Salicylic Acid Signaling in Plant Innate Immunity

Abstract

Plants are endowed with innate immune system to protect against invading pathogens. The innate immune system serves as a surveillance system against possible attack by viral, bacterial, fungal, and oomycete pathogens. The innate immune system is a sleeping giant to fight against pathogens, and specific signals are needed to activate them. The pathogen’s signature, pathogen-associated molecular pattern (PAMP), switches on the plant innate immune system. The PAMPs are perceived as alarm signals by plant pattern recognition receptors (PRRs), which have a “receptor” and a “signaling domain” in one molecule to perceive and transduce the PAMP signal. Several second messengers are involved in delivering the message generated by the PAMP/PRR signaling complex to plant hormone signals. Salicylic acid (SA) is the important endogenous plant hormone signal in delivering the extracellular PAMP message into the plant cell to initiate the transcription of defense genes. PAMP signaling system generates specific Ca²⁺ signature in the cytosol, which triggers SA biosynthesis. The information encoded in calcium signature is decoded by an array of calmodulins. A calmodulin-binding protein, CBP60g, has been shown to be involved in activating SA biosynthesis. Calcium signature signals transduced to calmodulin-binding protein CBP60g trigger activation of isochorismate synthase in SA biosynthesis pathway. ROS also acts upstream of SA accumulation. H₂O₂ causes an intracellular accumulation of benzoic acid (BA), and the conversion of BA to SA is catalyzed by benzoic acid 2-hydroxylase (BA2H), an inducible enzyme that is synthesized de novo in response to increased BA level. Nitric oxide (NO) activates SA biosynthesis pathway, by inducing phenylalanine ammonia lyase (PAL) which is a key enzyme in biosynthesis of salicylic acid. Several MAP kinase cascades have been shown to act upstream of SA signaling system. SA signaling induces increased expression of transcription factors to activate SA-responsive defense-related genes. NPR1 is a master regulator of the SA-mediated induction of defense genes. NPR1 directly binds SA and binding of SA occurs through Cys^521/529 via the transition metal copper. Nuclear localization of NPR1 protein is essential for its function. In the absence of pathogen challenge, NPR1 is retained in the cytoplasm. Without induction, NPR1 protein forms an oligomer and is excluded from the nucleus. Pathogen/PAMP exposure induces SA accumulation, and the induced SA controls the nuclear translocation of NPR1 through cellular redox changes. In the absence of pathogen challenge, NPR1 is continuously cleared from the nucleus by proteasome, which restricts its co-activator activity to prevent untimely activation of defense responses. Two NPR1 paralogues, NPR3 and NPR4, have been identified as adaptor proteins of the CUL3 E3 ligase, and they target NPR1 degradation in an SA concentration-dependent manner. At increased SA concentration after infection, SA binds to NPR4, and NPR1, freed from NPR4 binding, activates transcription of defense genes. NPR1 is a cofactor of TGA transcription factors, and it enhances binding of TGA transcription factors to the promoter of PR1 gene to activate transcription of PR1 gene. Systemic acquired resistance (SAR) is a salicylic acid-dependent heightened state of defense against a broad spectrum of pathogens activated throughout a plant following a local infection. Methyl salicylate, methyl salicylate esterase, a lipid transfer protein (DIR1), a lipid-derived molecule (glycerol-3-phosphate)-dependent factor, azelaic acid, dehydroabietinal, and pipecolic acid have been suggested to be the systemic mobile signal molecules involved in SAR. Some Mediators have been shown to be involved in triggering SA-mediated SAR. Mediator is a multiprotein complex that functions as a transcriptional coactivator. SAR is associated with priming of defense, and the priming results in a faster and stronger induction of defense mechanisms after pathogen attack. Some dormant MAPKs have been suggested to be important components required for priming. Pipecolic acid is an endogenous mediator of defense priming. SAR involves extensive reprogramming of transcription. SA mediates changes in the expression pattern of about 1,000–2,000 genes. Such a broad effect on gene transcription may be associated with extensive chromatin remodeling. The chromatin remodeling may involve substitution of canonical histones in the octamer by histone variants, in a process known as histone replacement. Chromatin structure is important for the regulation of gene expression, and chromatin states could control cellular memory. The primed genes may be poised for enhanced activation of gene expression by the histone modification in chromatin. There may be a tight correlation between histone modification patterns and gene priming, and also there may be a histone memory for information storage in the plant stress response. NPR1 may be involved in the chromatin modification-induced priming. NPR1 plays important role in inducing high levels of chromatin modification on promoters of the transcription factor genes. Chromatin remodeling may be instrumental for priming of SA-responsive loci to enable their enhanced reactivation upon subsequent pathogen attack. The priming can be inherited epigenetically from disease-exposed plants, and descendants of primed plants exhibit next-generation systemic acquired resistance. The descendants of primed plants showed a faster and higher accumulation of transcripts of defense-related genes in salicylic acid signaling pathway and enhanced disease resistance upon challenge inoculation with virulent pathogens. The transgenerational SAR was found to be sustained over one stress-free generation, indicating an epigenetic basis of the phenomenon. DNA methylation may also play an important role in transgenerational SAR. The transgenerational SAR is transmitted by hypomethylated genes that direct priming of SA-dependent defenses in the following generations.