Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis

Abstract

Cold signals interact with other environmental cues to modulate plant developmental processes. Recent studies have shown that many Pathogenesis-Related (PR) genes are induced and disease resistance is enhanced after exposure to low temperatures, linking cold signals with pathogenesis in plants. However, the underlying molecular mechanisms and signaling schemes are largely unknown. Here, we demonstrate that cold stimulates proteolytic activation of a plasma membrane-tethered NAC (NAM/ATAF1/2/CUC2) transcription factor NTL6. The transcriptionally active NTL6 protein enters the nucleus, where it induces a subset of PR genes by directly binding to a conserved sequence in the promoters of cold-responsive PR genes, such as PR1, PR2, and PR5. While transgenic plants overexpressing an active NTL6 form exhibited enhanced disease resistance, RNAi plants with reduced NTL6 activity were more susceptible to pathogen infection at low temperatures. Accordingly, cold induction of PR1 disappeared in the RNAi plants. Consistent with the close relationship between cold and pathogenesis, cold-acclimated plants showed enhanced resistance to pathogen infection. In this signaling cascade, controlled activation of the membrane-tethered, dormant NTL6 transcription factor serves as a molecular link that incorporates cold signals into pathogen resistance responses. However, the NTL6-mediated cold induction of the PR genes is independent of salicylic acid ( SA). The PR genes were still induced by SA in the NTL6 RNAi plants. Cold regulation of the PR genes through the membrane-mediated transcriptional control is thought to be an adaptive process that ensures quick plant responses to incoming pathogens that frequently occur during cold seasons.