade-off in nutrient retrieval priorities, where O₃-induced oxidative stress favors the conservation of nutrients central to metabolic integrity (N, S), at the expense of those involved in osmotic balance (K) and photoprotection (Mg). Through a combination of power-law regression and structural equation modeling, we identified a triadic framework of coexisting nutrient resorption controls: (1) nutrient concentration control, influencing RE across N, P, S, K, and Mg; (2) nutrient limitation control, specifically modulating N and P based on their functional scarcity; and (3) stoichiometric control, preserving internal N:P ratios in senescing leaves. Elevated O₃ triggered a transition from phosphorus limitation to nitrogen limitation, revealing a disproportionate disruption in nitrogen-related metabolic pathways under oxidative stress. At the mechanistic level, the observed changes in RE were mediated through two interconnected pathways: direct physiological impairment of nutrient translocation processes (e.g., damage to membrane transport systems) and indirect modulation of soil–plant-microbe interactions, including shifts in soil pH and microbial community composition. Collectively, these findings offer new insights into how chronic O₃ exposure reshapes nutrient resorption dynamics and regulatory mechanisms in trees. They also provide a conceptual foundation for forecasting forest ecosystem responses to atmospheric oxidative stress. This study underscores the critical need for species-specific investigations and sustained monitoring of nutrient fluxes in O₃-impacted environments, with significant implications for adaptive forest management under changing air quality conditions.

Keywords

Nutrient limitation / Nutrient resorption efficiency / Ozone pollution / Soil–plant-microbe interactions / Stoichiometric control

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