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How salicylic acid takes transcriptional control over jasmonic acid signaling.

Caarls L, Pieterse CM, Van Wees SC - Front Plant Sci (2015)

Bottom Line: Additionally, SA can induce negative regulators, among which WRKY transcription factors, that can directly or indirectly inhibit JA-responsive gene expression.Finally, at the DNA level, modification of histones by SA-dependent factors can result in repression of JA-responsive genes.These diverse and complex regulatory mechanisms affect important signaling hubs in the integration of hormone signaling networks.

View Article: PubMed Central - PubMed

Affiliation: Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University Utrecht, Netherlands.

ABSTRACT
Transcriptional regulation is a central process in plant immunity. The induction or repression of defense genes is orchestrated by signaling networks that are directed by plant hormones of which salicylic acid (SA) and jasmonic acid (JA) are the major players. Extensive cross-communication between the hormone signaling pathways allows for fine tuning of transcriptional programs, determining resistance to invaders and trade-offs with plant development. Here, we give an overview of how SA can control transcriptional reprogramming of JA-induced genes in Arabidopsis thaliana. SA can influence activity and/or localization of transcriptional regulators by post-translational modifications of transcription factors and co-regulators. SA-induced redox changes, mediated by thioredoxins and glutaredoxins, modify transcriptional regulators that are involved in suppression of JA-dependent genes, such as NPR1 and TGA transcription factors, which affects their localization or DNA binding activity. Furthermore, SA can mediate sequestering of JA-responsive transcription factors away from their target genes by stalling them in the cytosol or in complexes with repressor proteins in the nucleus. SA also affects JA-induced transcription by inducing degradation of transcription factors with an activating role in JA signaling, as was shown for the ERF transcription factor ORA59. Additionally, SA can induce negative regulators, among which WRKY transcription factors, that can directly or indirectly inhibit JA-responsive gene expression. Finally, at the DNA level, modification of histones by SA-dependent factors can result in repression of JA-responsive genes. These diverse and complex regulatory mechanisms affect important signaling hubs in the integration of hormone signaling networks. Some pathogens have evolved effectors that highjack hormone crosstalk mechanisms for their own good, which are described in this review as well.

No MeSH data available.


Related in: MedlinePlus

Simplified model of the molecular machinery involved in the transcriptional regulation of the SA signaling pathway (A), the JA signaling pathway (B), or the antagonism of SA on the JA signaling pathway (C). By inducing reduction and monomerization of NPR1, SA activates NPR1 (star-shaped), which then triggers gene expression in the nucleus. JA-responsive genes are kept in check by JAZ repressors in the absence of JA. In the presence of JA, MYC or ERF transcription factors activate JA-responsive genes, but only if SA is absent. Activation of both the SA and JA signaling pathways leads to antagonism of JA-responsive gene expression by SA. There are indications for roles in SA/JA crosstalk for cytosolic NPR1, and nuclear localized TGAs, GRX480, and WRKYs. See text for details on the molecular processes underlying the transcriptional control, like redox signaling, sequestration, degradation, phosphorylation, and chromatin modification. Solid lines indicate established (in)activities and dashed lines hypothesized (in)activities, where black arrows specify activation and red blocks suppression. Red crosses indicate that gene transcription is hampered.
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Figure 1: Simplified model of the molecular machinery involved in the transcriptional regulation of the SA signaling pathway (A), the JA signaling pathway (B), or the antagonism of SA on the JA signaling pathway (C). By inducing reduction and monomerization of NPR1, SA activates NPR1 (star-shaped), which then triggers gene expression in the nucleus. JA-responsive genes are kept in check by JAZ repressors in the absence of JA. In the presence of JA, MYC or ERF transcription factors activate JA-responsive genes, but only if SA is absent. Activation of both the SA and JA signaling pathways leads to antagonism of JA-responsive gene expression by SA. There are indications for roles in SA/JA crosstalk for cytosolic NPR1, and nuclear localized TGAs, GRX480, and WRKYs. See text for details on the molecular processes underlying the transcriptional control, like redox signaling, sequestration, degradation, phosphorylation, and chromatin modification. Solid lines indicate established (in)activities and dashed lines hypothesized (in)activities, where black arrows specify activation and red blocks suppression. Red crosses indicate that gene transcription is hampered.

Mentions: Transcriptional and post-translational regulatory mechanisms are important in both SA- and JA-controlled signaling pathways. In the SA pathway, activity of NPR1, which was identified as a master transcriptional co-regulator of SA-dependent genes, is tightly regulated by several SA-dependent modifications (reviewed by Fu and Dong, 2013). SA induces a biphasic fluctuation in the cellular redox state that can be sensed by NPR1, which then switches from an oligomer to monomer form by reduction of intermolecular disulfide bonds. Thioredoxins TRX-h5 and TRX-h3 catalyze the formation of NPR1 monomers, which translocate to the nucleus (Figure 1A). Regulation of NPR1 monomer levels in the nucleus is also dependent on SA. NPR1 and NPR1-homologs NPR3 and NPR4 were described to be SA-receptors (Fu et al., 2012; Wu et al., 2012). NPR3 and NPR4 act as CUL3 ligase adapter proteins in proteasome-mediated degradation of NPR1. NPR3 and NPR4 differ in both their binding affinity for SA and binding capacity to NPR1, so that SA levels determine when NPR1 is targeted for degradation. When SA levels are low, NPR4 interacts with NPR1, leading to its degradation, and in this way untimely transcriptional activation in absence of SA is prevented. High SA levels facilitate binding between NPR1 and NPR3, again leading to removal of NPR1 (Fu et al., 2012). This degradation of NPR1 is thought to help activate programmed cell death, of which NPR1 is a negative regulator. When SA levels are intermediate, interaction between NPR1 and NPR3 is prevented, allowing NPR1 to accumulate and activate SA-dependent defenses. By interacting with transcription factors of the TGA family, NPR1 acts as a co-activator of SA-induced gene transcription, activating SA marker genes such as PR1, but also several WRKY transcription factor genes, which then fine-tune and amplify downstream transcriptional responses (Wang et al., 2006; Eulgem and Somssich, 2007).


How salicylic acid takes transcriptional control over jasmonic acid signaling.

Caarls L, Pieterse CM, Van Wees SC - Front Plant Sci (2015)

Simplified model of the molecular machinery involved in the transcriptional regulation of the SA signaling pathway (A), the JA signaling pathway (B), or the antagonism of SA on the JA signaling pathway (C). By inducing reduction and monomerization of NPR1, SA activates NPR1 (star-shaped), which then triggers gene expression in the nucleus. JA-responsive genes are kept in check by JAZ repressors in the absence of JA. In the presence of JA, MYC or ERF transcription factors activate JA-responsive genes, but only if SA is absent. Activation of both the SA and JA signaling pathways leads to antagonism of JA-responsive gene expression by SA. There are indications for roles in SA/JA crosstalk for cytosolic NPR1, and nuclear localized TGAs, GRX480, and WRKYs. See text for details on the molecular processes underlying the transcriptional control, like redox signaling, sequestration, degradation, phosphorylation, and chromatin modification. Solid lines indicate established (in)activities and dashed lines hypothesized (in)activities, where black arrows specify activation and red blocks suppression. Red crosses indicate that gene transcription is hampered.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4373269&req=5

Figure 1: Simplified model of the molecular machinery involved in the transcriptional regulation of the SA signaling pathway (A), the JA signaling pathway (B), or the antagonism of SA on the JA signaling pathway (C). By inducing reduction and monomerization of NPR1, SA activates NPR1 (star-shaped), which then triggers gene expression in the nucleus. JA-responsive genes are kept in check by JAZ repressors in the absence of JA. In the presence of JA, MYC or ERF transcription factors activate JA-responsive genes, but only if SA is absent. Activation of both the SA and JA signaling pathways leads to antagonism of JA-responsive gene expression by SA. There are indications for roles in SA/JA crosstalk for cytosolic NPR1, and nuclear localized TGAs, GRX480, and WRKYs. See text for details on the molecular processes underlying the transcriptional control, like redox signaling, sequestration, degradation, phosphorylation, and chromatin modification. Solid lines indicate established (in)activities and dashed lines hypothesized (in)activities, where black arrows specify activation and red blocks suppression. Red crosses indicate that gene transcription is hampered.
Mentions: Transcriptional and post-translational regulatory mechanisms are important in both SA- and JA-controlled signaling pathways. In the SA pathway, activity of NPR1, which was identified as a master transcriptional co-regulator of SA-dependent genes, is tightly regulated by several SA-dependent modifications (reviewed by Fu and Dong, 2013). SA induces a biphasic fluctuation in the cellular redox state that can be sensed by NPR1, which then switches from an oligomer to monomer form by reduction of intermolecular disulfide bonds. Thioredoxins TRX-h5 and TRX-h3 catalyze the formation of NPR1 monomers, which translocate to the nucleus (Figure 1A). Regulation of NPR1 monomer levels in the nucleus is also dependent on SA. NPR1 and NPR1-homologs NPR3 and NPR4 were described to be SA-receptors (Fu et al., 2012; Wu et al., 2012). NPR3 and NPR4 act as CUL3 ligase adapter proteins in proteasome-mediated degradation of NPR1. NPR3 and NPR4 differ in both their binding affinity for SA and binding capacity to NPR1, so that SA levels determine when NPR1 is targeted for degradation. When SA levels are low, NPR4 interacts with NPR1, leading to its degradation, and in this way untimely transcriptional activation in absence of SA is prevented. High SA levels facilitate binding between NPR1 and NPR3, again leading to removal of NPR1 (Fu et al., 2012). This degradation of NPR1 is thought to help activate programmed cell death, of which NPR1 is a negative regulator. When SA levels are intermediate, interaction between NPR1 and NPR3 is prevented, allowing NPR1 to accumulate and activate SA-dependent defenses. By interacting with transcription factors of the TGA family, NPR1 acts as a co-activator of SA-induced gene transcription, activating SA marker genes such as PR1, but also several WRKY transcription factor genes, which then fine-tune and amplify downstream transcriptional responses (Wang et al., 2006; Eulgem and Somssich, 2007).

Bottom Line: Additionally, SA can induce negative regulators, among which WRKY transcription factors, that can directly or indirectly inhibit JA-responsive gene expression.Finally, at the DNA level, modification of histones by SA-dependent factors can result in repression of JA-responsive genes.These diverse and complex regulatory mechanisms affect important signaling hubs in the integration of hormone signaling networks.

View Article: PubMed Central - PubMed

Affiliation: Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University Utrecht, Netherlands.

ABSTRACT
Transcriptional regulation is a central process in plant immunity. The induction or repression of defense genes is orchestrated by signaling networks that are directed by plant hormones of which salicylic acid (SA) and jasmonic acid (JA) are the major players. Extensive cross-communication between the hormone signaling pathways allows for fine tuning of transcriptional programs, determining resistance to invaders and trade-offs with plant development. Here, we give an overview of how SA can control transcriptional reprogramming of JA-induced genes in Arabidopsis thaliana. SA can influence activity and/or localization of transcriptional regulators by post-translational modifications of transcription factors and co-regulators. SA-induced redox changes, mediated by thioredoxins and glutaredoxins, modify transcriptional regulators that are involved in suppression of JA-dependent genes, such as NPR1 and TGA transcription factors, which affects their localization or DNA binding activity. Furthermore, SA can mediate sequestering of JA-responsive transcription factors away from their target genes by stalling them in the cytosol or in complexes with repressor proteins in the nucleus. SA also affects JA-induced transcription by inducing degradation of transcription factors with an activating role in JA signaling, as was shown for the ERF transcription factor ORA59. Additionally, SA can induce negative regulators, among which WRKY transcription factors, that can directly or indirectly inhibit JA-responsive gene expression. Finally, at the DNA level, modification of histones by SA-dependent factors can result in repression of JA-responsive genes. These diverse and complex regulatory mechanisms affect important signaling hubs in the integration of hormone signaling networks. Some pathogens have evolved effectors that highjack hormone crosstalk mechanisms for their own good, which are described in this review as well.

No MeSH data available.


Related in: MedlinePlus