Perception of the plant immune signal salicylic acid
Introduction
Salicylic acid (SA) is one of the major plant hormones that regulates various stress responses and development, such as resistance to pathogens, flowering, thermogenesis, senescence, and abiotic stress responses [1, 2]. Among them, the most well studied role of SA is in plant immune response to pathogens. The plant immune system consists of different layers of active defense responses, including MAMP-triggered immunity (MTI), effector-triggered immunity (ETI) and systemic acquired resistance (SAR). Many studies have demonstrated that SA plays a central role in these responses [3, 4]. In 1979, White found that treatment of tobacco with SA, or its derivative aspirin (acetyl-salicylic acid), dramatically enhanced its resistance to tobacco mosaic virus (TMV) [5]. Later studies found that blocking SA accumulation by expressing a bacterial enzyme, salicylate hydroxylase (NahG), compromised both ETI and SAR in tobacco as well as in Arabidopsis [6, 7]. A central question related to SA is how it activates disease resistance. Studies in the past 20 years have greatly improved our understanding of the SA signaling pathway. This review focuses on the mechanisms by which the SA signal is perceived in plants.
Section snippets
Biochemical search for SA-binding proteins
As an immune signal, SA must be able to bind to cellular targets or receptors in order to activate downstream signaling events. This idea led to great efforts in the past 20 years to identify the SA receptor. Klessig and his colleagues found potential SA receptors by isolating SA-binding proteins (SABPs) using biochemical approaches. The first identified SABP was the tobacco catalase with a dissociation constant (Kd) of 14 μM [8, 9, 10]. It was proposed that SA could bind and inhibit catalase,
Genetic screens identified NPR1 as a master regulator of SA-mediated responses
In contrast to the biochemical approaches, several genetic screens for mutants defective in SA responses independently identified the same gene, NPR1 (Nonexpresser of PR genes 1, a.k.a. NIM1, SAI1), as a key regulator of the SA signaling pathway [20, 21, 22, 23, 24, 25]. NPR1, which contains two conserved protein–protein interaction domains: BTB (Bric-a-brac, Tramtrack, Broad-complex) domain and ankryin repeat domain, was found in yeast two-hybrid screens to interact with TGA transcription
Is NPR1 an SA receptor?
NPR1 would be a perfect candidate for being an SA receptor if only it could bind SA. Unfortunately, in the Fu et al. study, no considerable SA-binding activity for Arabidopsis NPR1 was detected using a traditional ligand-binding assay, in which significant binding activities were observed for other NPR proteins [31••]. However, Wu et al. reported that NPR1 could bind SA in an equilibrium dialysis assay [32••]. It was suggested that binding of SA requires copper as a cofactor through two key
The NPR1 homologs NPR3 and NPR4 are SA receptors
The failure to detect SA-binding activity of NPR1 leads to the hypothesis that other components controlling NPR1 may be the SA receptors. Spoel el al. found that proteasome-mediated NPR1 degradation plays dual roles in plant immunity [35]. In the absence of SA or pathogen infection, NPR1 is degraded to prevent spurious activation of defense responses. Upon induction, NPR1 degradation is also required to achieve maximum activation of defense gene expression likely by continuously refreshing the
Are there other SA receptors?
Although NPR1 plays a major role in SA-mediated transcriptional reprogramming, a large body of evidence indicates that there are SA-dependent but NPR1-independent pathways to regulate defense gene expression [40]. For example, in a genetic screen for the suppressors of npr1, SNI1 and SNC1 were identified as negative regulators of defense responses [41, 42]. In the sni1 npr1 and snc1 npr1 double mutants, expression of the SA-mediated defense gene was restored and constitutively activated,
How do plants with high basal level of SA perceive SA signal?
Compare to Arabidopsis, some plants have much higher basal level of SA. For example, rice has two orders of magnitude higher levels of SA than Arabidopsis. The studies in rice suggest that SA is not an effective signal to induce defense gene expression. Rather, SA plays an important role in protecting rice from oxidative damage during pathogen infections [50]. Although the main function of SA is different between rice and Arabidopsis, rice has all the homologs of Arabidopsis NPR1, NPR3 and NPR4
Conclusion and future prospective
SA plays a central role in plant immunity, in which the master regulator NPR1 has the intriguing functions of controlling both cell death and cell survival. The identification of NPR3 and NPR4 as SA receptors is a major step forward in our understanding of the SA signaling pathway [55, 56, 57]. This discovery explains how SA functions through binding with NPR3 and NPR4 to control NPR1 level to determine cell death and survival during pathogen infection. There are many interesting questions
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We would like to thank Drs. Steven Spoel and John Withers for helpful suggestions for this review. This work was funded by grants from NIH (GM069594-05), and Howard Hughes Medical Institute and Gordon and Betty Moore Foundation (through grant GBMF3032) to X.D.
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