NPR1, a key immune regulator for plant survival under biotic and abiotic stresses

Abstract

Nonexpressor of pathogenesis-related genes 1 (NPR1) was discovered in Arabidopsis as an activator of salicylic acid (SA)-mediated immune responses nearly 30 years ago. How NPR1 confers resistance against a variety of pathogens and stresses has been extensively studied; however, only in recent years have the underlying molecular mechanisms been uncovered, particularly NPR1's role in SA-mediated transcriptional reprogramming, stress protein homeostasis, and cell survival. Structural analyses ultimately defined NPR1 and its paralogs as SA receptors. The SA-bound NPR1 dimer induces transcription by bridging two TGA transcription factor dimers, forming an enhanceosome. Moreover, NPR1 orchestrates its multiple functions through the formation of distinct nuclear and cytoplasmic biomolecular condensates. Furthermore, NPR1 plays a central role in plant health by regulating the crosstalk between SA and other defense and growth hormones. In this review, we focus on these recent advances and discuss how NPR1 can be utilized to engineer resistance against biotic and abiotic stresses.

Keywords: NPR1; crop protection; disease resistance; plant immunity; plant stress; salicylic acid; systemic acquired resistance.

Figure 1.

Processes regulated by NPR1. A spatial model of the NPR1 dimer structure is shown with domains and cofactors indicated. BTB, BROAD-COMPLEX, TRAMTRACK AND BRIC-À-BRAC; BHB, BACK (BTB and carboxyterminal Kelch) helix bundle; ANK, ankyrin repeat; SBD, SA-binding domain; Zn, Zinc finger.

Figure 2.

Map of mutations in Arabidopsis NPR1 generated through forward and reverse genetic approaches. Top, a spatial model of the partial NPR1 dimer. Bottom, a linear model of the NPR1 monomer. Location of point mutations are mapped onto the spatial model as red-lined yellow dots and detailed on the linear model. Multiple mutations are: dim, dimerization; A-sub, alanine substitution; sim3, SUMO-interacting motif 3; rdr1/2/3, redox-associated disorder region 1/2/3; nls, nuclear localization signal; SAL, SBD-ANK locked. SBC, SA-binding core. Underlined mutations correspond to those identified in Arabidopsis NPR4. Asterisks indicate STOP codon. Red dots on the linear model indicate positions of cysteine residues.

Figure 3.

Activation cycle of NPR1. Left: SA-initiated PTMs of NPR1 and activation of defense transcription. P, phosphorylation; S, SUMOylation; U, ubiquitination. Right: effect of mutations that affect PTMs of NPR1 on plant immunity under basal (mock) and SA-induced conditions. Green plants indicate a lack of immune induction; red plants indicate induced immunity; small red plants indicate autoimmunity with retarded plant growth.

Figure 4.

Different strategies in engineering pathogen-specific and broad-spectrum (with NPR1 as an example) disease resistance in crop plants. In the upper panel, green indicates plants with uninduced immunity and red indicates plants with elevated immunity. In the lower panel, green indicates plants with resistance and yellow indicates plants with disease development. The smaller sized plants indicate fitness penalty as a result of constitutive immunity.