Abstract High-nighttime-temperature (HNT) poses a major challenge to tomato (Solanum lycopersicum L.) growth and productivity. To elucidate the molecular basis of HNT responses, this study systematically examined the morphological and transcriptomic changes in tomato seedlings under prolonged HNT stress. We observed that HNT suppressed plant growth and chlorophyll content while triggering H2O2 accumulation in new leaves; concurrently, it promoted thermomorphogenesis-related adaptations like reduced leaf angles and lower leaf trichome density, traits potentially facilitating heat dissipation. Transcriptome profiling identified 4,551 differentially expressed genes (DEGs), comprising 2,104 up-regulated and 2,447 down-regulated genes. Functional enrichment analysis revealed that up-regulated DEGs were primarily involved in glycosyl transfer, flavonoid biosynthesis, mismatch repair, and protein processing, whereas down-regulated DEGs were enriched in photosynthesis, metabolic, and immune signaling. These changes suggest a strategic trade-off, with down-regulated photosynthetic and metabolic activities potentially enabling the reallocation of resources toward stress resilience mechanisms. As a central heat shock response (HSR) mechanism, the SlHSPs-SlHSFs system responded to HNT, with 10-day stress inducing distinct expression patterns of SlHSP70/90 genes alongside concurrent suppression of SlHSFs. qPCR analysis unveiled a transcriptional shift in SlHSFs from an initial shock phase, marked by pronounced expression changes at 1-day HNT, to a sustained acclimation phase. Prolonged HNT also triggered gene-specific expression changes in the unfolded protein response (UPR) pathway, as well as in genes involved in ROS homeostasis and hormone signaling. In addition, it increased alternative splicing in genes associated with antioxidant defense, DNA repair, and protein processing. Collectively, these transcriptomic alterations reflect a systemic reprogramming that prioritizes energy conservation, redox homeostasis, and macromolecular stability to support nocturnal heat acclimation. Our findings provide novel insights into tomato adaptation to HNT and offer valuable genetic resources and a theoretical foundation for breeding HNT-resilient tomato varieties.
Fang et al. (Sun,) studied this question.