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Special Issue "Salicylic Acid Signalling in Plants"

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 October 2019).

Special Issue Editors

Prof. Dr. Tibor Janda
E-Mail Website
Guest Editor
Department of Plant Physiology, Agricultural Institute, Centre for Agricultural Research, Martonvásár, Hungary
Interests: abiotic stress; acclimation; oxidative stress; polyamines; plant stress physiology; photosynthesis; salicylic acid; signalling
Dr. Magda Pál
E-Mail Website
Guest Editor
Department of Plant Physiology, Agricultural Institute, Centre for Agricultural Research, Eötvös Loránd Research Network, H-2462 Martonvásár, Hungary
Interests: abiotic stress; acclimation; heavy metal stress; oxidative stress; polyamines; plant stress physiology; salicylic acid; signalling
Special Issues and Collections in MDPI journals
Prof. Dr. Gabriella Szalai
E-Mail Website
Guest Editor
Department of Plant Physiology, Agricultural Institute, Centre for Agricultural Research, Martonvásár, Hungary
Interests: abiotic stress; acclimation; analytical chemistry; oxidative stress; polyamines; plant stress physiology; salicylic acid; signalling

Special Issue Information

Dear Colleagues,

Salicylic acid (SA) is ubiquitously distributed in the whole plant kingdom. The basal level of SA differs widely among species. It is generally present either in the free state or in the form of glycosylated, methylated, glucose-ester, or amino acid conjugates. In plants, SA can be synthesized via two distinct and compartmentalized enzymatic pathways both requiring the primary metabolite chorismate. L-phenylalanine, derived from chorismate, can be converted into SA via the precursors free benzoic acid, benzoyl glucose, or ortho-hydroxy-cinnamic acid, depending on the plant species. Chorismate can also be converted into SA via isochorismate. Several physiological processes in which SA may play a role have reported, including seed germination, growth regulation, flower induction, thermogenesis, and, especially, the regulation of plant responses under biotic or abiotic stress conditions. SA may be involved in different signalling processes. For example, various hormones involved in plant defence mechanisms cross talk with SA, and both negative and positive interactions have been reported. SA signalling also leads to the reprogramming of gene expression and protein synthesis. It may affect the antioxidative metabolism, and it modulates cellular redox homeostasis. Although the therapeutic effect of SA in humans has been well studied for about 200 years, its role in plants has only been recognized in recent decades, and the full picture is still not clear. In spite of the extensive work on SA-related processes, the exact mode of action is poorly understood.

Papers submitted to this Special Issue must report high novelty results and/or new models on the mode of action of SA in plants. The molecular mechanism(s) of SA-related signalling processes, new results of the synthesis of SA, and the role of other related molecules (precursors, conjugated forms, etc.) are also interesting. Research articles and review papers are also welcome.

Prof. Dr. Tibor Janda
Dr. Magda Pál
Dr. Gabriella Szalai
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

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Keywords

  • acclimation
  • biosynthesis
  • cross talk
  • hormones
  • phenolics
  • plant growth and development
  • plant stress
  • salicylic acid
  • signalling

Published Papers (11 papers)

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Editorial

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Editorial
Salicylic Acid Signalling in Plants
Int. J. Mol. Sci. 2020, 21(7), 2655; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21072655 - 10 Apr 2020
Cited by 3 | Viewed by 1173
Abstract
Ten articles published in the “Special Issue: Salicylic Acid Signalling in Plants” are summarized, in order to get a global picture about the mode of action of salicylic acid in plants, and about its interaction with other stress-signalling routes. Its ecological aspects and [...] Read more.
Ten articles published in the “Special Issue: Salicylic Acid Signalling in Plants” are summarized, in order to get a global picture about the mode of action of salicylic acid in plants, and about its interaction with other stress-signalling routes. Its ecological aspects and possible practical use are also discussed. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)

Research

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Article
Involvement of Salicylic Acid and Other Phenolic Compounds in Light-Dependent Cold Acclimation in Maize
Int. J. Mol. Sci. 2020, 21(6), 1942; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21061942 - 12 Mar 2020
Cited by 4 | Viewed by 807
Abstract
The exposure of plants to non-lethal low temperatures may increase their tolerance to a subsequent severe chilling stress. To some extent, this is also true for cold-sensitive species, including maize. In the present work, based on our previous microarray experiment, the differentially expressed [...] Read more.
The exposure of plants to non-lethal low temperatures may increase their tolerance to a subsequent severe chilling stress. To some extent, this is also true for cold-sensitive species, including maize. In the present work, based on our previous microarray experiment, the differentially expressed genes with phenylpropanoid pathways in the focus were further investigated in relation to changes in certain phenolic compounds and other plant growth regulators. Phenylalanine ammonia lyase (PAL) was mainly activated under limited light conditions. However, light-induced anthocyanin accumulation occurred both in the leaves and roots. Chilling stress induced the accumulation of salicylic acid (SA), but this accumulation was moderated in the cold-acclimated plants. Acclimation also reduced the accumulation of jasmonic acid (JA) in the leaves, which was rather induced in the roots. The level of abscisic acid (ABA) is mainly related to the level of the stress, and less indicated the level of the acclimation. The highest glutathione (GSH) amount was observed during the recovery period in the leaves of plants that were cold acclimated at growth light, while their precursors started to accumulate GSH even during the chilling. In conclusion, different light conditions during the cold acclimation period differentially affected certain stress-related mechanisms in young maize plants and changes were also light-dependent in the root, not only in the leaves. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Article
Improving Phenolic Total Content and Monoterpene in Mentha x piperita by Using Salicylic Acid or Methyl Jasmonate Combined with Rhizobacteria Inoculation
Int. J. Mol. Sci. 2020, 21(1), 50; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21010050 - 19 Dec 2019
Cited by 8 | Viewed by 1559
Abstract
The effects of plant inoculation with plant growth-promoting rhizobacteria (PGPR) and those resulting from the exogenous application of salicylic acid (SA) or methyl jasmonte (MeJA) on total phenolic content (TPC) and monoterpenes in Mentha x piperita plants were investigated. Although the PGPR inoculation [...] Read more.
The effects of plant inoculation with plant growth-promoting rhizobacteria (PGPR) and those resulting from the exogenous application of salicylic acid (SA) or methyl jasmonte (MeJA) on total phenolic content (TPC) and monoterpenes in Mentha x piperita plants were investigated. Although the PGPR inoculation response has been studied for many plant species, the combination of PGPR and exogenous phytohormones has not been investigated in aromatic plant species. The exogenous application of SA produced an increase in TPC that, in general, was of a similar level when applied alone as when combined with PGPR. This increase in TPC was correlated with an increase in the activity of the enzyme phenylalanine ammonia lyase (PAL). Also, the application of MeJA at different concentrations in combination with inoculation with PGPR produced an increase in TPC, which was more relevant at 4 mM, with a synergism effect being observed. With respect to the main monoterpene concentrations present in peppermint essential oil (EO), it was observed that SA or MeJA application produced a significant increase similar to that of the combination with rhizobacteria. However, when plants were exposed to 2 mM MeJA and inoculated, an important increase was produced in the concentration on menthol, pulegone, linalool, limonene, and menthone concentrations. Rhizobacteria inoculation, the treatment with SA and MeJA, and the combination of both were found to affect the amount of the main monoterpenes present in the EO of M. piperita. For this reason, the expressions of genes related to the biosynthesis of monoterpene were evaluated, with this expression being positively affected by MeJA application and PGPR inoculation, but was not modified by SA application. Our results demonstrate that MeJA or SA application combined with inoculation with PGPR constitutes an advantageous management practice for improving the production of secondary metabolites from M. piperita. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Article
“Salicylic Acid Mutant Collection” as a Tool to Explore the Role of Salicylic Acid in Regulation of Plant Growth under a Changing Environment
Int. J. Mol. Sci. 2019, 20(24), 6365; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20246365 - 17 Dec 2019
Cited by 5 | Viewed by 1512
Abstract
The phytohormone salicylic acid (SA) has a crucial role in plant physiology. Its role is best described in the context of plant response to pathogen attack. During infection, SA is rapidly accumulated throughout the green tissues and is important for both local and [...] Read more.
The phytohormone salicylic acid (SA) has a crucial role in plant physiology. Its role is best described in the context of plant response to pathogen attack. During infection, SA is rapidly accumulated throughout the green tissues and is important for both local and systemic defences. However, some genetic/metabolic variations can also result in SA overaccumulation in plants, even in basal conditions. To date, more than forty Arabidopsis thaliana mutants have been described as having enhanced endogenous SA levels or constitutively activated SA signalling pathways. In this study, we established a collection of mutants containing different SA levels due to diverse genetic modifications and distinct gene functions. We chose prototypic SA-overaccumulators (SA-OAs), such as bon1-1, but also “non-typical” ones such as exo70b1-1; the selection of OA is accompanied by their crosses with SA-deficient lines. Here, we extensively studied the plant development and SA level/signalling under various growth conditions in soil and in vitro, and showed a strong negative correlation between rosette size, SA content and PR1/ICS1 transcript signature. SA-OAs (namely cpr5, acd6, bon1-1, fah1/fah2 and pi4kβ1β2) had bigger rosettes under high light conditions, whereas WT plants did not. Our data provide new insights clarifying a link between SA and plant behaviour under environmental stresses. The presented SA mutant collection is thus a suitable tool to shed light on the mechanisms underlying trade-offs between growth and defence in plants. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Article
Polyamine-Induced Hormonal Changes in eds5 and sid2 Mutant Arabidopsis Plants
Int. J. Mol. Sci. 2019, 20(22), 5746; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20225746 - 15 Nov 2019
Cited by 8 | Viewed by 1047
Abstract
Polyamines are multifaceted compounds which play a role in regulating plant growth and stress tolerance in interactions with plant hormones. The aim of the present study was to reveal how exogenous polyamines influence the synthesis of salicylic acid, with a special emphasis on [...] Read more.
Polyamines are multifaceted compounds which play a role in regulating plant growth and stress tolerance in interactions with plant hormones. The aim of the present study was to reveal how exogenous polyamines influence the synthesis of salicylic acid, with a special emphasis on the effect of salicylic acid deficiency on the polyamine metabolism and polyamine-induced changes in other plant hormone contents. Our hypothesis was that the individual polyamines induced different changes in the polyamine and salicylic acid metabolism of the wild type and salicylic acid-deficient Arabidopsis mutants, which in turn influenced other hormones. To our knowledge, such a side-by-side comparison of the influence of eds5-1 and sid2-2 mutations on polyamines has not been reported yet. To achieve our goals, wild and mutant genotypes were tested after putrescine, spermidine or spermine treatments. Polyamine and plant hormone metabolism was investigated at metabolite and gene expression levels. Individual polyamines induced different changes in the Arabidopsis plants, and the responses were also genotype-dependent. Polyamines upregulated the polyamine synthesis and catabolism, and remarkable changes in hormone synthesis were found especially after spermidine or spermine treatments. The sid2-2 mutant showed pronounced differences compared to Col-0. Interactions between plant hormones may also be responsible for the observed differences. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Article
Novel Salicylic Acid Analogs Induce a Potent Defense Response in Arabidopsis
Int. J. Mol. Sci. 2019, 20(13), 3356; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20133356 - 08 Jul 2019
Cited by 9 | Viewed by 1734
Abstract
The master regulator of salicylic acid (SA)-mediated plant defense, NPR1 (NONEXPRESSER OF PR GENES 1) and its paralogs NPR3 and NPR4, act as SA receptors. After the perception of a pathogen, plant cells produce SA in the chloroplast. In the presence of SA, [...] Read more.
The master regulator of salicylic acid (SA)-mediated plant defense, NPR1 (NONEXPRESSER OF PR GENES 1) and its paralogs NPR3 and NPR4, act as SA receptors. After the perception of a pathogen, plant cells produce SA in the chloroplast. In the presence of SA, NPR1 protein is reduced from oligomers to monomers, and translocated into the nucleus. There, NPR1 binds to TGA, TCP, and WRKY transcription factors to induce expression of plant defense genes. A list of compounds structurally similar to SA was generated using ChemMine Tools and its Clustering Toolbox. Several of these analogs can induce SA-mediated defense and inhibit growth of Pseudomonas syringae in Arabidopsis. These analogs, when sprayed on Arabidopsis, can induce the accumulation of the master regulator of plant defense NPR1. In a yeast two-hybrid system, these analogs can strengthen the interactions among NPR proteins. We demonstrated that these analogs can induce the expression of the defense marker gene PR1. Furthermore, we hypothesized that these SA analogs could be potent tools against the citrus greening pathogen Candidatus liberibacter spp. In fact, our results suggest that the SA analogs we tested using Arabidopsis may also be effective for inducing a defense response in citrus. Several SA analogs consistently strengthened the interactions between citrus NPR1 and NPR3 proteins in a yeast two-hybrid system. In future assays, we plan to test whether these analogs avoid degradation by SA hydroxylases from plant pathogens. In future assays, we plan to test whether these analogs avoid degradation by SA hydroxylases from plant pathogens. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Article
Involvement of Salicylic Acid in Anthracnose Infection in Tea Plants Revealed by Transcriptome Profiling
Int. J. Mol. Sci. 2019, 20(10), 2439; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20102439 - 17 May 2019
Cited by 7 | Viewed by 1813
Abstract
Anthracnose is a major leaf disease in tea plant induced by Colletotrichum, which has led to substantial losses in yield and quality of tea. The molecular mechanism with regards to responses or resistance to anthracnose in tea remains unclear. A de novo [...] Read more.
Anthracnose is a major leaf disease in tea plant induced by Colletotrichum, which has led to substantial losses in yield and quality of tea. The molecular mechanism with regards to responses or resistance to anthracnose in tea remains unclear. A de novo transcriptome assembly dataset was generated from healthy and anthracnose-infected leaves on tea cultivars “Longjing-43” (LJ43) and “Zhenong-139” (ZN139), with 381.52 million pair-end reads, encompassing 47.78 billion bases. The unigenes were annotated versus Gene Ontology (GO), Kyoto Encyclopedia of Genes and Genomes (KEGG), National Center for Biotechnology Information (NCBI) non-redundant protein sequences (Nr), evolutionary genealogy of genes: Non-supervised Orthologous Groups (eggNOG) and Swiss-prot. The number of differential expression genes (DEGs) detected between healthy and infected leaves was 1621 in LJ43 and 3089 in ZN139. The GO and KEGG enrichment analysis revealed that the DEGs were highly enriched in catalytic activity, oxidation-reduction, cell-wall reinforcement, plant hormone signal transduction and plant-pathogen interaction. Further studies by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR) and high-performance liquid chromatography (HPLC) showed that expression of genes involved in endogenous salicylic acid biosynthesis and also accumulation of foliar salicylic acid are involved in the response of tea plant to anthracnose infection. This study firstly provided novel insight in salicylic acid acting as a key compound in the responses of tea plant to anthracnose disease. The transcriptome dataset in this study will facilitate to profile gene expression and metabolic networks associated with tea plant immunity against anthracnose. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Review

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Review
The Ecology of Salicylic Acid Signaling: Primary, Secondary and Tertiary Effects with Applications in Agriculture
Int. J. Mol. Sci. 2019, 20(23), 5851; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20235851 - 21 Nov 2019
Cited by 8 | Viewed by 1347
Abstract
The salicylic acid pathway is one of the primary plant defense pathways, is ubiquitous in vascular plants, and plays a role in rapid adaptions to dynamic abiotic and biotic stress. Its prominence and ubiquity make it uniquely suited for understanding how biochemistry within [...] Read more.
The salicylic acid pathway is one of the primary plant defense pathways, is ubiquitous in vascular plants, and plays a role in rapid adaptions to dynamic abiotic and biotic stress. Its prominence and ubiquity make it uniquely suited for understanding how biochemistry within plants can mediate ecological consequences. Induction of the salicylic acid pathway has primary effects on the plant in which it is induced resulting in genetic, metabolomic, and physiologic changes as the plant adapts to challenges. These primary effects can in turn have secondary consequences for herbivores and pathogens attacking the plant. These secondary effects can both directly influence plant attackers and mediate indirect interactions between herbivores and pathogens. Additionally, stimulation of salicylic acid related defenses can affect natural enemies, predators and parasitoids, which can recruit to plant signals with consequences for herbivore populations and plant herbivory aboveground and belowground. These primary, secondary, and tertiary ecological consequences of salicylic acid signaling hold great promise for application in agricultural systems in developing sustainable high-yielding management practices that adapt to changing abiotic and biotic environments. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Review
The Multifaceted Roles of Plant Hormone Salicylic Acid in Endoplasmic Reticulum Stress and Unfolded Protein Response
Int. J. Mol. Sci. 2019, 20(23), 5842; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20235842 - 21 Nov 2019
Cited by 9 | Viewed by 1914
Abstract
Different abiotic and biotic stresses lead to the accumulation of unfolded and misfolded proteins in the endoplasmic reticulum (ER), resulting in ER stress. In response to ER stress, cells activate various cytoprotective responses, enhancing chaperon synthesis, protein folding capacity, and degradation of misfolded [...] Read more.
Different abiotic and biotic stresses lead to the accumulation of unfolded and misfolded proteins in the endoplasmic reticulum (ER), resulting in ER stress. In response to ER stress, cells activate various cytoprotective responses, enhancing chaperon synthesis, protein folding capacity, and degradation of misfolded proteins. These responses of plants are called the unfolded protein response (UPR). ER stress signaling and UPR can be regulated by salicylic acid (SA), but the mode of its action is not known in full detail. In this review, the current knowledge on the multifaceted role of SA in ER stress and UPR is summarized in model plants and crops to gain a better understanding of SA-regulated processes at the physiological, biochemical, and molecular levels. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Review
Salicylic Acid Binding Proteins (SABPs): The Hidden Forefront of Salicylic Acid Signalling
Int. J. Mol. Sci. 2019, 20(18), 4377; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20184377 - 06 Sep 2019
Cited by 18 | Viewed by 2135
Abstract
Salicylic acid (SA) is a phytohormone that plays important roles in many aspects of plant life, notably in plant defenses against pathogens. Key mechanisms of SA signal transduction pathways have now been uncovered. Even though details are still missing, we understand how SA [...] Read more.
Salicylic acid (SA) is a phytohormone that plays important roles in many aspects of plant life, notably in plant defenses against pathogens. Key mechanisms of SA signal transduction pathways have now been uncovered. Even though details are still missing, we understand how SA production is regulated and which molecular machinery is implicated in the control of downstream transcriptional responses. The NPR1 pathway has been described to play the main role in SA transduction. However, the mode of SA perception is unclear. NPR1 protein has been shown to bind SA. Nevertheless, NPR1 action requires upstream regulatory events (such as a change in cell redox status). Besides, a number of SA-induced responses are independent from NPR1. This shows that there is more than one way for plants to perceive SA. Indeed, multiple SA-binding proteins of contrasting structures and functions have now been identified. Yet, all of these proteins can be considered as candidate SA receptors and might have a role in multinodal (decentralized) SA input. This phenomenon is unprecedented for other plant hormones and is a point of discussion of this review. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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Review
Salicylic Acid Signals Plant Defence against Cadmium Toxicity
Int. J. Mol. Sci. 2019, 20(12), 2960; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20122960 - 18 Jun 2019
Cited by 15 | Viewed by 2146
Abstract
Salicylic acid (SA), as an enigmatic signalling molecule in plants, has been intensively studied to elucidate its role in defence against biotic and abiotic stresses. This review focuses on recent research on the role of the SA signalling pathway in regulating cadmium (Cd) [...] Read more.
Salicylic acid (SA), as an enigmatic signalling molecule in plants, has been intensively studied to elucidate its role in defence against biotic and abiotic stresses. This review focuses on recent research on the role of the SA signalling pathway in regulating cadmium (Cd) tolerance in plants under various SA exposure methods, including pre-soaking, hydroponic exposure, and spraying. Pretreatment with appropriate levels of SA showed a mitigating effect on Cd damage, whereas an excessive dose of exogenous SA aggravated the toxic effects of Cd. SA signalling mechanisms are mainly associated with modification of reactive oxygen species (ROS) levels in plant tissues. Then, ROS, as second messengers, regulate a series of physiological and genetic adaptive responses, including remodelling cell wall construction, balancing the uptake of Cd and other ions, refining the antioxidant defence system, and regulating photosynthesis, glutathione synthesis and senescence. These findings together elucidate the expanding role of SA in phytotoxicology. Full article
(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)
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