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Signal regulators of systemic acquired resistance

Qing-Ming Gao, Shifeng Zhu, Pradeep Kachroo and 1 more

Frontiers in Plant Science · 2015

doi:10.3389/fpls.2015.00228

Abstract

Salicylic acid (SA) is an important phytohormone that plays a vital role in a number of physiological responses, including plant defense. The last two decades have witnessed a number of breakthroughs related to biosynthesis, transport, perception and signaling mediated by SA. These findings demonstrate that SA plays a crictical role in both local and systemic defense responses. Systemic acquired resistance (SAR) is one such SA-dependent response. SAR is a long distance signaling mechanism that provides broad spectrum and long-lasting resistance to secondary infections throughout the plant. This unique feature makes SAR a highly desirable trait in crop production. This review summarizes the recent advances in the role of SA in SAR and discusses its relationship to other SAR inducers.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 21, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Plants being sessile are constantly exposed to a number of pathogenic microbes, which based on their infectious lifestyles can be broadly divided into biotrophs and necrotrophs. Biotrophic pathogens rely on nutrients from living host cells, whereas necrotrophic pathogens feed on dead cells. Plants employ distinct immune responses to counter these pathogens and this aspect has been covered in detail in several recent reviews. This first layer of host defense involves the recognition of pathogen (or microbe) associated-molecular patterns (PAMPs/MAMPs), such as bacterial flagellin, lipopolysaccharides, and peptidoglycans. PAMPs are recognized by specialized transmembrane proteins in the plant, termed pattern recognition receptors (PPRs). PRR-mediated recognition of PAMPs triggers downstream signaling leading to the activation of basal resistance termed PAMP-triggered immunity (PTI; ). PTI can be suppressed by pathogen encoded effector proteins commonly known as avirulence (avr) factors. The avr factors are in turn recognized by the host encoded resistance (R) proteins, which confer more durable and robust resistance termed R gene- or effector-triggered immunity (ETI;;,;;;; ). ETI is generally associated with programmed cell death (PCD) at the site of infection and this phenomenon is called hypersensitive response (HR;;; ).

Induction of local responses is associated with the transport of defense signals throughout the plant resulting in broad-spectrum disease resistance against secondary infections. This phenomenon, known as systemic acquired resistance (SAR), is conserved among diverse plants and confers long-lasting resistance to unrelated pathogens. Several studies have shown that the establishment of SAR involves the generation and transport of signals via phloem to the uninfected distal tissues. Among the signals contributing to SAR are salicylic acid (SA) and several components of the SA pathway including the methylated derivative of SA (methyl SA,MeSA, ). Additionally, the diterpenoid dehydroabietinal (DA, ), the nine carbon (C9) dicarboxylic acid azelaic acid (AzA, ), an amino acid derivative pipecolic acid (Pip; ), auxin, the phosphorylated sugar glycerol-3-phosphate (G3P,;; ), the free radicals nitric oxide (NO) and reactive oxygen species (ROS;; ), galactolipids, factors contributing to cuticle formation and the lipid transfer proteins (LTPs) DIR1 (Defective in Induced Resistance, ) and AZI1 (AzA insensitive, ), have all been proposed to serve as SAR signals. Here, we review the role of SA in SAR and discuss its relationship to these various SAR signals.

SA Biosysnthesis and SAR

Salicylic acid biosynthesis occurs via the shikimic acid pathway, which forms two distinct sub-branches both of which synthesize SA. These branched pathways, designated as isochorismate synthase (ICS)- and the phenylalanine ammonia-lyase (PAL)-derived pathways, utilize chorismate as the common precursor (;;;;;;;; Figure 1). The first step of the PAL pathway involves conversion of phenylalanine (Phe) to trans-cinnamic acid and this reaction is catalyzed by PAL, a key enzyme of this pathway that is induced by pathogen infection. The Arabidopsis genome encodes four PAL isoforms and PAL quadruple mutants or wild-type plants treated with the PAL inhibitor, 2-aminoindan-2-phosphonic acid contain reduced SA, show increased susceptibility to pathogens and are unable to induce SAR. Although relative contributions of PAL versus ICS branches toward SA biosynthesis vary between different plant species, at least in Arabidopsis majority of the pathogen-induced SA appears to be derived from the ICS branch. The ICS branch involves conversion of chorismate to isochorismate by ICS followed by coversion of isochorismate to SA by isochorismate pyruvate lyase (IPL). The Arabidopsis genome encodes two isoforms of ICS, of which ICS1 (SID2) accounts for ∼95% of basal- or pathogen-induced SA. A mutation in ICS1 also impairs SAR, suggesting that SA contributed by both PAL- and ICS-pathways is critical for the induction and/or establishment of SAR. This together with the compromised SAR phenotype of transgenic plants expressing bacterial salicylate hydroxylase (NahG; ), an enzyme that catalyzes the conversion of SA to catechol, reemphasize the importance of SA in SAR. It is unclear what factors govern the specific recruitment of the PAL or ICS pathways for SA biosynthesis.

Salicylic acid synthesized in the chloroplasts is exported out to the cytosol via EDS5, a member of the MATE (Multidrug and Toxin Extrusion) transporter family, located in the chloroplast envelope. Notably, a mutation in EDS5 results in complete shut down of SA biosynthesis rather than SA accumulation within the chloroplasts. Thus, mutations in ICS1 and EDS5 similarly affect SA levels and the corresponding mutants thereby exhibit overlapping defense defects. This is likely due to negative feed-back regulation of ICS1 by SA. The triphosphate tunnel metalloenzyme 2 is a negative regulator of the SA feed-back loop and functions in defense signal amplification. Pathogen induced expression of ICS1 requires the binding of calmodulin binding protein CBP60g and its homolog, non-calmodulin binding SARD1 (SAR Deficient 1) to the ICS1 promoter. CBP60g and SARD1 specifically bind the GAAATTTTGG sequence in the ICS1 promoter. The induction of ICS1 and thereby SA biosynthesis is inhibited in cbp60g sard1 double mutant, resulting in compromised SAR.

Although a number of studies have demonstrated the critical requirement of SA in SAR, a specific requirement for SA accumulation beyond basal levels during SAR has not been established. For instance, plants lacking a functional R protein RPS2 accumulate normal levels of SA in their distal tissues in response to infection by Pseudomonas syringae pv. tomato expressing avrRpt2, yet these plants are compromised for SAR. Additionally, exogenous application of either G3P or AzA, which induce SAR in wild-type plants, do not induce SA accumulation. However, neither G3P nor AzA can confer SAR in ics1 (sid2) mutant plants, which contain significantly reduced basal- and pathogen-induced SA. Thus, although SA is clearly critical for SAR, accumulation of SA alone is insufficient to establish SAR. Furthermore, although SA has been shown to accumulate to varying levels in the distal tissues of SAR induced plants (Table 1), there is no evidence suggesting that this accumulation is essential for SAR.

In comparison to local tissues, the distal tissues of SAR-induced plants have been shown to accumulate a broad range of SA ranging from as low as 10 ng/ g FW to ∼2.6 μg/g FW (Table 1;;;;;;;;;;;;,;;; ). The inability to accumulate SA in distal tissues has also been suggested to contribute to impaired SAR in ald1 (agd2-Like Defense response protein 1) and fmo1 (Flavin Monooxygenase 1) mutants, both of which accumulate normal SA in the local tissue. ALD1 encodes an aminotransferase that catalyzes the biosynthesis of the SAR inducer Pip, and FMO1 has been suggested to function downstream of Pip. Thus, other factors besides SA might contribute to the SAR defect of ald1 and fmo1 mutants. One possibility is that SAR can be induced via SA-independent factors so long as a minimum basal level of SA can be maintained. Alternatively, SA accumulation in distal tissues might contribute to the priming process resulting in the activation of stronger defense responses upon secondary infections.

SA-Derivatives and SAR

A majority of the synthesized SA is converted and stored as biologically inactive derivatives via glucosylation, methylation and amino acid conjugation since accumulation of the acidic SA has adverse physiological consequences. These include SA 2-O-β-D-glucose (SAG), SA glucose ester (SGE), methyl SA (MeSA), and SA-amino acid conjugates. Most recently, SA was shown to be derivatized to 2,3-dihydroxybenzoic acid (2,3-DHBA) and this reaction is catalyzed by SA 3-hydroxylase (S3H; ). As predicted s3h knockout plants contain very high levels of SA, while plants expressing S3H gain-of-function mutations accumulate high amounts of 2,3-DHBA. SA derivatives serve as storage forms that can be converted back to free SA. With the exception of MeSA however, the exact role of SA derivatives in SAR remains unclear.

Methyl SA is a volatile and phloem mobile SA derivative, which accumulates in infected and distal tissues in response to pathogen infection. Like MeSA, SA also accumulates in the phloem of tobacco leaves infected with tobacco mosaic virus or Colletotrichum lagenarium and in cucumber leaves infected with tobacco necrosis virus. For SAR, MeSA must be converted to SA in the distal tissues between the 48–72 h period post primary infection. This time-frame correlates with that of pathogen-inducible MeSA accumulation in infected and systemic tissues. The biosynthesis of MeSA is catalyzed by SA methyltransferases (SAMT/BSMT), and the conversion of MeSA back to SA is mediated by methyl esterase (MES;;; ). The tobacco MES was first identified based on its ability to bind SA, and therefore designated as SA-binding protein 2 (SABP2; ). Grafting studies in tobacco plants silenced for SABP2 have shown that SABP2 activity in scions, but not root-stocks is required for normal SAR. Furthermore, the synthetic SA analog, 2,2,2,2′-tetra-fluoroacetophenone, which inhibits the esterase activity of SABP2, also inhibits SAR. As in tobacco, homologs of SABP2 (AtMES9) and SAMT AtBSMT1 are required for SAR in Arabidopsis. Thus, the ability to derivatize SA to MeSA and reconvert MeSA back to SA are critical for SAR. Intriguingly, the requirement for AtBSMT1 in SAR can be bypassed by prolonged exposure to light after pathogen inoculation. However, the role of light signaling in SAR and how it might compensate for MeSA is unclear. It is also not known whether MeSA merely functions to deliver SA to the distal tissues or has other function(s) in SAR. Notably, a certain percentage of SA is always transported from the inoculated to distal tissues. The biological significance of this transport is unclear, particularly in view of the fact that SA is not considered to be the mobile SAR signal since wild-type tobacco scions grafted onto NahG root-stocks exhibit normal SAR.

Regulation of SA Accumulation and SAR

Besides proteins that directly contribute to SA biosynthesis (ICS and PAL) or transport (EDS5), a number of other proteins have been identified that participate in pathogen induced SA accumulation and thereby SAR. These include EDS1 (Enhanced Disease Susceptibility 1), PAD4 (Phytoalexin Deficient 4), and NDR1 (Non-race-specific Disease Resistance 1;,;;;;;;;;;;; ). Unlike ICS1 and EDS5, mutations in EDS1, PAD4, or NDR1 cause partial reduction in SA levels. EDS1 and PAD4 are lipase-like proteins, which together with another lipase-like protein SAG101 (Senescence Associate Gene 101) form binary and ternary complexes. EDS1 interacts with PAD4 in both cytosol and nucleus, and with SAG101 only in the nucleus. EDS1, PAD4, and SAG101 function cooperatively as well as independently in pathogen defense. For instance, all three proteins are required for R-mediated resistance against Turnip crinkle virus (TCV) but only PAD4 is required for the SA-mediated induction of the R gene which confers HR against TCV (HRT;,, ). Interestingly, EDS1, but not PAD4 or SAG101, interacts with HRT and potentiates HRT-mediated HR to TCV. Similarly, only PAD4 is required for resistance to the green peach aphid, whereas EDS1 and SAG101 are not. Both nuclear and extranuclear localization of EDS1 is important for its defense function. However, the role of binary or ternary complex formation between EDS1, PAD4, and SAG101 proteins remains unknown. EDS1 was recently shown to participate in both SAR signal generation in the local tissues as well as perception in the distal leaves.

The Arabidopsis genome encodes two isoforms of EDS1 that function redundantly and can compensate for each other. However, some Arabidopsis ecotypes, such as Wassilewskija, Landsberg, and Dujon, contain only one functional EDS1 isoform, and this is sufficient for normal resistance in these ecotypes. Like Arabidopsis, soybean also contains two EDS1 isoforms. Interestingly, Arabidopsis eds1 mutant expressing the soybean EDS1 orthologs is only partially restored in SA levels, but completely restored in bacterial resistance. This further questions the requirement for increased SA accumulation during defense activation and raises the possibility that a certain threshold of SA may be sufficient to induce appropriate defense responses. The soybean EDS1 orthologs are unable to potentiate TCV coat protein-derived activation of HRT even though they do interact with HRT. This suggests that EDS1 orthologs in different plants may have evolved to perform overlapping as well as distinct functions.

SA Signaling Components

Salicylic acid-mediated signaling leading to SAR is dependent on the ankyrin repeat containing protein NPR1 [Non-expressor of Pathogenesis-Related (PR) genes]. Under basal or uninduced conditions, NPR1 exists as a cytosolic inactive oligomer formed by intermolecular disulfide bonding. Reducing conditions resulting from accumulation of SA cause dissociation of the NPR1 oligomer into active monomers and the monomeric form of NPR1 is translocated into the nucleus. Nuclear localization of NPR1 facilitates its interaction with members of the TGACG motif binding (TGA) transcription factors that belong to the basic leucine zipper (bZIP) protein family. This in turn enhances binding of the TGA factors to promoter elements of NPR1-dependent target genes. Like NPR1, TGA factors are also required for SAR; the tga2 tga5 tga6 triple mutant is non-responsive to SA and is defective in SAR. Recent studies have shown that NPR1 and TGA1 also undergo S-nitrosylation, which is necessary for the proper functioning of NPR1 in immunity and increases the DNA binding activity of TGA1. On the other hand, thiol S-nitrosylation has also been shown to promote NPR1 oligomerization and thereby its inactivation. The nuclear NPR1 is phosphorylated and degraded in a proteasome-dependent manner, and the turnover of NPR1 is essential for SAR establishment. The Arabidopsis genome contains five paralogs of NPR1. Like NPR1, NPR3, and NPR4 also interact with TGA proteins. The npr3 npr4 mutant plants accumulate elevated levels of NPR1 and are consequently defective in SAR. NPR3 and NPR4 bind SA and function as adaptors of the Cullin 3 ubiquitin E3 ligase to mediate NPR1 degradation in an SA-dependent manner. However, the two differ in that NPR3 has higher affinity for SA than NPR4, and SA promotes the NPR1–NPR3 interaction but inhibits the NPR1–NPR4 interaction. These contrasting effects might offer a possible explanation for the nuances underlying NPR1-dependent immunity under different levels of SA. For instance, high concentration of SA in infected tissues might favor binding of NPR3 with SA, which would mediate degradation of the cell-death suppressor NPR1, and initiate PCD and local immunity. On the other hand, lower SA levels in the distal uninfected tissue would minimize NPR3-SA binding, thereby inhibiting PCD. Interestingly, in yet another study, NPR1 was also shown to bind SA via the transition metal copper. The binding of SA to NPR was suggested to induce a conformational change in NPR1, which in turn is important for NPR1-dependant PR1 expression.

NPR1 is also required for transgenerational SAR, which in turn involves epigenetic changes. NPR1 othologs have been characterized from a number of plants including rice, tobacco, soybean, and cacao. Transgenic expression of Arabidopsis NPR1 confers enhanced resistance in heterologous plants. Conversely, transgenic expression of soybean orthologs can complement the Arabidopsis npr1 mutation. Overexpression of NPR1 also enhances pathogen resistance in monocots. However, studies in rice and barley suggest that NPR1 function may not be fully conserved in monocots and dicots and that SA signaling and SAR in monocots might involve NPR1-independent pathways. Transcription analysis in distal tissues revealed that bacteria-triggered SAR in barley was likely associated with jasmonic acid, ethylene and ABA, rather than SA. In contrast, SAR in maize is associated with SA accumulation in local and distal leaves. Additionally, petiole exudates from pathogen infected Arabidopsis plants induced SAR in wheat. This suggests that SAR signaling in barley may not be similar to that in other monocots like maize and wheat.

The stability of NPR1 is dependent on Mediator (MED) 16 [allelic to Sensitive to Freezing (SFR) 6], a subunit of the MED complex which functions as a bridge between transcription factors and the general RNA polymerase II transcriptional machinery. A mutation in MED16 compromises SAR and SA-induced defense responses but does not affect SA levels or nuclear localization of NPR1. Thus, MED16 likely functions downstream of SA in the SAR pathway. Interestingly, MED16 is also required for jasmonic acid/ethylene-responsive gene expression and resistance to necrotrophic pathogens. Thus, MED16 might function by relaying signals from transcription factors that are specific to the SA and JA/ethylene pathways. A mutation in another MED subunit, MED 15 (isolated in a screen for non-recognition-of-the SA analog, BTH, nrb4), also attenuates SAR and SA responsiveness. However, MED15 is not required for NPR1 stability or localization and likely functions downstream of NPR1.

SA versus Other SAR Inducers

Systemic acquired resistance is a complex phenomenon that involves the interplay of a diverse group of chemicals and associated proteins, besides SA. Most of these molecules can now be placed in one of two main branches that comprise the SAR pathway. One branch involves SA and its signaling component NPR1, and the other branch involves the free radicals NO and ROS, which function directly upstream of AzA, which in turn is upstream of G3P. Unlike G3P and AzA, exogenous application of Pip or DA induces SA accumulation in the absence of pathogen infection. Therefore, Pip and DA likely function in the SA branch of SAR. The presence of two SAR branches is supported by the fact that SA cannot restore SAR in mutants defective in NO, ROS, or G3P biosynthesis, while NO/ROS cannot confer SAR on mutants defective in SA synthesis or signaling. Furthermore, pharmacological inhibitors of NO synthesis or NO scavengers attenuate SA-induced SAR in tobacco. Interestingly, unlike SA, both NO and ROS function in a concentration dependent manner because they can confer SAR only when present at an optimal concentration. Free radicals are well known to operate similarly in animal systems where too little or too much can produce opposing physiological effects. Free radicals are thought to participate in SAR by mediating the oxidation of carbon (C) 18 unsaturated fatty acids (FAs) containing a double bond on C 9. This results in the formation of 9-oxo nonanoic acid (ONA), which is converted to the di-carboxylic acid AzA by the addition of a carboxylic group. AzA is unable to confer SAR on mutants unable to synthesize G3P, indicating it functions upstream of G3P. Exogenous AzA increases the expression of the G3P synthesizing GLY1 and GLI1 genes, which encode G3P dehydrogenase and glycerol kinase, respectively. G3P operates in a feedback loop with the LTPs DIR1 and AZI1 such that lack of DIR1 or AZI1 impairs pathogen-induced G3P accumulation while lack of G3P results in reduced DIR1 and AZI1 transcripts. DIR1 and AZI1 form homo- and hetromers suggesting that a complex comprising these proteins might function in SAR. Perhaps such a complex or the individual LTPs serve in transporting SAR essential signal(s) to the distal tissues. G3P appears to be the logical choice for such a transported signal since it is a precursor for lipid biogenesis. However, no direct interaction could be detected between G3P and DIR1 raising the possibility that G3P may be derivatized and this derivative may then be transported from infected to distal tissues. Radiolabel feeding experiments showed that G3P is indeed converted to an as yet unidentified derivative which can translocate from infected to distal tissues in a DIR1-dependent manner.

Recent studies have shown that the C 18 FAs which serve as precusors for AzA are derived from the major plastidal lipids, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), which comprise ∼80% of the total lipids in plants. Thus, besides SA, NO, ROS and G3P, chloroplasts also serve as an important site for AzA biosynthesis. Notably, both galactose sugars in DGDG appear to be important for SAR since dgd1 plants producing α-glucose-β-galactose diacylglycerol via transgenic expression of a bacterial glucosyltransferase, are not restored in SAR even though they are partially restored in chloroplast function. Thus it appears that the position of the hydroxyl group on C 4 of galactose may be important for SAR since glucose and galactose are sterioisomeric sugars which differ only in the position of their axial hydroxyl group at C 4.

Cross Talk between SA and NO Pathways in SAR

Monogalactosyldiacylglycerol and DGDG galactolipids also serve additional functions in SAR. For instance, DGDG is required for SA and NO biosynthesis and for AzA responsiveness. Interestingly, in spite of their impaired SA and NO synthesis, petiole exudates from pathogen-infected dgd1 plants were able to confer SAR in wild-type plants. This suggests that dgd1 plants can make signals that are capable of inducing SA- and NO-synthesis in plants with normal DGDG levels. These results show that SAR involves DGDG-dependent retrograde signaling between the chloroplast and nucleus and emphasizes the fact that the two branches of SAR are intricately linked.

In fact it is well known that there is cross talk between SA- and NO-mediated signaling. For example, NO mediated S-nitrosylation of NPR1 can result in the oligomerization and nuclear localization of NPR1. Moreover, SA has been suggested to regulate chloroplast structure since exogenous SA can cause swelling of grana thylakoids, coagulation of the stroma and increased chloroplast volume. Regulation of SA and AzA levels by EDS1 is another case in point. Together, these results suggest that the parallel operation of the interlinked SA- and NO-pathways might allow multiple points of regulation in fine tuning the optimal onset of SAR. This may be particularly relevant for signals like NO and ROS, which are functional within specific concentration ranges.

Conclusion and Perspectives

Recent work on SAR has identified a number of chemical and protein signals and placed them in a common pathway that comprises at least two parallel branches (Figure 2). However, these studies also indicate the involvement of additional unknown signal(s) that function upstream of the branchpoint separating SA-NPR1- and NO-ROS-AzA-G3P-derived pathways. In addition, several chemical signals, including G3P and AzA, undergo derivatization into unknown compounds and at least one of the G3P-derivative is SAR bioactive (unpublished data). Identification of these signals should provide useful insights into signaling events leading to the induction and establishment of SAR. Another area of SAR research that has not received much attention is the transport and perception of signals in the distal tissues. Although cuticle was implicated in the perception of SAR signals, later studies on cuticle mutants have suggested that perception might relate to the severity of cuticular damage or perhaps other unknown factors. These aspects of SAR should provide exciting avenues for studying how SAR overlaps with basic physiological processes and the distinct events that decide the onset of SAR versus normal growth and development.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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    Fan W. Dong X. (2002 ). In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14 1377–1389

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    Kim H. S. Delaney T. P. (2002 ). Over-expression of TGA5 which encodes a bZIP transcription factor that interacts with NIM1/NPR1 confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J. 32 151–163

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    Kinkema M. Fan W. Dong X. (2000 ). Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12 2339–2350

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    Lucas W. J. Groover A. Lichtenberger R. Furuta K. Yadav S. R. Helariutta Y. (2013 ). The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 55 294–388

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    Marrtin F. Kamoun S. (2012 ). Effectors in Plant-microbe Interactions. Chichester; Ames, IA: Wiley-Blackwell.

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    McDowell J. M. Cuzick A. Can C. Beynon J. Dangl J. L. Holub E. B. (2000 ). Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1 EDS1 NPR1 and salicylic acid accumulation. Plant J. 22 523–529

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    Mishina T. E. Zeier J. (2006 ). The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141 1666–1675

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    Morel J. B. Dangl J. L. (1997 ). The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4 671–683

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    Narusaka M. Shirasu K. Noutoshi Y. Kubo Y. Shiraishi T. Iwabuchi M. (2009 ). RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60 218–226

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    Niggeweg R. Thurow C. Kegler C. Gatz C. (2000 ). Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters. J. Biol. Chem. 275 19897–19905

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    Pallas J. A. Paiva N. L. Lamb C. Dixon R. A. (1996 ). Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 10 281–293

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    Park S. W. Kaiyomo E. Kumar D. Mosher S. L. Klessig D. F. (2007 ). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318 113–116

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    Pegadaraju V. Louis J. Singh V. Reese J. C. Bautor J. Feys B. J. (2007 ). Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid1. Plant J. 52 332–341

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    Pierpoint W. S. (1994 ). Salicylic acid and its derivatives in plants: medicines, metabolites and messenger molecules. Bot. Res. 20 163–235

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    Rasmussen J. B. Hammerschmidt R. Zook M. N. (1991 ). Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97 1342–1347

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    Rietz S. Stamm A. Malonek S. Wagner S. Becker D. Medina-Escobar N. (2011 ). Different roles of enhanced disease susceptibility1 (EDS1) bound to and dissociated from phytoalexin deficient4 (PAD4) in Arabidopsis immunity. New Phytol. 191 107–119

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    Rivas-San Vicente M. Plasencia J. (2011 ). Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62 3321–3338

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    Sandhu D. Tasma I. M. Frasch R. Bhattacharyya M. K. (2009 ). Systemic acquired resistance in soybean is regulated by two proteins, Orthologous to Arabidopsis NPR1. BMC Plant Biol. 9:105

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    Schwessinger B. Ronald P. C. (2012 ). Plant innate immunity: perception of conserved microbial signatures. Annu. Rev. Plant Biol. 63 451–482

    Not in our library10.1146/annurev-arplant-042811-105518

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    Serrano M. Wang B. Aryal B. Garcion C. Abou-Mansour E. Heck S. (2013 ). Export of salicylic acid from the chloroplast requires the MATE-like transporter EDS5. Plant Physiol. 162 1815–1821

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    Shi Z. Maximova S. N. Liu Y. Verica J. Guiltinan M. J. (2010 ). Functional analysis of the Theobroma cacao NPR1 gene in Arabidopsis. BMC Plant Biol. 10:248

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    Shimono M. Sugano S. Nakayama A. Jiang C. J. Ono K. Toki S. (2007 ). Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19 2064–2076

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    Activity of Nitric Oxide Is Dependent On, But Is Partially Required for Function of, Salicylic Acid in the Signaling Pathway in Tobacco Systemic Acquired Resistance · 2001
    Not checked
  134. 134.

    Song J. T. Lu H. McDowell J. M. Greenberg J. T. (2004a ). A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 40 200–212

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    Not in our library10.1105/tpc.019372

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    Spoel S. Dong X. (2012 ). How do plants achieve immunity? Defence withoug specialized immune cells. Nat. Rev. Immunol. 12 89–100

    Not in our library10.1038/nri3141

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    Spoel S. H. Mou Z. Tada Y. Spivey N. W. Genschik P. Dong X. (2009 ). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual role in regulating plant immunity. Cell 137 860–872

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    Strawn M. A. Marr S. K. Inoue K. Inada N. Zubieta C. Wildermuth M. C. (2007 ). Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J. Biol. Chem. 282 5919–5933

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    Tada Y. Spoel S. H. Pajerowska-Mukhtar K. Mou Z. Song J. Wang C. (2008 ). Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321 952–956

    Not in our library10.1126/science.1156970

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    Truman W. Glazebrook J. (2012 ). Co-expression analysis identifies putative targets for CBP60g and SARD1 regulation. BMC Plant Biol. 12:216

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    Ung H. Moeder W. Yoshioka K. (2014 ). Arabidopsis triphosphate tunnel metalloenzyme2 is a negative regulator of the salicylic acid-mediated feedback amplification loop for defense responses. Plant Physiol. 166 1009–1021

    Not in our library10.1104/pp.114.248757

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    Uzunova A. N. Popova L. P. (2000 ). Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica 38 243–250

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    Enhanced Disease Susceptibility 1 and Salicylic Acid Act Redundantly to Regulate Resistance Gene-Mediated Signaling · 2009
    No notice
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    Not in our library10.1105/tpc.6.7.959

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    Wang C. El-Shetehy M. Shine M. B. Yu K. Navarre D. Wendehenne D. (2014a ). Free radicals mediate systemic acquired resistance. Cell Rep. 7 348–355

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    Not in our library10.1093/jxb/eru331

  157. 157.

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    Not in our library10.1007/s12374-010-9130-y

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    A Feedback Regulatory Loop between G3P and Lipid Transfer Proteins DIR1 and AZI1 Mediates Azelaic-Acid-Induced Systemic Immunity · 2013
    Not checked
  165. 165.

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    Zhang K. Halitschke R. Yin C. Liu C. J. Gan S. S. (2013 ). Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc. Natl. Acad. Sci. U.S.A. 110 14807–14812

    Not in our library10.1073/pnas.1302702110

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    Zhang X. Wang C. Zhang Y. Sun Y. Mou Z. (2012 ). The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24 4294–4309

    Not in our library10.1105/tpc.112.103317

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    Not in our library10.1111/j.1365-313x.2006.02903.x

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    Zhang Y. Fan W. Kinkema M. Li X. Dong X. (1999 ). Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. U.S.A. 96 6523–6528

    Not in our library10.1073/pnas.96.11.6523

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    Zhang Y. Tessaro M. J. Lassner M. Li X. (2003 ). Knockout analysis of Arabidopsis transcription factors TGA2 TGA5 and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15 2647–2653

    Not in our library10.1105/tpc.014894

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    Zhang Y. Xu S. Ding P. Wang D. Cheng Y. T. He J. (2010 ). Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. U.S.A. 107 18220–18225

    Not in our library10.1073/pnas.1005225107

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    Zhou J. M. Trifa Y. Silva H. Pontier D. Lam E. Shah J. (2000 ). NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant Microbe Interact. 13 191–202

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  173. 173.
    SAG101 Forms a Ternary Complex with EDS1 and PAD4 and Is Required for Resistance Signaling against Turnip Crinkle Virus · 2011
    No notice
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    Zoeller M. Stingl N. Krischke M. Fekete A. Waller F. Berger S. (2012 ). Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol. 160 365–378

    Not in our library10.1104/pp.112.202846

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    Zwicker S. Mast S. Stos V. Pfitzner A. J. Pfitzner U. M. (2007 ). Tobacco NIMIN2 proteins control PR gene induction through transient repression early in systemic acquired resistance. Mol. Plant Pathol. 4 385–400

    Not in our library10.1111/j.1364-3703.2007.00399.x

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