Cold-priming uncouples cold and light regulation of otherwise tightly co-regulated genes. In this study, we focused on the early regulatory processes in Arabidopsis within the first 2 h in cold and in high light after a 5-d lag-phase at 20 °C and 24 h cold-priming at 4 °C. Priming quickly modified gene expression in a trigger-specific manner. In the early stress-response phase during cold and high-light triggering, it reduced the regulatory amplitudes of many up- and down-regulated genes. A third of the priming-regulated genes were jasmonate-sensitive, including the full set of genes required for oxylipin biosynthesis. Analysis of wild-type and mutant plants based on qPCR demonstrated that biosynthesis of the jasmonic acid (JA) precursor 12-oxo phytenoic acid (OPDA) relative to the availability of JA dampened the response of the genes for oxylipin biosynthesis. In oxylipin biosynthetic mutants, cold-priming more strongly affected genes involved in the biosynthesis of OPDA than in its conversion to JA. In addition, priming-dependent dampening of the triggering response was more linked to OPDA than to regulation of the JA concentration. Spray application of OPDA prior to triggering counteracted the priming effect. Regulation of the oxylipin hub was controlled by modulation of the oxylipin-sensitivity of the genes for OPDA biosynthesis, but it was insensitive to priming-induced accumulation of thylakoid ascorbate peroxidase, thus identifying a parallel-acting cold-priming pathway.
