LAUSR

Abstract Cold adversely affects tomato (Solanum lycopersicum) growth and yield during winter and early spring in northern China. Trehalose (Tre) is a growth regulator that is widely used to enhance plant stress tolerance. However, there are few reports on the mechanistic role of Tre in regulating tomato cold tolerance or the interactions between hydrogen peroxide (H2O2) and nitric oxide (NO) in Tre-induced cold stress tolerance in plants. Here, we explored the role of Tre in tomato cold tolerance and evaluated whether H2O2 and NO were involved in this regulation. Tre pretreatment significantly upregulated superoxide dismutase (Cu/Zn SOD) and glutathione reductase (GR1) transcription and increased catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR) activities under normal temperatures. Under cold stress, Tre pretreatment dramatically elevated Cu/Zn SOD and CAT1 transcription and increased SOD and CAT activities. Tre pretreatment reduced membrane lipid peroxidation and alleviated plant growth inhibition caused by cold stress conditions. Under normal temperatures, Tre pretreatment upregulated the expression of respiratory burst oxidase homolog1 (RBOH1), nitrate reductase (NR), and nitric oxide synthase (NOS) and elevated H2O2 and NO levels. Treating tomato leaves with H2O2 and NO scavengers [dimethylthiourea (DMTU) and 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), respectively] significantly diminished Tre-mediated alleviation of membrane lipid peroxidation. The effect of H2O2 on reducing cold stress-induced damage in tomato was essentially abolished by cPTIO treatment. These results indicated that exogenous Tre enhanced cold stress tolerance in tomato by regulating the antioxidant defense system. Tre may act as an exogenous inducer of H2O2 and NO that regulate antioxidase gene expression and activities to promote plant responses to cold stress, enhance cold stress tolerance, and reduce membrane lipid peroxidation and cellular injury. NO may act downstream of H2O2 to mediate Tre-regulated tomato oxidative stress tolerance under cold stress.