Jasmonic acid-regulated putrescine biosynthesis attenuates cold-induced oxidative stress in tomato plants

•Cold promotes accumulation of putrescine (Put) and jasmonic acid (JA).•JA increases Put accumulation and cold tolerance.•Suppression of JA signaling reduces Put accumulation.•JA-regulated Put biosynthesis attenuates cold-triggered oxidative stress. Previous studies have shown that jasmonic acid (JA) and putrescine (Put), a major polyamine, are both accumulated in tomato plants upon cold treatment. However, it is unclear whether JA regulates Put biosynthesis in tomato plants under the cold condition. The goal of the present work was to determine whether JA regulates Put biosynthesis and how JA-regulated Put accumulation affects cold tolerance in tomato plants. We found that among three major polyamines, putrescine was predominantly accumulated in cold-stressed tomato plants and exogenous putrescine markedly alleviated cold-induced oxidative stress, indicating an important role of putrescine in tomato cold response. We then identified ADC1 as a major putrescine biosynthetic gene in response to cold and JA. Further experiments using a JA biosynthesis inhibitor sodium diethyldithiocarbamate (DIECA), MeJA and an ADC (arginine decarboxylase 1) enzyme inhibitor difluoromethylarginine (DFMA) confirmed that JA functions in the putrescine biosynthesis by acting on ADC. Finally, we found that RNAi-mediated suppression of MYC2, a master regulator of JA signaling, decreased the expression of ADC1, reduced putrescine accumulation and enhanced cold-induced oxidative damages, implying that JA-induced putrescine biosynthesis relies, at least partially, on MYC2 in tomato plants. Our study thus establishes a link between JA signaling and polyamine metabolism in tomato plants under cold stress. Our data support that JA signaling is crucial for putrescine biosynthesis during cold stress and JA-induced accumulation of putrescine mitigates cold-induced oxidative stress in plants.