The mobile SAR signal N-hydroxypipecolic acid induces NPR1-dependent transcriptional reprogramming and immune priming

Abstract

N-Hydroxypipecolic acid (NHP) accumulates in the plant foliage in response to a localized microbial attack and induces systemic acquired resistance (SAR) in distant leaf tissue. Previous studies indicated that pathogen inoculation of Arabidopsis (Arabidopsis thaliana) systemically activates SAR-related transcriptional reprogramming and a primed immune status in strict dependence of FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1), which mediates the endogenous biosynthesis of NHP. Here, we show that elevations of NHP by exogenous treatment are sufficient to induce a SAR-reminiscent transcriptional response that mobilizes key components of immune surveillance and signal transduction. Exogenous NHP primes Arabidopsis wild-type and NHP-deficient fmo1 plants for a boosted induction of pathogen-triggered defenses, such as the biosynthesis of the stress hormone salicylic acid (SA), accumulation of the phytoalexin camalexin and branched-chain amino acids, as well as expression of defense-related genes. NHP also sensitizes the foliage systemically for enhanced SA-inducible gene expression. NHP-triggered SAR, transcriptional reprogramming and defense priming are fortified by SA accumulation and require the function of the transcriptional co-regulator NON-EXPRESSOR OF PR GENES1 (NPR1). Our results suggest that NPR1 transduces NHP-activated immune signaling modes with predominantly SA-dependent and minor SA-independent features. They further support the notion that NHP functions as a mobile immune regulator capable of moving independently of active SA signalling between leaves to systemically activate immune responses.

Transcriptome Responses of Wild Arachis to UV-C Exposure Reveal Genes Involved in General Plant Defense and Priming

“…Likewise, FLA is one of the few candidates downregulated in response to fungus, UV, and drought treatments. FLA encodes a fasciclin-like arabinogalactan protein associated with both structural and signaling function in plant cell walls and, in accordance with our results, was also strongly downregulated during SAR establishment and defense priming [ 57 , 60 ], as well as in response to different distinct multi-stresses conditions [ 55 ]. All these transcriptional alterations in genes involved in cell wall dynamics suggest that biotic and abiotic stresses can trigger wall structure and integrity modifications, which may be determinants in A. stenosperma adaptation to marginal habitats.…”

“…More detailed expression analysis was conducted by qRT-PCR for another 18 A. stenosperma previously associated with priming phase ( Table S2 ), such as genes involved in secondary metabolism (IRL, STS, UGT, BBE, N8DT, and PAL); cell wall structure and integrity (EXLB, EGC, FLA, LAC, and PRP); basal defense pathways (eGCL, NUDT, SYP); or stress signal transduction (LOB, AKT) [ 8 , 19 , 55 , 56 , 57 , 58 , 59 , 60 ]. These candidate genes were selected among the 1460 metaDEGs identified here as commonly regulated by a broad range of primary stresses ( Figure 6 ).…”

Salicylic Acid and Nitric Oxide: Insight Into the Transcriptional Regulation of Their Metabolism and Regulatory Functions in Plants

“…Similarly, Yildiz et al (2021) confirmed that the mobile SAR signal induced by treating Arabidopsis thaliana plants with N-hydroxypipecolic acid (NHP) stimulated NPR1 mediated transcriptional reprogramming of Flavin-dependent Monooxygenase 1 (FMO1) and other downstream genes, thus systematically activating an immune response against pathogenic attack. The role of plant natural product NHP in activating immune response has been identified more recently (Yildiz et al, 2021), which is synthesized directly from pipecolic acid catalyzed by FMO1 in a series of transamination/reduction steps mediated by SARD-4 and AGD2-like defense response protein (ALD1). SA-mediated activation of NPR1 has also been shown to stimulate the ubiquitination of several cytoplasmic proteins by forming SA-induced condensates (SINC).…”

Plant Responses to Biotic Stress: Old Memories Matter

“…It has been observed that NPR1 and SA largely control the function of HDAC19 to impose priming in plants [ 63 ]. In Arabidopsis , after pathogenic ingression, the accumulation of N-hydroxypipecolic acid (NHP) was observed, which served defence priming by inducing SAR in NPR1-dependent manner [ 64 ]. Other HDACs, such as HDA6, are also involved in JA-mediated signalling in WRKY-dependent pathways.…”