Plasma-activated water reprograms the root–rhizosphere continuum to enhance nitrogen use efficiency and sustain maize productivity under reduced nitrogen input

Improving nitrogen use efficiency (NUE) while sustaining crop productivity is a major challenge for sustainable maize production. Plasma-activated water (PAW), enriched with reactive oxygen and nitrogen species, has emerged as a promising biostimulant for enhancing nutrient acquisition and plant performance. This study evaluated the effects of PAW on root architecture, rhizosphere metabolism, nitrogen acquisition, agronomic nitrogen use efficiency (ANUE), and grain yield (GY) under four nitrogen application rates (0, 50, 75, and 100% of the recommended dose) in maize grown under controlled polyhouse conditions. PAW significantly increased root surface area (RSA), root hair density (RHD), root hair length (RHL), total organic carbon (TOC), organic acid secretion (OAS), free amino acid (FAA) accumulation, nitrogen uptake, GY, harvest index (HI), and ANUE compared with normal water irrigation (P ≤ 0.001). Field Emission Scanning Electron Microscopy (FESEM) revealed pronounced root hair proliferation and elongation under PAW, particularly at 75% nitrogen, while High-Performance Liquid Chromatography (HPLC) demonstrated greater accumulation of citric, malic, succinic, and oxalic acids, indicating enhanced rhizosphere carbon metabolism and nutrient mobilization. Multivariate analyses identified coordinated regulation of root and rhizosphere traits as the principal driver of productivity. Principal component analysis explained 95.2% of the total variation and clearly separated PAW + 75% N and PAW + 100% N from the remaining treatments. Pearson correlation and hierarchical clustering analyses demonstrated strong positive associations among RSA, rhizosphere metabolites, nitrogen uptake, GY, and HI, confirming an integrated root–rhizosphere functional network. Piecewise latent path analysis revealed that improved root architecture enhanced rhizosphere activity (β = 0.631), leading to improved nitrogen acquisition (β = 0.697), and ultimately higher grain productivity (β = 1.043). Random Forest analysis identified nitrogen uptake (27.99%), HI (22.95%), FAA (19.27%), TOC, and RSA as the strongest predictors of GY. PAW + 75% N achieved the highest Treatment Performance Index, outperforming PAW + 100% N and sustaining superior productivity with 25% lower fertilizer nitrogen application. These findings demonstrate that PAW reprograms the root–rhizosphere–nitrogen acquisition continuum to maximize NUE, providing a mechanistic framework for improving nitrogen acquisition under controlled polyhouse conditions; field validation is required before broad agronomic application.