It is well established that salicylic acid (SA) plays a critical role in the transcriptional reprograming that occurs during the plant defense response against biotic and abiotic stress. In the ...course of the defense response, the transcription of different sets of defense genes is controlled in a spatio-temporal manner via SA-mediated mechanisms. Interestingly, different lines of evidence indicate that SA interplays with reactive oxygen species (ROS) and glutathione (GSH) in stressed plants. In this review we focus on the evidence that links SA, ROS, and GSH signals to the transcriptional control of defense genes. We discuss how redox modifications of regulators and co-regulators involved in SA-mediated transcriptional responses control the temporal patterns of gene expression in response to stress. Finally, we examine how these redox sensors are coordinated with the dynamics of cellular redox changes occurring in the defense response to biotic and abiotic stress.
Summary
Salicylic acid (SA) is an important signaling molecule of the plant immune system.
In Arabidopsis thaliana, SA biosynthesis is indirectly modulated by the closely related transcription ...factors TGACG‐BINDING FACTOR 1 and 4 (TGA1 and TGA4, respectively). They activate expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT1, the gene product of which regulates the key SA biosynthesis gene ISOCHORISMATE SYNTHASE 1.
Since TGA1 interacts with the SA receptor NONEXPRESSOR OF PATHOGENESIS‐RELATED GENES 1 (NPR1) in a redox‐dependent manner and since the redox state of TGA1 is altered in SA‐treated plants, TGA1 was assumed to play a role in the NPR1‐dependent signaling cascade. Here, we identified 193 out of 2090 SA‐induced genes that require TGA1/TGA4 for maximal expression after SA treatment. One robustly TGA1/TGA4‐dependent gene encodes for the SA hydroxylase DOWNY MILDEW RESISTANT 6‐LIKE OXYGENASE 1, suggesting an additional regulatory role of TGA1/TGA4 in SA catabolism.
Expression of TGA1/TGA4‐dependent genes in mock/SA‐treated or Pseudomonas‐infected plants was rescued in the tga1 tga4 double mutant after introduction of a mutant genomic TGA1 fragment encoding a TGA1 protein without any cysteines. Thus, the functional significance of the observed redox modification of TGA1 in SA‐treated tissues remains enigmatic.
The jasmonate family of phytohormones plays central roles in plant development and stress acclimation. However, the architecture of their signaling circuits remains largely unknown. Here we describe ...a jasmonate family binding protein, cyclophilin 20-3 (CYP20-3), which regulates stress-responsive cellular redox homeostasis. (+)-12-oxo-phytodienoic acid (OPDA) binding promotes CYP20-3 to form a complex with serine acetyltransferase 1, which triggers the formation of a hetero-oligomeric cysteine synthase complex with O -acetylserine(thiol)lyase B in chloroplasts. The cysteine synthase complex formation then activates sulfur assimilation that leads to increased levels of thiol metabolites and the buildup of cellular reduction potential. The enhanced redox capacity in turn coordinates the expression of a subset of OPDA-responsive genes. Thus, we conclude that CYP20-3 is a key effector protein that links OPDA signaling to amino acid biosynthesis and cellular redox homeostasis in stress responses.
TGA transcription factors are essential regulators of various cellular processes, their activity connected to different hormonal pathways, interacting proteins and regulatory elements. Belonging to ...the basic region leucine zipper (bZIP) family, TGAs operate by binding to their target DNA sequence as dimers through a conserved bZIP domain. Despite sharing the core DNA-binding sequence, the TGA paralogues exert somewhat different DNA-binding preferences. Sequence variability of their N- and C-terminal protein parts indicates their importance in defining TGA functional specificity through interactions with diverse proteins, affecting their DNA-binding properties. In this review, we provide a short and concise summary on plant TGA transcription factors from a structural point of view, including the relation of their structural characteristics to their functional roles in transcription regulation.
SUMMARY
The nonexpressor of pathogenesis‐related (NPR) gene family is well known to play a crucial role in transactivation of TGA transcription factors for salicylic acid (SA)‐responsive genes, ...including pathogenesis‐related protein 1 (PR1), during plants' immune response after pathogen attack in the model dicot Arabidopsis thaliana. However, little is known about NPR gene functions in monocots. We therefore explored the functions of NPRs in SA signaling in the model monocot Brachypodium distachyon. BdNPR1 and BdNPR2/3 share structural similarities with A. thaliana AtNPR1/2 and AtNPR3/4 subfamilies, respectively. The transcript level of BdNPR2 but not BdNPR1/3 appeared to be positively regulated in leaves in response to methyl salicylate. Reporter assays in protoplasts showed that BdNPR2 positively regulated BdTGA1‐mediated activation of PR1. This transactivation occurred in an SA‐dependent manner through SA binding at Arg468 of BdNPR2. In contrast, BdNPR1 functioned as a suppressor of BdNPR2/BdTGA1‐mediated transcription of PR1. Collectively, our findings reveal that the TGA‐promoted transcription of SA‐inducible PR1 is orchestrated by the activator BdNPR2 and the repressor BdNPR1, which function competitively in B. distachyon.
Significance Statement
We present a novel function of Brachypodium distachyon NPR (BdNPR) in the transcriptional machinery for the defensin gene pathogenesis‐related 1 (PR1). We address here the TGA‐activated transcriptional machinery for SA‐inducible PR1 expression, in which BdNPR2 and BdNPR1 work competitively in B. distachyon.
N‐hydroxypipecolic acid (NHP) accumulates in pathogen‐inoculated and distant leaves of the Arabidopsis shoot and induces systemic acquired resistance (SAR) in dependence of the salicylic acid (SA) ...receptor NPR1. We report here that SAR triggered by exogenous NHP treatment requires the function of the transcription factors TGA2/5/6 in addition to NPR1, and is further positively affected by TGA1/4. Consistently, a tga2/5/6 triple knockout mutant is fully impaired in NHP‐induced SAR gene expression, while a tga1/4 double mutant shows an attenuated, partial transcriptional response to NHP. Moreover, tga2/5/6 and tga1/4 exhibited fully and strongly impaired pathogen‐triggered SAR, respectively, while SA‐induced resistance was more moderately compromised in both lines. At the same time, tga2/5/6 was not and tga1/4 only partially impaired in the accumulation of NHP and SA at sites of bacterial attack. Strikingly, SAR gene expression in the systemic tissue induced by local bacterial inoculation or locally applied NHP fully required functional TGA2/5/6 and largely depended on TGA1/4 factors. The systemic accumulation of NHP and SA was attenuated but not abolished in the SAR‐compromised and transcriptionally blocked tga mutants, suggesting their transport from inoculated to systemic tissue. Our results indicate the existence of a critical TGA‐ and NPR1‐dependent transcriptional module that mediates the induction of SAR and systemic defence gene expression by NHP.
Summary statement
N‐hydroxypipecolic acid activates plant systemic acquired resistance (SAR) and SAR gene expression via the transcription factors TGA2/5/6 and the coregulator NPR1. SAR is also promoted by TGA1/4, which mediates expression of a subset of SAR genes and supports the biosynthesis of SAR‐inducing hormones.
Salicylic acid (SA) is a hormone that modulates plant defenses by inducing changes in gene expression. The mechanisms that control SA accumulation are essential for understanding the defensive ...process. TGA transcription factors from clade II in Arabidopsis, which include the proteins TGA2, TGA5, and TGA6, are known to be key positive mediators for the transcription of genes such as PR-1 that are induced by SA application. However, unexpectedly, stress conditions that induce SA accumulation, such as infection with the avirulent pathogen P. syringae DC3000/AvrRPM1 and UV-C irradiation, result in enhanced PR-1 induction in plants lacking the clade II TGAs (tga256 plants). Increased PR-1 induction was accompanied by enhanced isochorismate synthase-dependent SA production as well as the upregulation of several genes involved in the hormone’s accumulation. In response to avirulent P. syringae, PR-1 was previously shown to be controlled by both SA-dependent and -independent pathways. Therefore, the enhanced induction of PR-1 (and other defense genes) and accumulation of SA in the tga256 mutant plants is consistent with the clade II TGA factors providing negative feedback regulation of the SA-dependent and/or -independent pathways. Together, our results indicate that the TGA transcription factors from clade II negatively control SA accumulation under stress conditions that induce the hormone production. Our study describes a mechanism involving old actors playing new roles in regulating SA homeostasis under stress.
Glutaredoxins (GRXs) are small oxidoreductases of the thioredoxin family proteins that can either regulate the thiol redox state of proteins or are linked to iron metabolism because of their ability ...to incorporate iron-sulfur 2Fe–2S clusters. Here we review recent research on a land plant-specific class of GRX-like proteins, which are characterized by the conserved CC motif in the active centre. Loss-of-function mutants of CC-type GRXs in Arabidopsis (also named ROXYs), maize, and rice have unraveled a role in floral development, including regulation of organ primordia initiation, control of organ identity gene expression, and progression into meiosis in the male germ line. Other CC-type GRXs play a role in stress responses, most likely through their capacity to regulate nuclear gene expression. Consistently, CC-type GRXs, physically and genetically interact with individual members of the TGA transcription factor family. One of the challenges in the future is to unravel whether ROXYs control the redox state of TGA factors or other yet unknown target proteins or whether they regulate gene expression through other processes. Other intriguing questions concern the original function of the first CC-type GRXs in basal land plants and their potential contribution to the extremely successful radiation of angiosperms.
Summary
The three closely related Arabidopsis basic leucine zipper (bZIP) transcription factors TGA2, TGA5 and TGA6 are required for the establishment of the salicylic acid (SA)‐dependent plant ...defense response systemic acquired resistance, which is effective against biotrophic pathogens. Here we show that the same transcription factors are essential for the activation of jasmonic acid (JA)‐ and ethylene (ET)‐dependent defense mechanisms that counteract necrotrophic pathogens: the tga256 triple mutant is impaired in JA/ET‐induced PDF1.2 and b‐CHI expression, which correlates with a higher susceptibility against the necrotroph Botrytis cinerea. JA/ET induction of the trans‐activators ERF1 and ORA59, which act upstream of PDF1.2, was slightly increased (ERF1) or unaffected (ORA59). PDF1.2 expression can be restored in the tga256 mutant by increased expression of ORA59, as observed in the tga256 jin1 quadruple mutant, which lacks the transcription factor JIN1/AtMYC2 that functions as a negative regulator of the JA/ET‐dependent anti‐fungal defense program. Whereas JA/ET‐induced PDF1.2 expression is strongly suppressed by SA in wild‐type plants, no negative effect of SA on PDF1.2 expression was observed in the tga256 jin1 quadruple mutant. These results imply that the antagonistic effects of TGA factors and JIN1/AtMYC2 on the JA/ET pathway are necessary to evoke the SA‐mediated suppression of JA/ET‐induced defense responses.
Summary
Salicylic acid (SA) is a plant signaling molecule that mediates the induction of defense responses upon attack by a variety of pathogens. Moreover, it antagonizes gene induction by the stress ...signaling molecule jasmonic acid (JA). Several SA‐responsive genes are regulated by basic/leucine zipper‐type transcription factors of the TGA family. TGA factors interact with NPR1, a central regulator of many SA‐induced defense responses including SA/JA antagonism. In order to identify further regulatory proteins of SA‐dependent signaling pathways, a yeast protein interaction screen with tobacco TGA2.2 as bait and an Arabidopsis thaliana cDNA prey library was performed and led to the identification of a member of the glutaredoxin family (GRX480, encoded by At1g28480). Glutaredoxins are candidates for mediating redox regulation of proteins because of their capacity to catalyze disulfide transitions. This agrees with previous findings that the redox state of both TGA1 and NPR1 changes under inducing conditions. Transgenic Arabidopsis plants ectopically expressing GRX480 show near wild‐type expression of standard marker genes for SA‐ and xenobiotic‐inducible responses. In contrast, transcription of the JA‐dependent defensin gene PDF1.2 was antagonized by transgenic GRX480. This, together with the observation that GRX480 transcription is SA‐inducible and requires NPR1, suggests a role of GRX480 in SA/JA cross‐talk. Suppression of PDF1.2 by GRX480 depends on the presence of TGA factors, indicating that the GRX480/TGA interaction is effective in planta.
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