Opposite Roles of Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Transcriptional Regulation of Plant Immunity

Abstract

Salicylic acid (SA) is a plant defense hormone required for immunity. Arabidopsis NPR1 and NPR3/NPR4 were previously shown to bind SA and all three proteins were proposed as SA receptors. NPR1 functions as a transcriptional co-activator, whereas NPR3/NPR4 were suggested to function as E3 ligases that promote NPR1 degradation. Here we report that NPR3/NPR4 function as transcriptional co-repressors and SA inhibits their activities to promote the expression of downstream immune regulators. npr4-4D, a gain-of-function npr4 allele that renders NPR4 unable to bind SA, constitutively represses SA-induced immune responses. In contrast, the equivalent mutation in NPR1 abolishes its ability to bind SA and promote SA-induced defense gene expression. Further analysis revealed that NPR3/NPR4 and NPR1 function independently to regulate SA-induced immune responses. Our study indicates that both NPR1 and NPR3/NPR4 are bona fide SA receptors, but play opposite roles in transcriptional regulation of SA-induced defense gene expression.

The potato transcription factor StbZIP61 regulates dynamic biosynthesis of salicylic acid in defense against Phytophthora infestans infection

“…NPR1 was identified as a receptor of SA and is a transcription co‐activator that functions as a master regulator of plant defense (Rochon et al ., ; Wu et al ., ; Pajerowska‐Mukhtar et al ., ; Ding et al ., ). Both NPR3 and NPR4 were also demonstrated as SA receptors (Fu et al ., ; Ding et al ., ), and functioned as transcriptional co‐repressors to negatively regulate defense gene expression (Ding et al ., ). Thus, it was concluded that NPR1 and NPR3/NPR4 play opposite roles in transcriptional regulation of plant immunity (Ding et al ., ).…”

“…Thus, it was concluded that NPR1 and NPR3/NPR4 play opposite roles in transcriptional regulation of plant immunity (Ding et al ., ). Accordingly, genetic analysis demonstrated that mutation of NPR1 results in decreased expression of defense response genes and increased susceptibility to pathogens (Cao et al ., ; Volko et al ., ; Dong, ; Yan and Dong, ), while NPR3 and NPR4 negatively regulate the pathogen resistance and a gain‐of‐function npr4 mutant repressed the immune responses constitutively in Arabidopsis (Zhang et al ., ; Ding et al ., ). Such a negative role of NPR3 was also reported with the TcNPR3 gene from cacao (Shi et al ., ).…”

“…Both NPR3 and NPR4 were also demonstrated as SA receptors (Fu et al ., ; Ding et al ., ), and functioned as transcriptional co‐repressors to negatively regulate defense gene expression (Ding et al ., ). Thus, it was concluded that NPR1 and NPR3/NPR4 play opposite roles in transcriptional regulation of plant immunity (Ding et al ., ). Accordingly, genetic analysis demonstrated that mutation of NPR1 results in decreased expression of defense response genes and increased susceptibility to pathogens (Cao et al ., ; Volko et al ., ; Dong, ; Yan and Dong, ), while NPR3 and NPR4 negatively regulate the pathogen resistance and a gain‐of‐function npr4 mutant repressed the immune responses constitutively in Arabidopsis (Zhang et al ., ; Ding et al ., ).…”

Characterization of NPR1 and NPR4 genes from mulberry (Morus multicaulis) and their roles in development and stress resistance

“…This finding indicated that NPR3 and NPR4 negatively regulate the basal defense response (Zhang et al ). In addition, NPR3 and NPR4 were proposed to act as transcription repressors of key immune genes and negatively regulate plant immunity (Ding et al ). Our results also showed that the ectopic expression of MuNPR4 in Arabidopsis conferred the transgenic plants enhanced susceptibility to Pst .…”

Calcium‐dependent protein kinase 5 links calcium signaling with N‐hydroxy‐l‐pipecolic acid‐ and SARD1‐dependent immune memory in systemic acquired resistance

“…PAD4, in concerted action with a lipase‐like protein, ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), is required for the expression of multiple defense responses in basal defense in PTI and ETI, as well as for ETI‐associated hypersensitive response leading to systemic resistance (Glazebrook et al ., ; Wiermer et al ., ; Rietz et al ., ). SA is perceived by NON‐EXPRESSOR OF PATHOGENESIS‐RELATED GENES 1 (NPR1) as one of three known SA receptors (Fu et al ., ; Wu et al ., ; Yan & Dong, ; Manohar et al ., ; Y. Ding et al ., ). Continuous SA signaling will thus have an impact on changes in histone modification, gene expression, and metabolite production and lead to persistent plant resistance to pathogens.…”