The transcriptomic landscape of the photoperiodic stress response in Arabidopsis thaliana resembles the response to pathogen infection

Plants are exposed to regular diurnal rhythms of light and dark. Changes in the photoperiod by the prolongation of the light period cause photoperiod stress in short day-adapted Arabidopsis thaliana. Here we report on the transcriptional response to photoperiod stress of wild-type A. thaliana and photoperiod stress-sensitive cytokinin signaling and clock mutants. Transcriptomic changes induced by photoperiod stress included numerous changes in reactive oxygen species (ROS)-related transcripts and showed a strong overlap with alterations occurring in response to ozone stress and pathogen attack, which have in common the induction of an apoplastic oxidative burst. A core set of photoperiod stress-responsive genes has been identified, including salicylic acid (SA)-biosynthesis and -signaling genes. Genetic analysis revealed a central role for NPR1 in the photoperiod stress response as npr1-1 mutants were stress-insensitive. Photoperiod stress treatment led to a strong increase in camalexin levels which is also observed in response to pathogen infections. Photoperiod stress induced the resistance of Arabidopsis plants to a subsequent infection by Pseudomonas syringae pv. tomato DC3000 indicating priming of the defence response. Together, photoperiod stress causes transcriptional reprogramming resembling plant pathogen defence responses and induces systemic acquired resistance in the absence of a pathogen. 5-weeks-old short day-grown Arabidopsis plants (WT, ahk2 ahk3, cca1 lhy) were exposed to a 24 h-extended light period (32 h light in total). Sampling for RNAseq analysis was done at 0 h, 4 h, 6 h and 12 h after the end of the prolonged light period. Control plants were sampled on the same moment. For each sampling point, three biological and three technical replicates were taken.