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Research Journal of Biotechnology Vol. 13 (12) December (2018)
Res. J. Biotech
97
Review Paper:
Plant Defense against Pathogens:
The Role of Salicylic Acid
Kumar Vinod and AlMomin Sabah
Biotechnology Program, Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, KUWAIT
vinodk@kisr.edu.kw; smomen@kisr.edu.kw
Abstract
Increasing demand for the global food production in
the agricultural sector is a crucial driving force for the
development of new disease-management methods that
are not only effective against known pathogens, but
also to the ones that will evolve. Plants possess
specialized structures, chemicals and sophisticated
mechanisms to defend themselves from pathogens.
Understanding these defense mechanisms and
pathways are critical for developing innovative
approaches to protect crop plants from diseases as
pathogens are continually evolving intricate means of
breaching plant defenses. Plant defense pathways
involve a number of signaling compounds that regulate
the production of defense-related chemicals. These
pathways are strongly connected with salicylic acid
(SA), ethylene (ET), jasmonic acid (JA) and abscisic
acid (ABA). The compound that is in the center of
interest in this review article is salicylic acid due to its
involvement in a variety of functions including biotic
and abiotic stress management in plants.
The adverse effects of overuse of pesticides have led to
the development and adoption of genetically
engineered crops including those expressing genes
involved in SA mediated defense pathways for
enhanced defense capabilities, higher yields under
biotic stress with reduced use of harmful pesticides.
This review article focuses on latest developments in
the plant-pathogen interaction and in particular, on the
functional role played by salicylic acid in plant defense.
A better understanding of plant defense mechanisms
will enable scientists to develop more efficient methods
of protecting plants from pathogens for sustainable
agriculture.
Keywords: Defense Activation, Jasmonic Acid, Plant–
Pathogen Interaction, Plant diseases, Salicylic Acid,
Transgenic Plants.
Introduction
Plants possess mechanisms for withstanding drought,
salinity, extreme temperatures, toxins and diseases caused
by pathogens1,2. Many species of bacteria, fungi, viruses and
nematodes attack plants often with devastating impact. From
germination onwards, plants are vulnerable to different types
of pathogens that may be present in the habitat and to
environmental factors that compromise plant immunity.
Some pathogens infect, multiply and complete their life
cycles within a living host, whereas others kill the host in the
course of the development of the infection. Plants have
therefore evolved diverse means of protecting themselves
from the pathogens that attack them.
Modern agriculture relies heavily on integrated disease-
management methods in order to protect plants from
devastating diseases that can cause substantial economic
losses. A better understanding of plant defense signaling
would enable researchers to develop better methods of
disease control for the protection of crops. Recent progress
made in systems biology, transcriptomics, metabolomics
and genomics has significantly enhanced our knowledge of
plant defense and has contributed to improvements in crop
protection methods.
This review focuses on developments in the area of plant
defense mechanisms and specifically on the role of salicylic
acid (SA) in disease and abiotic stress management. The
review will also discuss some of the signaling pathways
involved in chemical responses to pathogens with a specific
focus on the role of SA in those pathways.
A critical step in a successful plant defense is early
recognition of the pathogen by the host. Host plants can
recognize a wide range of chemicals, known as pathogen-
associated molecular patterns (PAMPs), that originate from
the invading pathogen3-5. PAMPs may be structural
components of the pathogen cell wall, or they may be
substances secreted by the pathogen and then recognized by
the plant with the help of receptors4,6,7.
In addition, various fungal hydrolytic enzymes can generate
plant-derived elicitors from the host cell wall and these
molecules can also participate in signaling8. Among the most
important of these elicitors are flagellin, elongation factor
Tu(EF-Tu), AvrXa21, chitin oligomers, peptidoglycans and
lipopolysaccharides5,9,10. These signals are perceived by the
host plant’s receptors activating the defense machinery
through a complex cascade of events.
Subsequent steps in the defense of the plant involve the
activation of signaling, which in turn leads to the production
of defense-related compounds11,12. Defense pathways in
plants are strongly associated with four compounds: SA,
ethylene (ET), jasmonic acid (JA) and abscisic acid
(ABA)12,13. SA is synthesized in plants from cinnamate and
isochorismate14 and its involvement in the regulation of plant
Research Journal of Biotechnology Vol. 13 (12) December (2018)
Res. J. Biotech
98
defense against specific types of pathogens has been
described in detail15-23. Emerging evidence suggests that SA
is also involved in abiotic stress management24-26.
Of the other compounds, JA plays a vital role in defense
against insects and herbivores27,28. Further complexity
results from the significant overlap and crosstalk between
the defense responses mediated by SA and those mediated
by JA13,29-31.
The Role of Salicylic Acid and Related Compounds in
Plant Defense: Salicylate derivatives such as acetylsalicylic
acid (aspirin), have long been used in pharmacology for their
anti-inflammatory effects32-34. In plant defense, the earliest
evidence for the role of acetylsalicylic acid in plant-pathogen
interaction was found in Nicotiana tabacum that had been
infected with tobacco mosaic virus23. A growing body of
evidence suggests that SA is essential not only for
establishing the local defense of a plant, but also for
protecting the healthy neighboring tissues during
infection17,19,21,22,26,35-38. This is achieved by transmitting
signals from the infected parts, a process is known as
systemic acquired resistance (SAR) and is part of the plant's
response to infection by biotrophic pathogens.
Biotrophic pathogens keep the host plant alive until the
completion of their life cycle, with the consequence that a
plant’s SA-mediated resistance to biotrophic pathogens is
mainly effected by means of SA signaling21.
NPR1-Mediated Defense in Plants: SA is linked to various
essential components of plant defense through intricate
networks. Non-expressor of PR1 protein (NPR1) is an
important component in plant defense signaling. The
detailed mechanism of SA-mediated regulation of defense
through NPR1-mediated signaling has been well
documented39-43 and the role of NPR1 in SA-mediated
defense signaling and its regulation in the cytoplasm and
nucleolus are summarized in figure 1. NPR1 is constitutively
expressed in most cell types and it remains mostly inactive
in the cytosol in an oligomeric form until the host is infected
with a pathogen.
Following infection, the host plant produces more SA and
the increased SA content is associated with an alteration in
the cell’s redox potential. As a result, the NPR1 oligomer is
reduced to biologically active monomers. The monomeric
NPR1 then moves to the nucleus where it interacts with TGA
proteins. This interaction results in the expression of various
SA-dependent pathogenesis-related (PR) genes44,45.
Various factors influence the translocation of NPR1 to the
nucleus. It has been proposed that phospholipase D affects
translocation of NPR1 to the nucleus in Arabidopsis 46. The
role of glutathione (GSH) in plant defense and stress
physiology is well known and recent research has
investigated in more detail the active part it plays in plant
defense signaling47-49. Transgenic tobacco plants that
produce enhanced levels of GSH have been found to
accumulate more SA than those with normal levels of GSH.
Enhanced expression of genes belonging to an NPR1-
dependent SA-mediated pathway has also been observed
providing further indication that GSH is closely involved in
plant defense50.
Nitric oxide (NO) participates in the redox regulation of the
NPR1-TGA1 system and the translocation of NPR1 into the
nucleus51,52. Crosstalk between NO and GSH is critical for
NPR1-mediated defense in Arabidopsis and there is
evidence to suggest that NO is involved in activating an
NPR1-mediated defense response through SA48. Although
NO has been well studied as a signaling molecule that
participates in various physiological activities, little is
known about its regulatory role in defense signaling.
Kovacs et al48 reported an NO-activated, SA-dependent
defense response in Arabidopsis thaliana. They found that a
donor of NO, S-nitrosoglutathione (GSNO), promoted the
nuclear accumulation of NPR1 protein, elevated the SA
concentration and activated the transcription of PR genes,
thereby producing an increased resistance against infection.
In the same study, the authors observed an increase in the
concentration of GSH, thus reconfirming the role of GSH in
plant defense. Thus, their data provide evidence for crosstalk
between NO and GSH in SA-mediated, NPR1-dependent
defense.
Although most hormones in plants and animals have specific
receptors, SA receptors were discovered only recently. In
Arabidopsis, proteins NPR1 through NPR6 constitute a
multigene family53; of these, NPR3 and NPR4 have been
shown to interact with SA54, functioning as adaptors of the
Cullin-3 ubiquitin E3 ligase to mediate NPR1 degradation in
an SA-regulated manner55. NPR3 and NPR4 have been
shown to bind SA directly and this binding modulates their
interaction with NPR154.
The turnover of NPR1 is critical for regulating defense.
SUMOylation (SUMO: small ubiquitin-like modifier) of
NPR1 triggers its degradation, while phosphorylation at
NPR1 residues Ser55/Ser59 inhibits this SUMOylation, thus
stabilizing NPR1. These post-translational modifications
play a critical role in the precise control of NPR1-mediated
plant defense responses42,56-58.
Certain components negatively regulate the nuclear
transportation of NPR1. It has been shown that pathogen-
triggered (or SA-induced) nuclear translocation is prevented
by accumulation of H2O2 in the cytosol and that the
cytoplasmic reactive oxygen species (ROS) has a negative
effect on NPR1-dependent gene expression59. In addition to
SA, several synthetic analogs such as 2,6-
dichloroisonicotinic acid (INA) and benzo-(1,2,3)-
thiadiazole-7-carbothioic acid S-methyl ester (BTH), have
been shown to induce SAR60-63. These findings open up new
Research Journal of Biotechnology Vol. 13 (12) December (2018)
Res. J. Biotech
99
avenues for developing novel compounds similar to SA that
can activate defense responses in crop plants.
Modulation of SA and NPR1-Mediated Defense through
a Transgenic Approach: Genetic engineering has become
a valuable tool for enhancing disease resistance in plants. For
example, genes encoding defense-related proteins have been
successfully engineered into crop plants. Since the NPR1
protein is directly involved in plant defense, the encoding
gene has been successfully used to engineer plants including
cotton, tobacco, citrus, tomato, apple, strawberry and carrot
to improve their resistance to diseases64-75. We and others
have tested transgenic cotton plants expressing the AtNPR1
gene against various pathogens66,69,75,76.
The transgenic plants showed a rapid activation of their
defense genes in response to infection with the fungal
pathogens Fusarium oxysporum, Rhizoctonia solani,
Thielaviopsis basicola and Verticillium dahliae and also in
response to the reniform nematode. Molecular analysis
revealed that the activation of SA-mediated defense was one
of the major contributing factors in the enhanced defense
response of transgenic cotton plants expressing the AtNPR1
gene70.
SA is involved in a variety of functions including plant
abiotic stress management. For example, transgenic cotton
plants expressing an endochitinase gene (isolated from
Trichoderma virens) showed symptoms of abnormal defense
gene activation including the formation of a lesion-mimic
phenotype, characterized by cell death under nutrient stress
conditions.
Fig. 1: Model depicting crosstalk among the components of SA-mediated defense
Upon pathogen infection, SA accumulates and activates the non-expressor of pathogenesis-related gene 1 (NPR1).
Once activated, NPR1 is localized to the nucleus, where it interacts with TGA transcription factors and this leads to
the activation of PR genes. In the cytosol, the activated NPR1 negatively regulates JA-responsive gene expression 80.
Elevated accumulation of glutathione (GSH) takes place through oxidative modulation of GSH by an NO burst via
NO-donor S-nitrosoglutathione (GSNO) 81. This leads to activation of isochorismatesynthase1 (ICS1)-mediated SA
production and leads to monomerization of NPR1. Kovacs et al (2015) have demonstrated the involvement of
crosstalk between NO and GSH in NPR-mediated defense signaling48. The cellular homeostasis of oligomeric and
monomeric NPR1 is regulated via S-nitrosylation (SNO) and thioredoxins. Monomeric NPR1, Cullin-3-based E3
ligase protein complex and an unknown substrate adaptor protein (Adp-A) interact prior to the recruitment of NPR1.
The NPR1 is constantly degraded by ubiquitin (Ub) via a nuclear proteasome pathway. Activation of systemic
acquired resistance (SAR) results in the influx of monomeric NPR1 to the nucleus, a portion of which will be
phosphorylated. However, both forms of NPR1 have been shown to interact with TGA transcription factors.
Constant recycling of NPR1 is required in order to maintain cellular homeostasis.
NPR1
oligomer
Nucleus
Cytoplasm
SA
NPR1
JA
responses
NPR1
TGA
PR-1
Pathogen
JA
PDF1.2
VSP
LOX2
NO
Elevated GSH
ICS1
NO/GSNO
SNO
TRXs
Resistance
CUL3
UB
Adp-B
NPR1
Complex
Degraded
NPR1
Research Journal of Biotechnology Vol. 13 (12) December (2018)
Res. J. Biotech
100
The formation of lesions was associated with high levels of
hydrogen peroxide and increased lipoxygenase activity. This
abnormal phenotype was rescued when SA was applied
through the roots directly to the growing plants77. This
clearly shows that SA has many different roles in plant
including abiotic stress management. Further research in this
field would allow the development of SA-based
formulations for enhancing the ability of plants to tolerate
both biotic and abiotic stress.
Conclusion
In the last decade, there have been tremendous developments
in the field of plant-pathogen interactions. These includes
the discovery of new elicitors, PAMPs, receptors and
antimicrobial compounds as well as improvements in our
understanding of the roles played by signaling pathways and
their crosstalk. However, very little translation into field
applications has resulted from all the acquired data. The
growth of the world’s population has led to a high and
increasing demand for food and a significant challenge
facing us is how to maximize crop output from a limited
amount of agricultural land and resources.
Heavy pesticide usage in intensive agriculture has become a
great cause for concern, owing to its increasing cost and its
negative impact on human health and on the
environment78,79. For these reasons, there is an excellent
opportunity to develop novel approaches for a more
sustainable agriculture, based on plant defense signaling
chemicals that use the plants’ own defense systems to confer
resistance to biotic and abiotic stress. The genetic
engineering of crop plants with useful traits has dramatically
enhanced crop productivity in an environmental-friendly
and sustainable way. The development of improved methods
for disease management would significantly reduce our
dependence on the excessive use of chemical pesticides.
Acknowledgement
The authors gratefully acknowledge Kuwait Foundation for
the Advancement of Sciences (KFAS) for funding the
project (Grant No. 2013-4401-01).
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(Received 23rd March 2018, accepted 25th June 2018)
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