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Unravelling chemical priming machinery in plants: the
role of reactive oxygennitrogensulfur species in
abiotic stress tolerance enhancement
Chrystalla Antoniou1,3, Andreas Savvides1,3, Anastasis Christou2
and Vasileios Fotopoulos1
Abiotic stresses severely limit crop yield and their detrimental
effects are aggravated by climate change. Chemical priming is
an emerging field in crop stress management. The exogenous
application of specific chemical agents before stress events
results in tolerance enhancement and reduction of stress
impacts on plant physiology and growth. However, the
molecular mechanisms underlying the remarkable effects of
chemical priming on plant physiology remain to be elucidated.
Reactive oxygen, nitrogen and sulfur species (RONSS) are
molecules playing a vital role in the stress acclimation of plants.
When applied as priming agents, RONSS improve stress
tolerance. This review summarizes the recent knowledge on the
role of RONSS in cell signalling and gene regulation
contributing to abiotic stress tolerance enhancement.
Addresses
1
Department of Agricultural Sciences, Biotechnology and Food Science,
Cyprus University of Technology, Lemesos, Cyprus
2
Agricultural Research Institute, Ministry of Agriculture, Rural
Development and Environment, Nicosia, Cyprus
Corresponding author: Fotopoulos, Vasileios
(vassilis.fotopoulos@cut.ac.cy)
3
These authors contributed equally to this work.
Current Opinion in Plant Biology 2016, 33:101107
This review comes from a themed issue on Cell signalling and gene
regulation
Edited by Kimberley Snowden and Dirk Inze
http://dx.doi.org/10.1016/j.pbi.2016.06.020
1369-5266/# 2016 Elsevier Ltd. All rights reserved.
Introduction
Abiotic stresses severely limit crop yield and their detrimental effects are aggravated by climate change worldwide [1]. Accordingly, to maintain global food security,
stress tolerance improvement in plants is attracting much
attention during the last decades. Different methodologies have been employed to enhance stress tolerance;
some are particularly time-consuming (e.g. conventional
breeding) and others are currently unacceptable in many
countries around the world (e.g. plant genetic modification) [2]. Chemical priming is a rapidly emerging field in
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Figure 1
Non-primed
cell
Abiotic
stress
Normal
tolerance
Impact
RONSS exogenous
application
Abiotic
stress
Primed
cell
Enhanced
tolerance
Impact
Osmoprotection
Primed cell
ROS
detoxification
SNP
Ionic homeostasis
Protein homeostasis
NO
NaHS
Cross-talk
H2O2
H2O2
H2 S
Abiotic
stress
Enhanced tolerance
Physiological
homeostasis
Enhanced
growth
Stress-responsive
genes
PTMs
regulatory
elements
RONSS exogenous application enhances stress tolerance of plants later exposed to abiotic stress and ameliorates stress impacts. Exogenous
application of either H2O2 or SNP (NO donor) or NaHS (H2S donor) initially results in an endogenous accumulation of the chemical compound and
in changes of the endogenous levels of the other RONSS (i.e. cross-talk). A signalling stream is triggered resulting in cell signalling (e.g. posttranslational modifications; PTMs) and gene regulation of stress responsive genes and gene regulatory elements. After exposure to abiotic stress,
pronounced cell signalling and gene regulation events occur leading to enhanced tolerance mechanisms, such as osmoprotection, ROS
detoxification, ionic homeostasis as well as protein homeostasis. Primed plants have increased physiological homeostasis and enhanced growth
when compared with non-primed plants under stress.
Priming plants with RONSS against abiotic stress Antoniou et al. 103
Several reports exist indicating whole genome transcriptional changes that happen shortly (i.e. within hours or
even minutes) after NO or H2O2 application. SNP infiltration in Arabidopsis leaves, revealed significant regulation
of genes encoding proteins implicated in stress response,
photosynthesis, cellular transport, disease resistance and
basic metabolism, within 10 minutes, 1 h and 3 h after
treatment [13]. Remarkably, the majority of these genes
(38%) was rapidly transcriptionally activated within
10 minutes, but the activation was short-lasting, whereas
8.5% and 29.6% of the transcripts showed increased levels
1 h and 3 h after treatment, respectively [13]. In another
study where SNP was applied in Arabidopsis roots, transcriptional analysis on the rosette revealed regulation of
several genes with diverse functions, such as transcripts
encoding proteins related to plant defence response, amelioration of ROS, iron homeostasis and cellular detoxification (e.g. ABC transporter, glutathione S-transferase; GST).
Interestingly, part of the regulated transcripts were genes
encoding TFs and genes implicated in signal transduction
pathways (e.g. mitogen activated protein (MAP) kinases;
[12]). Additionally, in the same study, the transcriptional
response of two SNP concentrations (0.1 mM and 1 mM)
was assessed and 162 genes showed a dose-dependent
expression increase [12]. In a similar report, transcriptional analysis of H2O2 pre-treated plants showed an induction of stress-responsive genes, TFs (e.g. CBFs, DDF1)
and detoxification related genes (e.g. cytochrome P450), but
also a suppression of some genes involved in plant growth
and development [11]. It is proposed that H2O2 is a global
regulator of transcriptional expression [11]. In regard with
H2S, which is the latest player to enter the field, the
available information is limited on the expression profile
of specific genes (i.e. stress-related genes). Application of
NaHS on Arabidopsis and strawberry plants before a
multitude of stress factors affected the expression of
stress-responsive genes, such as heat shock proteins (HSPs;
[20]), Salt Overly Sensitive (SOS; [21]) components,
DREBs[21], CBFs, NCED3 and ABA2 [10]. The massive
transcriptional changes observed in previous studies during
the PS suggests that the exogenous application of RONSS
prepares plants to respond faster, stronger or both when
encountering an abiotic stress pressure.
Genes regulated by the three compounds under
different stresses
The mode of action of these priming agents as signalling molecules is not completely elucidated; however,
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Osmoprotective molecules (e.g. proline and oligosaccharides) and polyamines (e.g. putrescine, spermidine and
spermine) are metabolites with pivotal role in osmotic
adjustment and maintenance of membrane stability
[26,27]. Several reports have shown an up-regulation of
genes-coding biosynthetic enzymes implicated in the
biosynthesis of osmoprotectants in primed plants under
non-stress and stress conditions. For instance, induction
of the genes P5CS (delta 1-pyrroline-5-carboxylate
synthase), which encodes a rate-limiting enzyme in proline formation, and SPS (sucrose-phosphate synthase)
were observed after SNP and H2O2 application in Oryza
sativa plants [28]. A comprehensive gene expression
analysis on the biosynthetic (e.g. ADC) and catabolic
enzymes of polyamines pathway (e.g. PAO, DAO) after
treatment of mature and senescing Medicago truncatula
plants with SNP demonstrated more pronounced gene
expression levels in senescing plants [29].
TFs, kinases and miRNAs are also an important part of
the RONSS-regulated genes pool. They can act downstream by regulating the expression of several genes
involved in many physiological and stress tolerancerelated processes during the PS and after the exposure
to stress. SNP and H2O2 primed plants revealed an
Current Opinion in Plant Biology 2016, 33:101107
Although, gene regulation phenomena before stress exposure share similarities between the three compounds,
there are also stress-specific transcriptional changes. For
example, application of H2O2 in soybean plants enhanced
the expression of genes implicated in oligosaccharides
biosynthesis, mainly 4 h and 6 h after treatment, such as
GmMIPS2 (i.e. myo-inositol synthase) and GmGolS (i.e.
galactinol synthase) under drought stress [16]. Furthermore, SNP application delayed salt-inducible leaf senescing by inducing the expression of genes-coding Na+/H+
antiporters (SOS1 and NHX1) and a cytokinin biosynthesis gene (IPT1), as well as by suppressing the expression
of genes implicated in ABA biosynthesis (NCED2,
NCED9) [31]. Another example is the maximum induction of five Cd-associated genes (MYB107, CAX3, POX1,
MT3 and PCS1) in Arabidopsis 3 h after NaHS pre-treatment [19].
Post-translational modifications
A number of reports exists building a hypothesis of selfpropagation of RONSS and translocation of the signal
from the compartment of the plant where application
takes place to other parts of the plant. This is quite
interesting, especially if, for instance, a priming event
occurred in the root and transcriptional differences could
be recorded in both roots and leaves suggesting a systemic
Current Opinion in Plant Biology 2016, 33:101107
Priming plants with RONSS against abiotic stress Antoniou et al. 105
Known aspects of the mode of action of RONSS presented herein, including cell signalling and gene regulation during the PS, but also the triggered tolerance
mechanisms at stress exposure, strongly suggest that
RONSS may be effectively used as priming agents for
cross-protection against multiple/combined stresses.
However, further research is needed in this area. To
further understand the cellular transcriptional responses
caused by RONSS at PS and after exposure to stress,
comprehensive genomic analyses using detailed time
series with the use of mutants impaired in RONSS
biosynthesis should be incorporated in future studies.
This information is necessary to understand the gene
regulatory network build up by the signalling action of the
compounds.
Acknowledgments
Concluding remarks
Exogenous application of RONSS results in massive
transcriptional regulation of genes during the PS. The
vast majority of these genes are defence-related genes,
such as enzymatic antioxidants and genes implicated in
the production of osmoprotectants and polyamines. The
similarities observed in the type of genes regulated by
either H2O2, NO or H2S application, the involvement of
each of them in the accumulation of the others during the
PS and pharmacological studies (the use of scavengers
and/or inhibitors) suggests a cross-talk network between
RONSS during the PS necessary for tolerance enhancement. The exogenous application of RONSS prepares
plants to respond faster, stronger or both when encountering an abiotic stress pressure. After stress imposition,
primed plants show more pronounced gene expression
levels compared with non-primed plants.
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2.
Hu H, Xiong L: Genetic engineering and breeding of droughtresistant crops. Annu Rev Plant Biol 2014, 65:715-741.
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19. Qiao Z, Jing T, Jin Z, Liang Y, Zhang L, Liu Z, Liu D, Pei Y: CDPKs
enhance Cd tolerance through intensifying H2S signal in
Arabidopsis thaliana. Plant Soil 2016, 398:99-110.
Priming plants with RONSS against abiotic stress Antoniou et al. 107
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