Genetic Regulation of Cross Tolerance in Plants
Under Biotic and Abiotic Stresses
Review Article
Mahya Bahmani, Reza Maali-Amiri *
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University College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
Abstract
Plants face many biotic and abiotic stresses at the same time during their growth under field conditions. Plants
responses toward combined stresses are often more complex than their responses to one type of stress in a
way that the results of these responses are called as cross tolerance. This mixture of stresses activates specific
models of gene expression that causes special signaling networks and activation of some components of resistance reactions in plants like systemic acquired resistance and R-genes. Recently, because of great progresses
in genetic sciences, genetic regulation of cross tolerance has gained a lot of attention and it seems that genome
reprogramming influenced by combined stresses can play a special role through inducing defense responses in
plants. Depending on the nature, duration, and intensity of stresses, their impacts on plants can be additive or
antagonistic. Actually, a range of molecular mechanisms are activated in order to respond to a new situation.
The components of these mechanisms include reactive oxygen species, hormone signaling and transcription
factors. Nowadays, a great challenge in plant cross tolerance is how plants balance their resources between
growth and defence against stresses. This review focuses on the responses of plants to simultaneous biotic and
abiotic stresses at the molecular level and the importance of studying plant stress factors in combination.
Key words: Gene; Gene Regulation; Reactive Oxygen Species; Transcription Factors; Hormones
Introduction
Plants have improved special mechanisms that
allow them to recognize precise environmental
changes and respond to several stress situations,
reducing the damage while protecting necessary
resources for growth and reproduction (1). Plant
stresses can be divided into two major abiotic and
biotic groups. Abiotic stresses such as heat, cold,
drought, and salinity are the most common factors
that have a huge effect on the crop production and
reduce the average yield by >50% (2). Moreover,
biotic stresses are pests, pathogens, fungi, bacteria,
viruses, and nematodes (3). When a plant encounters
one stress, it may become more tolerant to another;
this phenomenon that is called cross tolerance has
been realized since years ago (4).
* Reza Maali Amiri, PhD
Department of Agronomy and Plant Breeding, University College of Agriculture and Natural Resources, University of Tehran,
Karaj, Iran
Email: [email protected]
Submission Date: 22 Apr. 2015 Acceptance Date: 22 Jul. 2015
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Genetics in the 3rd Millennium, Vol. 13, No.3 Autumn 2015
Many plants grow in suboptimal conditions that
prevent them from reaching their full genetic potential
for growth and reproduction (5). Thus, plants activate
a specific and unique stress response when subjected
to a combination of multiple stresses. Recent
evidence suggests that appropriate mechanisms can
not be understood directly from individual stress
studies where each stress is applied independently
(6). In recent years, demand for creating plant
abiotic and biotic tolerance has become apparent
and because of advanced progresses in genetic
sciences, genetic regulation of cross tolerance has
become more important than before, and it seems
that reprogramming of genome influenced by
multiple stresses can play an important role in plants
tolerance to simultaneous stresses. Most responses
in transcriptional and translational levels can change
under multiple stresses; nowadays, it is believed that
gene expression in combined stresses may be an
approach to react under complex stress situations.
According to current climate prediction models,
the average surface temperature will increase by
3-5ºC in the next 50-100 years, so this climate
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changing will expand the range of hosts for pests
and pathogens because thermal increase can change
the pattern of crop cultivation and causes alternation
of spring cultivation to fall cultivation in some
plants (7). Also, thermal fluctuation can be the most
important cause of damage which can change during
short term daily or seasonal temperature conditions;
these factors that cause the greatest damage to crop
plants and their activated mechanisms show the least
level of tolerance to this fluctuation (8). Plants that
encounter these challenges lose their full genetic
potential for growth and reproduction. The changing
climatic conditions, as well as an increasing pressure
on global food productivity because of population
increase, results in a request for stress-tolerant crop
varieties (9). Therefore, realizing the reactions to a
mixture of stresses is crucial in producing broadspectrum crops that tolerate multiple stresses.
The simultaneous incidence of different stresses
can have positive or negative impacts on plants
depending on the nature and duration of the stresses
(10). In the following parts, the study will focus
on the negative and positive interactions by some
examples of stresses in plants. Then, the mechanisms
which play a role in stress interactions will be
explained such as hormone signalling, transcription
factors (TFs), reactive oxygen species (ROS), R-gene
resistance, and systemic acquired resistance.
Negative interactions
A high temperature increases the susceptibility
of plants to disease. In tobacco (Nicotiana tabacum)
and pepper (Capsicum annuum), a high temperature
suppresses the tolerance to Tobacco mosaic virus
(TMV) and Tomato spotted wilt virus (TSWV),
respectively (11). In a six-year experiment, results
showed that an increase in nocturnal temperature
caused severe spot blotch (Cochliobolus sativus)
(12). Low temperature combined with high light
decreases chlorophyll and b-carotene in two strains
of Dunaliella salina, indicating that these treatments
cause photooxidative stress. Such a status increases
the total ascorbate pool by 10–50% and the total
glutathione pool by 20–100% with no consistent
effect on their redox state (13). It has been reported
that heavy metals cause a higher detrimental effect
on plant growth when combined with other abiotic
stresses. Growth inhibition is observed in both the
shoot and root of pea seedlings by nickel (Ni) or
UV-B alone, and a more severe damage is observed
as a result of combined stresses (14). In plants under
high temperature stress, a hypersensitive response
(induced by R-genes) is also postponed against
virus attack (PVX and TMV) in potato and tomato
(15). Drought stress can also have similar effects
on plant pathogen resistance. In both common bean
and sorghum, treated plants by drought stress show
a greater susceptibility to the charcoal rot fungus
(Macrophomina phaseolina) (16). Similarly, drought
stress increases the spread of leaf scorch symptoms
caused by bacterial and fungal pathogens on date
palms and vine (17). So, biotic and abiotic stress
combinations can interact negatively and cause
damages to plants.
Positive interactions
Abiotic stresses may interact in a positive way
with biotic stresses. While cold temperatures are
lethal to most plants, winter annual and perennial
plants mostly survive due to the acclimation
process realized by the exposure of plants to low
but non-freezing temperatures (7). It can be related
to cold-responsive genes that encode for primary
and secondary metabolites like enzymes involved
in photosynthesis and respiration, carbohydrates,
lipids, regulatory and defence proteins (18,19).
Ascochyta blight is the most important disease
of the chickpea world-wide. This fungal disease
injures all the above ground biomass, leading to total
destruction of chickpea (20). According to Bahmani
and Maali-Amiri (2014), the existence of biotic and
abiotic cross tolerance in cold acclimated chickpea
against the ascochyta blight was confirmed. Under
acclimation conditions, a decrease in Electrolyte
Leakage Index (ELI) and Malondialdehyde (MDA)
proves that cold acclimation (11ºC for one week) of
chickpea genotypes induces tolerance to its fungal
pathogen (Ascochyta rabei). It seems that responses
to the acclimation temperature and cold stress induce
reprogramming in genome in transcriptional and
translational levels that are responsible for general
tolerance to Ascochyta blight. Similar mechanisms
might exist in other plants too (21). The positive
effect of cold on plant tolerance to disease was also
reported by Tronsmo et al. (2009) (22); they showed
increased resistance of Poa pratensis plants to
Puccinia poa-nemoralis when hardened at 1-8ºC for 2
weeks. They also reported cold-induced resistance of
several grass species to snow mould. Moreover, it has
been shown that short-term acclimation can induce
greater cold tolerance upon the increase of oxidative
stress in chickpea (23). In barley, salinity induces a
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significant tolerance to powdery mildew (24), and
drought can confer resistance to the fungal pathogen
(Botrytis cinerea) in tomato (25). Plant pathogens
may have positive impacts on plant tolerance against
abiotic stresses like drought. One of their mechanisms
to achieve this goal is stomatal closure in infected
tissues to decrease the shortage of water (26). Also,
the ability of herbivore (Spodoptera exigua) declines
for feeding on drought-stressed tomato leaf tissue
because as a result of the abiotic stress, they contain
secondary metabolites which have a defensive role
against this pest (27). In the potato, simultaneous
water stress and nematodes attack does not damage
the plants whereas they individually have negative
impacts on plant growth (28). A positive interactive
effect has also been reported for drought and
nematode infection (Meloidogyne graminicola) on
the rice (29).
Many bacteria and arbuscular mycorrhizal fungi
are known to increase stress tolerance in plants. They
produce antioxidants, stabilize soil structure, suppress
ethylene production, increase osmolyte production,
and improve abscisic acid (ABA) regulation (30).
Timmusk and Wagner (1999) (31) discovered that
useful microorganisms positively affected the crop
tolerance when they showed that plants treated with
the rhizobacterium (Paenibacillus polymyxa) had a
greater resistance to drought and further bacterial
attack, which was related to the expression of the
ERD15 gene (32,33).
A combination of salt and heat stresses provides
a significant level of protection against the effects of
salt stress alone in tomato plants (34); this protection
is caused by the accumulation of glycine betaine and
trehalose. Previous studies have shown that glycine
betaine has a crucial role in the protection of PSII
against photo- and heat-induced inactivation and
protection of cells against oxidative stress (35,36).
Hormone signalling pathway in stress interactions
Plant hormones may have a more important role
in signalling under stress. Therefore, understanding
the master regulator between the two major stresses
(abiotic and biotic) seems to be helpful. ABA is
central in the regulation of stress responses and is
considered a global adjuster that can allow plants to
respond to the most severe threats by recognizing
the priority of response to biotic or abiotic stresses
(Figure 1) (1). High concentrations of ABA, either
because of exogenous application or droughtinduced accumulation, affect plant disease resistance
(37). ABA has both negative and positive roles in
the plant response to pathogen infections. Its impact
depends on the duration of infection and the nature
of the pathogen (38). Higher levels of ABA in plants
suppress signalling mediated through salicylic acid
Figure 1: Interaction of biotic and abiotic stresses with plant hormones demonstrate the role of hormones in fine-tuning the responses between biotic and
abiotic stress encountered. Positive regulation is shown by solid arrows, while negative regulation or inhibition is shown by dashed bars. ABA abscisic
acid, JA jasmonic acid, SA salicylic acid, SAR systemic acquired resistance (1).
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Mahya Bahmani, Reza Maali-Amiri
(SA), jasmonic acid (JA) or ethylene and finally can
repress the expression of defence genes (39). ABA
acts through the SA signalling pathway as a chief
strategy to induce stomatal closure and therefore
declines infection in the primary stages of defence
against microbial invasion (40). After penetration,
ABA is vital for callose deposition induced by
β-amino-butyric acid (BABA); this phenomena is a
defensive mechanism against fungal pathogens (41),
whilst during bacterial infection ABA can block
callose production or indeed has a positive effect, a
balance that depends on the external environmental
factors such as light and glucose levels (42).
However, increased ABA levels arising from
abiotic stress conditions may repress the SA, JA,
and ethylene responses (43). JA hormone is also
activated by several biotic and abiotic stresses;
therefore, it seems to play a role in multiple stresses
because of pathways and secondary metabolites that
are synthesized by it. JA levels in plant tissues vary
with development, tissue type, and the presence or
absence of external stimuli (wounding, pathogens, or
mechanical). Kazemi-Shahandashti et al. (2013) (7)
reported that LOX activity may play an important
role in the mechanism of cold tolerance in chickpea,
because it synthesizes several secondary metabolites
such as JA in response to thermal treatments, not to
regulate cellular metabolism at optimum temperature.
In addition, the genes regulated by JA range from those
that encode proteinase inhibitors, fungal inhibiting
proteins, and enzymes in phytoalexin biosynthesis to
vegetative storage proteins and the large subunit of
ribulose bisphosphate carboxylase. The variation in
responses and genes regulated by JA demonstrates the
existence of multiple levels of control over jasmonate
biosynthesis and that JA acts with other effectors to
potentiate gene expression. In the soybean, in leaves
that were stressed by losing 15% of their fresh
weight, JA levels increased 5-fold within 2 hours
and declined to approximately the control levels by
4 hours (44). JA production can contribute positively
to tolerance against certain abiotic stresses such as
chilling, salt, drought and osmotic stress (45). On the
other hand, SA is known to obstruct the abiotic stress
signalling, leading to drought susceptibility in maize
when applied exogenously (46).
Transcription factors (TFs) in stress interactions
A TF, sometimes called a sequence-specific
DNA-binding factor, controls the rate of transcription
of genetic information from DNA to mRNA. TFs
are of great importance in producing specificity in
stress responses and they control a vast range of
downstream events. Genetic manipulations of TFs in
plant genotypes can be considered one of the most
significant opportunities for generating multiple
stress tolerant plants according to this fact that these
TFs can induce several downstream genes involving
in response to biotic and abiotic stresses (47).
Classification of TFs may be on the basis of their 1)
mechanism of action; 2) regulatory function; and 3)
sequence homology (and hence structural similarity)
in their DNA-binding domains.
MYC2 (also called JIN 1) has a central role for
interaction between biotic and abiotic signalling
pathways (48). It specifically regulates JA-induced
defence genes in a positive way but represses genes
induced by combined JA/ethylene signalling (49).
The MYB family a big, functionally diverse group
of TFs participates in regulating plant responses to
simultaneous biotic and abiotic stresses, specifically
the regulation of pathways that leads to biosynthesis
of phenylpropanoid (50). A member of this family,
MYB96, is induced by drought and stimulates
ABA-dependent stress tolerance by triggering the
biosynthesis of cuticular wax. MYB96 also stimulates
ABA-dependent SA biosynthesis, leading to PR
gene expression and defence mechanisms against
biotic stresses, performing as a connection between
these two hormones in achieving broad-spectrum
stress tolerance (51). In the MYB family of TFs,
there are conserved cysteine residues; it is assumed
that the MYB activity might be controlled by cellular
redox status (50) so that oxidative processes induced
by reactive oxygen species (ROS) can lead to the
oxidation or sulfur-nitrosylation of cysteine residues,
affecting DNA-protein interactions (52).
Another family of TFs are WRKY family, and one
of its members (WRKY-45) is induced by ABA, SA,
NaCl, mannitol, dehydration, cold, heat, Pyricularia
oryzae, and Xanthomonas oryzae stimuli. WRKY-45
overexpression could increase pathogen resistance
in the rice and Arabidopsis and induces ABAresponsive abiotic stress tolerance genes (53). In
Arabidopsis, another TF, ZAT7, induces salinity, heat,
oxidative stress, heat, and wounding that suppresses
a repressor of defence responses to a vast range of
stresses, including WRKY70, a mediator between JA
and SA signalling (54). Recent discoveries indicate
that TFs may be appropriate aims for developing
broad-spectrum tolerance in crops through genetic
engineering (47).
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Reactive oxygen species (ROS) in stress interactions
Due to the toxic nature of ROS, they can
induce various manifestations of damage to cell
macromolecules such as nucleic acids (DNA and
RNA), proteins, lipids, and carbohydrates. At
the whole plant level, these damages can cause
reduction of photosynthesis, impaired translocation
of assimilates, and reduced carbon gain, leading
to altered growth and reproduction (23). ROS has
special properties that enable them to play as signal
components involved in the induction of gene
expression and genome reprogramming. Also, due to
the bilateral function of these molecules, a regulatory
network for balancing the roles of ROS is necessary
in plants to control the interplay between defence
and damage pathways. These factors determine the
degree of tolerance to biotic and abiotic stresses.
ROS generation can be triggered by several factors,
providing the plant with oxidative stress conditions.
Enzymatic and non-enzymatic antioxidants play an
important role in plant defence mechanisms against
environmental stresses. A well-known phenomenon
among plants in response to various oxidative stresses
is proline accumulation that enhances antioxidant
defence systems (Figure 2) (7). Accumulation of
proline seems to have several roles under osmotic
stress conditions such as protection of the cellular
functions by ROS scavenging, and stabilization of
proteins, membranes and sub-cellular structures (55).
Numerous studies have demonstrated that signal
transduction, cellular defence, reprogramming of gene
expression and metabolism control may be elucidated
by the cellular redox state (56). Pentatricopeptide
repeat protein for germination on NaCl (PGN) is a
lately discovered gene that outstands the role of ROS
in response to the interaction between biotic and
abiotic stresses. It is assumed that the regulation of
ROS homeostasis in the mitochondria takes place by
PGN through interacting with genes like alternative
oxidase 1 (AOX1) (57). APX appears to be central
in the redox regulation leading to programmed cell
death (PCD). Decreased activity of APX isoforms is
observed in heat-induced PCD; APX isoforms are also
commonly up-regulated under abiotic stress. Redox
changes and post-translational modifications appear
to be integral in priming for stress tolerance after
exogenous application of chemicals. This provides a
potential explanation of the mechanism of action of
diverse chemicals in plant defence sensitization.
By realizing that the pattern of defence
mechanisms are similar in all environmental
stresses, it seems that a combination of stresses can
inducesgeneral and specific defence systems through
induction of tolerance against environmental stresses.
The best candidates for generating broad-spectrum
stress tolerant species can be provided by identifying
Figure 2: Convergence of various biotic and abiotic stress stimuli onto plant defence response via reactive oxygen species (ROS) as a
common factor, leading to activation of antioxidant defence genes (7).
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Mahya Bahmani, Reza Maali-Amiri
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master regulators of ROS metabolism.
R-gene resistance and systemic acquired resistance in
stress interactions
Resistance genes are genes that act as a potential
tool in defence mechanisms of plants, especially in
response to fungal stresses. Successive counteracting
suppression of defence responses by pathogens
through secretion of effector proteins makes plant
immune system (58). Identification of the effectors by
corresponding R-genes relating to NB-LRR protein
family or the impact of the effectors on intracellular
host proteins (guarded proteins) causes effectortriggered immunity (ETI). The ETI regulation
complexity is determined through network analyses
of individual and combined hormone mutants, which
reveals compensatory interactions in opposite of
synergistic interaction observed in PTI (PAMPtriggered immunity) and that can explain the sturdiness
of ETI to genetic disturbance. This robustness may
be ideal in building tolerance to combinatorial stress
through pyramiding R-genes with genes conferring
abiotic stress tolerance (59). On the other hand, it is
clear that there are multiple points of regulation at
the NB-LRR protein level that are essential for the
deployment of R-gene resistance (60). They include
partial regulation of NB-LRR accumulation in
cellular compartments (e.g. the nucleus). Reduction
of nuclear NB-LRR accumulation has been shown
to be responsible for the heat stress at attenuation of
disease resistance conferred by the proteins SNC1
and RPS4 in Arabidopsis (61). In Arabidopsis and
tobacco, treatment with ABA results in the repression
of systemic acquired resistance (SAR) that begins
by SA induction; moreover, ABA treatment prevents
the synthesis and accumulation of compounds that
participate in defence mechanisms like lignins
and phenylpropanoids (62). Kim et al. (2014) (63)
studied the resistance genes linked to both heat and
fungal stresses and reported that high temperature
conditions affected plant disease development by
attenuating plant disease resistance while promoting
pathogen growth. The phenotypes of several lesionmimic mutants of Arabidopsis thaliana, that are
caused through mis-regulated R genes are suppressed
by environmental hints (64), recommending the
existence of crosstalk between R-gene mediated
disease resistance responses and abiotic stress
responses. Moreover, the abundance of the barley’s
R proteins MLA1 and MLA6 is reduced specially
within several hours of a temperature shift from 18ºC
to 37ºC, without any reduction in MLA1 and MLA6
abundance (65).
Conclusion
Plants have improved special mechanisms that
allow them to sense and respond to individual or
multiple environmental stresses. This phenomenon
that is still an important challenge in research is
known as cross tolerance. As plants have limited
resources that must be balanced between growth and
defence against stresses, both natural and induced
stress tolerance often come with a growth or yield
penalty, making it agriculturally disadvantageous.
By realizing that the pattern of defence mechanisms
are similar in all environmental stresses, it seems
that a combination of stresses can induce general
and specific defence systems through changing the
Table 1. Negative or positive interactions of stress combinations
Plant
References
Nutrient
UV
Positive/negative
interactions
Negative
Positive
Arabidopsis
Arabidopsis
(66)
Heat
Negative
Wheat
(12)
Heat
Negative
Tobacco
(15)
Salinity
Positive
Barley
(24)
Pathogen (fungal)
Cold
Positive
Chickpea
(21)
Herbivore (insect)
Drought
Positive
Tomato
(27)
Pathogen (viral)
Drought
Positive
Sugar beet
(32)
Pathogen (nematode)
Drought
Positive
Rice
(68)
Biotic stress
Abiotic stress
Pathogen
Pathogen
Pathogen (fungal)
Pathogen (bacterial &
viral)
Pathogen (fungal)
(67)
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Cross tolerance in plants and genetic regulation
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first and secondary metabolites following genome
reprogramming (Table 1). The best candidates for
generating broad-spectrum stress tolerant species can
be provided by identifying master regulators of ROS
metabolism. The antioxidant defence machinery
is one of the important pathways that seems to be
the basis of plants tolerance to stress combinations.
Recent investigations have showed the connection
of higher antioxidant capacity or lower ROS
accumulation with plant cross tolerance. It may be
more beneficial to focus on producing cross tolerant
crops with high photosynthesis, growth rates, and
yield rather than developing crops that can survive
under extreme stress events. The response of plants
to different stress combinations might be regulated
by the coordination of different pathways and
signals like hormone signalling pathways, TFs, and
R-genes. Therefore, by using novel biotechnological
approaches, breakdown of resistance due to evolving
pathogens can be reduced. Our knowledge of the
molecular and biochemical mechanisms that regulate
the responses of plants to stress combinations is still
very limited and further studies are required to address
these mechanisms. The challenge for plant scientists
in the 21st century will be to improve stable multiple
stress tolerant traits in agronomically important crops
to improve yields, particularly in areas with adverse
environmental conditions in order to contribute to the
global food security.
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