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Salicylic Acid Signalling in Plants

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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) | Viewed by 67686

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Prof. Dr. Tibor Janda

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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
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Dr. Magda Pál

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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
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Prof. Dr. Gabriella Szalai

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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

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Keywords

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

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Published Papers (11 papers)

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Editorial

Jump to: Research, Review

6 pages, 227 KiB

Open AccessEditorial

Salicylic Acid Signalling in Plants

by Tibor Janda, Gabriella Szalai and Magda Pál

Int. J. Mol. Sci. 2020, 21(7), 2655; https://doi.org/10.3390/ijms21072655 - 10 Apr 2020

Cited by 65 | Viewed by 6626

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.

(This article belongs to the Special Issue Salicylic Acid Signalling in Plants)

Research

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18 pages, 3715 KiB

Open AccessArticle

Involvement of Salicylic Acid and Other Phenolic Compounds in Light-Dependent Cold Acclimation in Maize

by Magda Pál, Tibor Janda, Imre Majláth and Gabriella Szalai

Int. J. Mol. Sci. 2020, 21(6), 1942; https://doi.org/10.3390/ijms21061942 - 12 Mar 2020

Cited by 22 | Viewed by 3317

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 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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22 pages, 3205 KiB

Open AccessArticle

Improving Phenolic Total Content and Monoterpene in Mentha x piperita by Using Salicylic Acid or Methyl Jasmonate Combined with Rhizobacteria Inoculation

by Lorena del Rosario Cappellari, Maricel Valeria Santoro, Axel Schmidt, Jonathan Gershenzon and Erika Banchio

Int. J. Mol. Sci. 2020, 21(1), 50; https://doi.org/10.3390/ijms21010050 - 19 Dec 2019

Cited by 54 | Viewed by 5324

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 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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15 pages, 2691 KiB

Open AccessArticle

“Salicylic Acid Mutant Collection” as a Tool to Explore the Role of Salicylic Acid in Regulation of Plant Growth under a Changing Environment

by Kamila Pluhařová, Hana Leontovyčová, Věra Stoudková, Romana Pospíchalová, Petr Maršík, Pavel Klouček, Anastasiia Starodubtseva, Oksana Iakovenko, Zuzana Krčková, Olga Valentová, Lenka Burketová, Martin Janda and Tetiana Kalachova

Int. J. Mol. Sci. 2019, 20(24), 6365; https://doi.org/10.3390/ijms20246365 - 17 Dec 2019

Cited by 18 | Viewed by 6125

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 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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23 pages, 5417 KiB

Open AccessArticle

Polyamine-Induced Hormonal Changes in eds5 and sid2 Mutant Arabidopsis Plants

by Judit Tajti, Kamirán Áron Hamow, Imre Majláth, Krisztián Gierczik, Edit Németh, Tibor Janda and Magda Pál

Int. J. Mol. Sci. 2019, 20(22), 5746; https://doi.org/10.3390/ijms20225746 - 15 Nov 2019

Cited by 24 | Viewed by 4234

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 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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15 pages, 3726 KiB

Open AccessArticle

Novel Salicylic Acid Analogs Induce a Potent Defense Response in Arabidopsis

by Ian Arthur Palmer, Huan Chen, Jian Chen, Ming Chang, Min Li, Fengquan Liu and Zheng Qing Fu

Int. J. Mol. Sci. 2019, 20(13), 3356; https://doi.org/10.3390/ijms20133356 - 8 Jul 2019

Cited by 27 | Viewed by 5246

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, 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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21 pages, 4268 KiB

Open AccessArticle

Involvement of Salicylic Acid in Anthracnose Infection in Tea Plants Revealed by Transcriptome Profiling

by Yun-Long Shi, Yue-Yue Sheng, Zhuo-Yu Cai, Rui Yang, Qing-Sheng Li, Xu-Min Li, Da Li, Xiao-Yuan Guo, Jian-Liang Lu, Jian-Hui Ye, Kai-Rong Wang, Long-Jie Zhang, Yue-Rong Liang and Xin-Qiang Zheng

Int. J. Mol. Sci. 2019, 20(10), 2439; https://doi.org/10.3390/ijms20102439 - 17 May 2019

Cited by 32 | Viewed by 5900

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 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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19 pages, 3569 KiB

Open AccessReview

The Ecology of Salicylic Acid Signaling: Primary, Secondary and Tertiary Effects with Applications in Agriculture

by Camila C. Filgueiras, Adalvan D. Martins, Ramom V. Pereira and Denis S. Willett

Int. J. Mol. Sci. 2019, 20(23), 5851; https://doi.org/10.3390/ijms20235851 - 21 Nov 2019

Cited by 55 | Viewed by 5777

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 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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13 pages, 638 KiB

Open AccessReview

The Multifaceted Roles of Plant Hormone Salicylic Acid in Endoplasmic Reticulum Stress and Unfolded Protein Response

by Péter Poór, Zalán Czékus, Irma Tari and Attila Ördög

Int. J. Mol. Sci. 2019, 20(23), 5842; https://doi.org/10.3390/ijms20235842 - 21 Nov 2019

Cited by 40 | Viewed by 5753

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 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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20 pages, 2036 KiB

Open AccessReview

Salicylic Acid Binding Proteins (SABPs): The Hidden Forefront of Salicylic Acid Signalling

by Igor Pokotylo, Volodymyr Kravets and Eric Ruelland

Int. J. Mol. Sci. 2019, 20(18), 4377; https://doi.org/10.3390/ijms20184377 - 6 Sep 2019

Cited by 68 | Viewed by 9887

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 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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19 pages, 859 KiB

Open AccessReview

Salicylic Acid Signals Plant Defence against Cadmium Toxicity

by Bin Guo, Chen Liu, Yongchao Liang, Ningyu Li and Qinglin Fu

Int. J. Mol. Sci. 2019, 20(12), 2960; https://doi.org/10.3390/ijms20122960 - 18 Jun 2019

Cited by 65 | Viewed by 8031

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) 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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