Fine-tuning plant defense signaling: Regulation and function of NPR1.

摘要

Plants activate distinct defense responses depending on the lifestyle of the attacker encountered. In these responses salicylic acid (SA) and jasmonic acid (JA) play important signaling roles. SA induces defense against biotrophic pathogens that feed and reproduce on live host cells, whereas JA activates defense against necrotrophic pathogens that kill host cells for nutrition and reproduction. Cross-talk between these defense signaling pathways has been shown to optimize the response against a single attacker. However, its role in defense against multiple pathogens with distinct lifestyles is unknown. Here I show that trade-offs between SA- and JA-dependent defenses against biotrophic and necrotrophic pathogens, respectively, are highly regulated. The cross-talk modulator NPR1 was found to tightly control these trade-offs in a previously unrecognized spatial and pathogen type-specific fashion. This allows plants to prevent unfavorable signal interactions and maximize their ability to concomitantly fend off multiple pathogens.;In addition to modulating SA/JA cross-talk, NPR1 is a central regulator of SA-mediated systemic acquired resistance (SAR) that provides broad-spectrum immunity to pathogens. NPR1 protein is retained in the cytoplasm as an oligomer. Upon infection, SA induces the release of monomer that translocates into the nucleus to regulate defense gene expression. I found that NPR1 monomer is targeted for proteasome-mediated degradation in the nucleus by a Cullin3-RING E3 ligase. Inducers of SAR promote Cullin3-mediated NPR1 degradation by phosphorylation of Ser11/15 residues. Importantly, degradation of NPR1 was required for the activation of NPR1-dependent gene expression and establishment of SAR. Thus, NPR1 protein turnover depicts a novel mode of transcriptional control.;Understanding how regulation and function of NPR1 are coupled is hampered by the lack of knowledge of its protein structure. Therefore, the tertiary and quaternary structures of the N-terminal half of NPR1 were computationally modeled. These models predict novel NPR1 features, including the effect of Ser11/15 phosphorylation on protein conformation and activity, as well as a detailed topology of higher-order oligomer formation.;In summary, the work described here has unveiled previously unrecognized mechanisms of NPR1 regulation and function. In addition, important predictions are presented that may lead to novel discoveries in plant defense signaling in the near future.