Sub-Low Temperature Preconditioning Induced Cold Signaling and Antiviral Defenses Correlate with Reduced TSWV Accumulation in Tomato

Tomato spotted wilt disease, caused by Tomato spotted wilt virus (TSWV), poses a severe, widespread threat to commercial crop production. Triggering endogenous plant defense capacity serves as a promising tactic for sustainable disease control. Environmental factors, such as temperature, can modulate plant metabolic activities to suppress disease development. To characterize how sub-low temperatures shape tomato responses to TSWV, we maintained tomato seedlings under three regimens: room temperature (25 °C) and two sub-low temperatures (15 °C and 10 °C). Subsequent viral inoculation and phenotypic monitoring revealed that 15 °C pretreatment was associated with markedly reduced TSWV disease severity. RT-qPCR quantification further demonstrated that this 15 °C priming correlated with diminished accumulation of the viral NSs gene. Transcriptome profiling indicated that the 15 °C regime was linked to coordinated activation of cold acclimation pathways, hormone signaling cascades, and antiviral defense programs, which correlated with reduced TSWV accumulation. Specifically, 15 °C conditioning was correlated with the induction of a cold-responsive transcriptional network that overlaps with plant antiviral immune responses. This activated transcriptional signature is putatively associated with the stimulation of defensive cascades, maintenance of cellular homeostasis, and lowered viral accumulation, which collectively align with alleviated spotted wilt symptoms. To our knowledge, this work presents the first correlative evidence associating 15 °C sub-low temperature preconditioning with reduced TSWV accumulation in tomato. Collectively, these observations highlight the potential of temperature manipulation as a chemical-free disease mitigation approach and provide a valuable reference for sustainable crop protection strategies.