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

Abstract

SUMMARYCold 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.

Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain

“…Controlled proteolytic release of membrane-bound transcription factors is emerging as a versatile way of inducing rapid transcriptional changes in plants, e.g., in response to environmental changes (26). Recently, the functions of several membranebound NAC transcription factors were documented as well as their stimulus-dependent nuclear translocation (34)(35)(36)(37). The Cvi FSQ6/ANAC089 protein lacks the membrane anchor because of the premature stop mutation.…”

The Arabidopsis Transcription Factor NAC016 Promotes Drought Stress Responses by Repressing AREB1 Transcription through a Trifurcate Feed-Forward Regulatory Loop Involving NAP

“…However, NAC family members have different C-terminal regions, suggesting that the C-terminal regions may have critical roles in determining the specific cis-elements that they recognize in their respective target genes (Tran et al, 2010). Furthermore, some NAC TFs contain a transmembrane domain (TMD) in the C-terminal region, which may determine their subcellular localization and conditional TF activity (Seo et al, 2008(Seo et al, , 2010.…”

“…Indeed, NTL6-OX plants and ntl4 null mutants exhibit drought tolerance (Kim et al, 2012;Lee and Park, 2012), indicating that the functions of NTL4 and NTL6 counteract each other in drought stress-responsive signaling. Notably, their C-terminal TMDs conditionally regulate the TF activities of these two NTLs; under water deficit conditions, cleavage of their TMDs allows NTL6 and NTL4 to translocate from the cytoplasm to the nucleus (Kim et al, 2010;Lee and Park, 2012).…”

The E3 Ubiquitin Ligase HOS1 Regulates Arabidopsis Flowering by Mediating CONSTANS Degradation Under Cold Stress

“…Recombinant MBP and MBP-HOS1 proteins were synthesized in E. coli Rosetta2 (DE3) pLysS strain (Novagen, Madison, WI) and partially purified as described previously (40). Protein synthesis was induced by adding 0.1 mM isopropyl 1-thio-␤-D-galactopyranoside at 20°C overnight.…”