A Localized Pseudomonas syringae Infection Triggers Systemic Clock Responses in Arabidopsis

Abstract

The circadian clock drives daily rhythms of many plantphysiological responses, providing a competitive advantage that improves plant fitness and survival rates [1-5]. Whereas multiple environmental cues are predicted to regulate the plant clock function, most studies focused on understanding the effects of light and temperature [5-8]. Increasing evidence indicates a significant role of plant-pathogen interactions on clock regulation [9, 10], but the underlying mechanisms remain elusive. In Arabidopsis, the clock function largely relies on a transcriptional feedback loopbetween morning (CCA1 and LHY)- and evening (TOC1)-expressed transcription factors [6-8]. Here, we focused on these core components to investigate the Arabidopsis clock regulation using a unique biotic stress approach. We found that a single-leaf Pseudomonas syringae infection systemically lengthened theperiod and reduced the amplitude of circadian rhythms in distal uninfected tissues. Remarkably, the low-amplitude phenotype observed upon infection was recapitulated by a transient treatment with the defense-related phytohormone salicylic acid (SA), which also triggered a significant clock phase delay. Strikingly, despite SA-modulated circadian rhythms, we revealed that the master regulator of SA signaling, NPR1 [11, 12], antagonized clock responses triggered by both SA treatment and P.syringae. In contrast, weuncovered that the NADPH oxidase RBOHD [13] largely mediated the aforementioned clock responses after either SA treatment or the bacterial infection. Altogether, we demonstrated novel and unexpected roles for SA, NPR1, and redox signaling in clock regulation by P.syringae and revealed a previously unrecognized layer of systemic clock regulation by locally perceived environmental cues.