Dynamic Root-Zone Temperature Regulation Enhances Cherry Tomato Productivity Through Coordinated Root and Leaf Responses

Low and fluctuating root-zone temperatures constrain tomato productivity during winter greenhouse cultivation, yet the advantages of dynamic regulation over fixed-temperature control remain unclear. In this study, cherry tomato plants were subjected to an unregulated control (CK), three constant root-zone temperatures (15, 20, and 25 °C), and dynamic temperature treatment (DT). The experiment was conducted in a commercial winter greenhouse, where cherry tomato plants were grown in coconut coir and monitored from 70 to 145 days after transplanting, with five plants per treatment; root-zone temperature was regulated by circulating water through pipes embedded in the cultivation troughs. DT maintained root-zone temperature within 14.9–22.2 °C while reducing cumulative pump operating time by 11.45–21.23% relative to the fixed-temperature treatments. DT sustained high root activity during reproductive development, promoted dry-matter allocation to fruits, accelerated fruit expansion, and achieved the highest total and fourth-truss yields. In leaves, DT improved PSII photochemical performance, as indicated by increased PIABS and ΦPSII and reduced DI0/RC. It also maintained relatively low POD and SOD activities, comparatively high CAT activity during fruit expansion, and lower MDA accumulation, indicating reduced oxidative pressure and membrane lipid peroxidation. Transcriptomic responses were strongly stage-dependent, with the most pronounced changes occurring during fruit setting and expansion. Differentially expressed genes were mainly associated with auxin response, electron transfer, protein-disulfide reduction, cellular redox homeostasis, and phosphorylation-related processes. WGCNA further identified trait-associated modules linked to mitochondrial electron transport and oxidative phosphorylation, including eight candidate genes associated with respiratory complexes I, III, IV, and V. Collectively, dynamic root-zone temperature regulation improved the temporal matching between thermal supply and crop developmental demand, thereby sustaining root activity, optimizing leaf photochemical and redox status, and promoting dry-matter allocation to fruits. Transcriptomic and WGCNA analyses integrally indicate that mitochondrial electron transport and oxidative phosphorylation may participate in the leaf response to dynamic root-zone temperature regulation.