Plant Immune System Nejat and Mantri

Curr. Issues Mol. Biol. (2017) 23: 1-16. caister.com/cimb

Plant Immune System: Crosstalk Between

Responses to Biotic and Abiotic Stresses the
Missing Link in Understanding Plant Defence

Naghmeh Nejat* and Nitin Mantri* identification of new targets and development of
novel methods to combat biotic and abiotic stresses
School of Science, Health Innovations Research under global climate change.
Institute, RMIT University, Melbourne, Victoria,
Australia Introduction
Biotic and abiotic stresses, as a part of the natural
*Corresponding authors: [email protected]; ecosystem, seriously impact crop productivity and
[email protected]; threaten global food security. Plants in their natural
habitats are persistently and simultaneously
DOI: http://dx.doi.org/10.21775/cimb.023.001 confronted with a range of biotic (e.g. biotrophic and
necrotrophic fungi, bacteria, phytoplasmas,
Abstract oomycetes and nematodes, and non-cellular
Environmental pollution, global warming and climate pathogens i.e. viruses and viroids) and abiotic
change exacerbate the impact of biotic and abiotic stress factors (such as heat, cold, drought, salinity,
stresses on plant growth and yield. Plants have mechanical wounds, high light intensity, freezing,
evolved sophisticated defence network, also called heavy metals and metalloids; Mantri et al. 2014).
innate immune system, in response to ever-
changing environmental conditions. Significant Plants have evolved a plethora of complex immune
progress has been made in identifying the key response pathways which enable them as sessile
stress-inducible genes associated with defence organisms to survive not only specific stresses but
response to single stressors. However, relatively also a combination of stresses (Nejat et al. 2015).
little information is available on the signaling Plant-biotic and/or abiotic stress interactions trigger
crosstalk in response to combined biotic/abiotic a wide range of defence reactions at molecular and
stresses. Recent evidence highlights the complex cellular levels to ensure that plant cells are insulated
nature of interactions between biotic and abiotic from the challenges they encounter (Kim et al.
stress responses, significant aberrant signaling 2014) (Figure 1).
crosstalk in response to combined stresses and a
degree of overlap, but unique response to each A sophisticated defence network is activated to
environmental stimulus. Further, the results of orchestrate transcriptional reprogramming using a
simultaneous combined biotic and abiotic stress two-tiered defence approach (Dodds and Rathjen
studies indicate that abiotic stresses particularly 2010; Tsuda and Katagiri 2010). Pathogen/microbe
heat and drought enhance plant susceptibility to associated molecular patterns (PAMP/MAPM)-
plant pathogens. It is noteworthy that global climate triggered immunity (PTI) is the first line of defence. It
change is predicted to have a negative impact on is a general and non-specific defence response and
biotic stress resistance in plants. Therefore, it is vital provides basal resistance not only against entire
to conduct plant transcriptome analysis in response classes of microbial pathogens but also abiotic
to combined stresses to identify general or multiple stresses. PTI constitutes the inducible defence
stress- and pathogen-specific genes that confer through an array of early cellular responses
multiple stress tolerance in plants under climate comprising of ion flux across the membrane,
change. Here, we discuss the recent advances in production of reactive oxygen species (ROS) and
our understanding of the molecular mechanisms of mitogen-activated protein kinase (MAPK) cascades
crosstalk in response to biotic and abiotic stresses. phosphorylation and long-term later responses that
Pinpointing both, common and specific components induce callose deposition (Nakagami et al. 2005;
of the signaling crosstalk in plants, allows Dodds and Rathjen 2010; Tsuda and Katagiri 2010;

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Plant Immune System Nejat and Mantri

High salinity
Drought
Heat Fungi and Oomycetes
Bacteria and
Abiotic stresses Cold Biotic stresses Phytoplasmas
High or low osmolarity
Wounding (Pathogens) Viruses
Ozone
UV

Ca2+ channels O2 O2 .-
Apoplast
PRRs
Signal perception
ROS
NADPH oxidase (H2O2)
RBOHD
Cytosol
ABA
Phosphorylation
Protein phosphatase
Stomatal closure
MAPKKK

Plasma membrane
WRKY
MYC Defence against (hemi) biotrophs
MYB Transcription factors MAPKK
NAC activation
DREB
AP2/ERF MAPK
Nucleus

NF-Y Gene expression

bZIP
Zing fingers Defence against necrotrophs/
mRNA herbivorous insects

Response protein

Figure 1. The overall model of plant immunity in response to biotic and abiotic stresses. Perception of pathogen-associated molecular patterns (PAMPs),
sensing abiotic stress and/or any extracellular signals by surface-localised pattern recognition receptors (PRRs) trigger phosphorylation of the RBOHD
(respiratory burst oxidase-D) and activate the NADPH oxidase RBOHD for rapid production of reactive oxygen species (ROS) in calcium-independent or -
dependent manner, which subsequently trigger mitogen-activated protein kinase (MAPK) phosphorylation as general defence response. MAPK transduce
extracellular signals to nucleus leading to activation of transcription factors that regulate immunity gene expression. There is antagonistic and synergistic
crosstalk between hormone signal transduction pathways in response to various attackers. ABA: abscisic acid; SA: salicylic acid; JA: jasmonic acid; ET:
ethylene.

Schwessinger et al. 2015). Defence-related response that is specific to the pathogen infection. It
phytohormones comprise salicylic acid (SA), is activated by resistance (R) genes when pathogen
jasmonic acid (JA), ethylene (ET) and abscisic acid virulence factors, called effectors, are released into
(ABA) as the core immune signaling components. plant cells (Cui et al 2015). If the first line of
They are produced in response to both, biotic and inducible non-specific defence, so-called PTI, is
abiotic stresses (Dodds and Rathjen 2010; Tsuda successfully overcome by pathogens through
and Katagiri 2010). Among those, ROS, MAP- suppression of PTI response, then the second line
kinase cascades and hormone signalling pathways of plant immunity is activated to produce defence
are of paramount importance as they lead the proteins that cause programmed cell death. This is
defence responses to biotic and abiotic stresses also referred to as the hypersensitive response (HR)
(Nakagami et al. 2005; Fujita et al. 2006; Atkinson (Thomma et al. 2011).
and Urwin 2012; Kissoudis et al. 2014; Perez and
Brown 2014; Schwessinger et al. 2015) (Figure 2). Hence, after stress recognition, the immune system
Therefore, the authors propose that PTI which is triggers a wide range of defence mechanisms to
activated either by PAMP or MAPM is the "stress- orchestrate transcriptional reprogramming through
triggered immunity" as it has evolutionary conserved receptor proteins, signal transduction cascades,
molecular signatures across similar types of kinase cascades, reactive oxygen species, hormone
microbes or abiotic stresses. signaling pathways, heat shock proteins, and
transcription factors to protect plants against
The effector-triggered immunity (ETI) is the second, different attackers (Figure 1). However, recent
prolonged and robust layer of plant immune advances suggest significant aberrant signaling

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Plant Immune System Nejat and Mantri

Microbial PAMPs Generation of reactive

oxygen species (ROS)

Pattern-triggered
immunity response Hormone signaling
(PTI) ABA, SA, JA, ET, GA
Abiotic Stresses:
Heat, Cold,
Drought, Salinity, Mitogan-activated protein
Heavy metals (MAP) kinase cascades

Figure 2. Activation of the first line of defence in a non-specific approach. ABA: Abscisic acid; SA: Salicylic acid; JA: Jasmonic acid; ET: Ethylene; GA:
Gibberellins.

crosstalk in plant immune response to a Atkinson 2011; Prasch and Sonnewald 2013;
combination of biotic and abiotic stresses compared Sewelam et al. 2014; Kissoudis et al. 2015).
with an individual stress (Atkinson et al. 2013;
Prasch et al. 2013; Suzuki et al. 2014). In this Study of the molecular response of A. thaliana to
review, we discuss the major factors affecting the concurrent drought stress and plant-parasitic
signaling pathways in response to single and nematode, Heterodera schachtii, infection using
combined stresses, their common and overlapping microarrays revealed that drought stress increased
responses, and the crosstalk between signaling the susceptibility of A. thaliana to nematode
pathways in response to biotic and abiotic stresses. infection. Moreover, induction patterns of
differentially expressed genes following these stress
Crosstalk between responses to environmental treatments displayed not only a specific response to
stimuli in the post-genome era each stress but also a particular response that was
Plant responses to biotic and abiotic stresses uniquely activated by the combination of biotic/
involve complex signaling pathways. Increasing abiotic stress (Atkinson 2011).
evidence suggest that there is significant overlap
and several defence genes are commonly involved Similarly, combined heat and drought stress
in response to multiple biotic and abiotic stresses as increased the susceptibility of Arabidopsis plants to
shared or general stress-responsive genes (Table 1) Turnip mosaic virus infections through suppression
(Massa et al. 2013; Mantri et al., 2010; Narsai et al. of defence responses to the biotic stress (Prasch
2013; Shaik and Ramakrishna 2013; Sham et al. and Sonnewald, 2013). Further, salt stress
2014,2015; Zhang et al. 2016). Nevertheless, in significantly increased the susceptibility of tomato
response to combination of stresses, plants plants to powdery mildew (Kissoudis et al. 2015).
orchestrate extensive transcriptional reprogramming
and exhibit a unique program of transcript response In 2010, Mantri et al. analysed the chickpea
that is not similar to that of either stresses transcriptome in response to drought, cold, high-
individually, although there is significant overlap in salinity and the necrotrophic fungal pathogen
response pathways to combined environmental Ascochyta rabiei using 768-feature boutique
stresses (Mantri et al. 2010; Atkinson 2011; Prasch microarray. Their results showed that A. rabiei and
and Sonnewald 2013; Rasmussen et al. 2013; high salinity which were both studied at the seedling
Sham et al. 2015). Several studies revealed stage, shared the highest number of deferentially
crosstalk between responses to combined stress expressed transcripts and to a lesser extent
treatment synergistically or antagonistically. Of note, between A. rabiei and cold, and A. rabiei and
abiotic stresses have a negative impact on biotic drought which were studied at flowering stage.
stress resistance and can lead to enhanced plant Further, 51 transcripts were differentially expressed
susceptibility to biotic stresses (Wang et al. 2009; in the shoot tissues in response to A. rabiei, of
which 21 transcripts were commonly differentially

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Plant Immune System Nejat and Mantri

Table 1.to biotic and abiotic stresses in various plant species.

Table 1. Key genes responsive

Gene Plant species Stressors Function References

HSPs A. Thaliana Biotic, drought, salinity, heat, stabilize Sham et al. 2014; 2015;
osmotic↑; Nematode & proteins Ma et al. 2007;
drought↓; Rasmussen et al. 2013;
Sewelam et al. 2014;
Atkinson 2011;
ABA A. Thaliana Drought, cold, salinity, cold, Defence against Seki et al. 2002; Kreps et
osmotic↑ abiotic stresses al. 2002
Ethylene A. Thaliana Drought, cold, salinity↑ Defence signals Seki et al. 2002
biosynthesis genes
Senescence-related A. Thaliana Nematode, virus, heat & Defence signals Atkinson 2011; Prasch &
genes drought↑; Sonnewald 2013; Kreps
et al. 2002
PR proteins A. Thaliana Virus & heat↓; Resistance Prasch & Sonnewald
2013;
Photosynthesis- C. arietinum, Biotic (Fungi, bacteria, virus, decreased Mantri et al. 2010,
related genes A. Thaliana, O. nematodes), drought, cold, metabolic rate Prasch & Sonnewald
sativa salinity, heat↓; Xanthomonas 2013; Shaik &
oryzae & drought↑ Ramakrishna 2013;
Atkinson 2011; Zhang et
al. 2015; Narsai et al.
2013
Cytochrome p450 A. Thaliana Nematode & drought ↓; Bacteria, cell wall Atkinson 2011; Narsai et
fungi, drought, salt & heat ↑&↓ reinforcement al. 2013, Shaik &
Ramakrishna 2013;
Peroxidase A. Thaliana, O. Biotic, cold, drought↓ generating Narsai et al. 2013; Shaik
sativa H2O2 & Ramakrishna 2013;

Abbreviations: nd: not determined; ↑: up-regulated; ↓: down-regulated; ↑&↓: some

members were up-regulated, some were down-regulated.

expressed among the fungal pathogen and one or al. 2013). Their results exhibited that Pathogen-
more of the abiotic stresses, while no transcript was related genes are more specifically induced than
commonly regulated across all the four stresses abiotic- and hormone-related genes and hormones
assessed. and abiotic stresses share proportionately more
differentially expressed genes than each does with
In A. thaliana, Sham et al. using microarray mRNA the biotic stress. Further, a weighted gene co-
expression profiling found that the genes regulated expression network analysis revealed that 50% of
in response to Botrytis cinerea were more similar to the differentially expressed genes were not specific
those induced by osmotic stress than genes and expressed in response to two or more stress
differentially expressed in response to heat and salt conditions, whilst the 50% remaining were stress-
stresses. Conversely, 13 stress-inducible and 29 specific genes that were only regulated in response
stress-repressible genes were responsive to all four to single environmental factor (Massa et al. 2013).
stresses (Sham et al. 2015). In 2013, in-depth The results of this study exhibited a degree of
transcriptome analysis of potato (Solanum overlap in the defence response to pathogen
tuberosum L.) using RNA-Seq was conducted in infection and abiotic stresses, but a unique
response to biotic stress, potato late blight fungus response to each environmental stress.
(Phytophthora infestans), several abiotic stresses
i.e. salinity, drought, and heat, and plant hormone Further, Weston et al. 2011 using a weighted gene
treatment (abscisic acid, 6-benzylaminopurine, co-expression network approach found that heat
gibberellic acid, and indole-3-acetic acid (Massa et shock proteins respond to heat stress in a species-

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Plant Immune System Nejat and Mantri

specific manner. A gene co-expression network and transported to the plasma membrane via the
analysis of 1094 microarrays of Arabidopsis using a secretory pathway (Frescatada-Rosa et al. 2015).
non-target approach revealed that genes involved in PRRs have been classified into receptor-like
photosynthesis, protein synthesis and response to kinases (RLKs) and receptor-like proteins (RLPs)
oxidative stress are also largely involved in containing extracellular ligand-binding domains that
response to environmental stresses (Mao et al. perceive a wide range of extracellular signals such
2009). as PAMPs and abiotic stresses. They trigger the
downstream intracellular stress signaling cascades
Another study indicated that the course of day by phosphorylation of intracellular serine/threonine
affected transcriptome response of the plant to kinase domains (Osakabe et al. 2013; Zipfel 2014;
drought and the response can vary with the time of Trdá et al. 2015). RLKs form one of the largest gene
day (Wilkins et al. 2010). In addition, responses of superfamily in the genomes of different plant
different plant species to drought is not just affected species with 610 and 1131 members in Arabidopsis
by the time of day but also clone history and and rice, respectively (Gish and Clark 2011). They
location (Raj et al. 2011). The authors investigated are classified into 44 subfamilies including lysine
the impact of individual environmental history on motifs, lectin, epidermal growth factor-like repeats,
response to drought stress and their results showed self-compatibility domain (S-domain), wall-
that differences in transcript abundance patterns in associated kinase (WAK) and leucine-rich repeats
response to drought was based on differences in (LRRs) (Frescatada-Rosa et al. 2015; Trdá et al.
geographic origin of clones, suggesting the interplay 2015). The latter constitute the largest group of
between genotype and environment. RLKs in plants which play essential roles in a wide
range of processes governing growth and
Therefore, the level of crosstalk between different development as key regulators, grain yield
defence response pathways and plant immune components improvement, hormone perception,
responses to single stresses and the combination of initiating innate immune defence at front-line against
different environmental stimuli depend upon several microbial pathogens and adaptation to abiotic
factors such as plant species, tissues, develop- stresses (Osakabe et al. 2013; Macho and Zipfel
mental stage, stressors, stress intensity, time series, 2014; Zou et al. 2015).
time of day, geographic origin, etc. (Wu et al. 2009;
Mantri et al. 2010; Skibbe et al. 2010; Cramer et al. The role of LRR-RLKs in pathogen sensing and
2011; Weston et al. 2011; Massa et al. 2013; Shaik activation of downstream defence responses has
et al. 2013; Asai and Shirasu 2015; Li et al. 2015; been reviewed in depth lately (Macho and Zipfel
Pandey et al. 2015). Further, these data 2014; Frescatada-Rosa et al. 2015; Trdá et al.
demonstrate the complex nature of interactions and 2015). Despite, there is growing evidence indicating
exhibit that the complex mechanisms comprising that RLKs can have positive and negative regulatory
overlap and specific signaling pathways fine-tune role in both biotic and abiotic stress response
plant responses. (Tanaka et al. 2012; Zhao et al. 2013; Jun et al.
2015).
Collectively, multi-parallel single stress along with
the combination of single stresses require to be Recent studies revealed that GbRLK, a receptor-
investigated at spatial and temporal resolution, as like kinase (RLK) gene, involved in response to
comparative spatiotemporal gene expression both biotic and abiotic stresses is a positive
analysis, to identify a unique response modulated regulator. GbRLK increased salinity and drought
by combined stress. Here, we discuss the recent stress tolerance through reduction of water loss
advances in the understanding of the mechanisms rate in leaves and increased sensitivity to ABA and
underlying plant immunity, at the molecular level, enhanced tolerance to Verticillium wilt in GbRLK
against biotic and abiotic stresses and the latest transgenic cotton and Arabidopsis lines (Zhao et al.
findings on the signaling crosstalk in response to the 2013; Jun et al. 2015). In recent past, Jun et al.
combination of biotic and abiotic stresses. used transgenic GbRLK cotton and Arabid-opsis
lines to reveal that overexpression of GbRLK
Receptor proteins as frontline defence modulated expression of several genes involved in
Plant pattern-recognition receptors (PRRs) as a biotic and abiotic stresses and suggested that the
frontline of the immune system are an extremely increased resistance to Verticillium dahliae
diverse family of cell surface-localized receptors. infection in transgenic plants could be a result of
They are synthesized in the endoplasmic reticulum reduction in the water damage losses and

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Plant Immune System Nejat and Mantri

regulation of defence-related gene expression (Jun

et al. 2015). These findings suggest that GbRLK The Arabidopsis BOTRYTIS SUSCEPTIBLE 1
could possibly be a key regulator of both, biotic and (BOS1) gene encoding an R2R3MYB transcription
abiotic signaling. factor conferred resistance to pathogens and
tolerance to salt and drought abiotic stress factors
In another study, ABA and osmotic stress signal through a JA-mediated defence signaling pathway.
transduction in A. thaliana is negatively regulated by BOS1-deficient mutant bos1 displayed increased
a receptor-like cytosolic kinase (RLCK) gene, susceptibility to necrotrophic fungi B. cinerea and
ARCK1, that encodes a cytosolic protein kinase Alternaria brassicicola and biotrophic bacterial
belonging to the RLCK family and cysteine-rich pathogen Pseudomonas syringae and impaired
repeat (CRR) RLK sub-family (Tanaka et al. 2012). tolerance to abiotic stresses salinity, drought and
The arck1 knockout mutant showed higher oxidative stress (Mengiste et al. 2003). The results
sensitivity to ABA and osmotic stress than the wild- of this study indicate that MYB TFs play essential
type. Microarray analysis using CRK36 RNAi roles in multiple stress responses.
transgenic plants exhibited significantly increased
ABA-responsive gene expression. CRK36 is Functional studies of the Arabidopsis Botrytis
another member of the CRR RLK sub-family that Susceptible1 Interactor (BOI) and three BOI-
interacts with ARCK1 to form a complex to fine-tune RELATED GENES (BRGs) encoding a subclass of
defence responses against abiotic stresses and RING E3 ligases have revealed that BOI interacts
adjust growth via hormone signaling according to with BOS1 and ubiquitinates it to confine the extent
the growth phase. Hence, ARCK1 is not involved in of cell death induced by pathogens and abiotic
the suppression of ABA-responsive genes per se stresses (Luo et al 2010). B. cinerea and salt
(Tanaka et al. 2012). induced the expression of BOI but its expression
was intriguingly suppressed by gibberellins. BOI
As discussed, RLKs are multifunctional receptors RNA interference (RNAi) plants showed more
which are involved in regulation of plant responses susceptibility to fungal pathogen and salt stress and
to both, biotic and abiotic stresses. Altogether this reduced growth responsiveness to gibberellin.
suggests a conserved mechanism for signal Hence, BOI and BRGs are associated with
perception and activating downstream signaling resistance to both, biotic and abiotic stresses via
networks, hence PRRs could be signal recognition suppression of cell death which is different from HR
receptors (SRRs). However, a mechanism for cell death mediated by the disease resistance
crosstalk of signal perception in response to genes RPM1 and RPS2 (Luo et al 2010). This
environmental stimuli remains to be addressed. finding suggests that the expression of BOI gene is
complex and regulated by multiple factors and there
Transcription factors is hormonal crosstalk between JA and GA to
Transcription factors (TFs) include members of the regulate the expression of BOS1. Further, GA may
APETALA2/ETHYLENE-RESPONSE ELEMENT act as a negative regulator of BOI. However, more
BINDING FACTOR (AP2/ERF), basic-helix-loop- comprehensive analysis is required to dissect the
helix (bHLH), basic domain leucine zipper (bZIP), complex interacting pathways with cross-talk at
MYB, NAC and WRKY families (Ford et al. 2015). different levels.
TFs are the central core of the gene regulatory
networks and precisely modulate the transcription A transcription factor of the NAC family, one of the
rate through either repression or activation of gene largest TFs family that is only found in plants,
expression. They are multi-functional and mediate Arabidopsis thaliana activating factor1 (ATAF1) is
diverse aspects of developmental processes and induced in response to various biotic and abiotic
responses to various biotic and abiotic stimuli in stresses. ATAF1 is drought-inducible gene and it
plants (Tsuda and Somssich 2015). was significantly expressed in an ABA-deficient
mutant aba2 in response to drought and high
Carrera et al. 2009 performed a gene co-expression salinity, demonstrating that ATAF1 expression is
network analysis of 1,436 microarray experiments of ABA-independent. ATAF1 is also involved in
Arabidopsis using InferGene software. Their results stomatal regulation and extensively expressed in
showed that several TFs were the most central stomatal guard cells (Lu et al. 2007; Wu et al. 2009).
regulatory hubs including KAN3 involved in auxin, Therefore, ATAF1 may augment plant drought
MYB29 in gibberellin, MYB121 in abscisic acid, and tolerance by stomatal closure via both ABA-
ERF1 in ethylene responses. dependent and ABA-independent signaling pathway.

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Plant Immune System Nejat and Mantri

On the other hand, ABA biosynthesis aldehyde Moreover, ATAF1 knockout mutant positively
oxidase gene (AAO3) was induced in ataf1 mutant regulates the expression of several stress-
plants upon biotrophic powdery mildew fungal responsive genes such as COR47, ERD10, KIN1,
pathogen Blumeria graminis f.sp. hordei (Bgh) RD22 and RD29A under drought stress (Lu et al.
infection and compromised penetration resistance 2007; Wu et al. 2009). By contrast, overexpression
towards Bgh (Jansen et al. 2008). By contrast, ABA of ATAF1 in transgenic plants ATAF1-OE increased
biosynthesis-deficient mutant was highly resistant to susceptibility to B. cinerea, Alternaria brassicicola,
attempted Bgh penetration. These data suggest that and P. syringae pv. Tomato, whilst ATAF1 chimeric
ATAF1 is a stimulus-dependent transcriptional repressor construct enhanced disease resistance to
regulator of ABA biosynthesis and ABA is a negative these pathogens via up-regulation of pathogenesis-
regulator of penetration resistance. Moreover, the related (PR) genes, PR-1 and PR-5, and JA/ET-
expression of JA/ET-activated transcription of plant mediated defence responsive gene plant
defensin genes was suppressed in ataf1 mutants defensin1.2 (PDF1.2) (Lu et al. 2007). In line with
whereas induced in the wild-type plants (Jansen et this, Prasch and Sonnewald found that the
al. 2008). Further, barley ATAF1 homologue expression of PR genes and R genes-mediated
HvNAC6 is also a positive regulator of basal disease resistance was suppressed and virus
defence and offers penetration resistance towards resistance was compromised in virus infected A.
virulent Bgh attack (Jensen et al. 2007) (Figure 3). thaliana under simultaneous double drought and
heat stress, whereas PR1, PR2, and PR5 were
Collectively, ATAF1 as a point of crosstalk, play a induced in response to single virus infection (Prasch
critical role in the regulation of antagonistic interplay and Sonnewald, 2013).
between ABA- and JA/ET-mediated signaling and
regulates the inhibitory effect of ABA on JA/ET- Therefore, these studies corroborate that ATAF1 is a
activated transcription of plant defensin genes to repressor of basal defence and negative regulator of
enhance plant tolerance in response to biotrophic disease resistance, which seems to be ABA-
fungus. mediated, in response to both, necrotrophic fungi

CATGTG

Figure 3. A schematic representation of transcriptional regulatory networks of NAC transcription factors in biotic and abiotic stresses responses.

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Plant Immune System Nejat and Mantri

and biotrophic bacterial pathogen through wide variety of environmental stimuli to protect cells
repression of PRs (Wang et al. 2009). against stress by preventing protein aggregation
and stabilizing misfolded proteins and cellular
Recently, a novel role has been identified for ATAF1 homeostasis (Wang et al. 2004). Recent findings
as a positive regulator of senescence via activating reveal that over-expression of OsHSP18.6
senescence-promoting TF ORESARA1 (AtNAC092) augmented tolerance to diverse types of abiotic
and repressing MYB transcription factor GOLDEN2- stresses including heat, drought, salt and cold in
LIKE1 (GLK1) by directly binding to their promoters rice (Wang et al. 2015). In addition, genes encoding
(Garapati et al. 2015). These findings demonstrate HSPs were induced in Arabidopsis by necrotrophic
that ATAF1 is a multifaceted TF with versatile fungus Botrytis cinerea infection, cold, drought and
capabilities and plays an important role in mediating oxidative stress (Sham et al. 2014). Therefore,
crosstalk between biotic and abiotic stress HSPs may regulate pathogen defence as well as
responses, though further research is required to abiotic stress tolerance.
unravel the role of senescence-associated genes in
defence response and the correlation between The transcription of HSPs is primarily regulated by
ATAF1, hormone signaling, and disease resistance. heat shock transcription factors (HSFs) which bind
to highly conserved motifs of the promoter regions
The OsNAC6 gene, another member of the NAC of HSP genes known as heat stress-elements
family which has high similarity to genes in the ATAF (HSEs; 5′ -AGAAnnTTCT-3′) resulting in increased
subfamily is a positive regulator of defence in tolerance to biotic and abiotic stresses (Hu et al.
response to both, biotic and abiotic stresses 2015; Virdi et al. 2015). Recently, genome-wide
(Nakashima et al. 2007). OsNAC6 was induced by transcriptional analyses in a number of plants have
cold, drought, high salinity, wounding, ABA, JA, and shown that HSFs have an integral role in response
blast disease in rice (Ohnishi et al. 2005; to biotic and abiotic stresses such as heat, cold,
Nakashima et al. 2007; Takasaki et al. 2010). salt, drought and oxidative stress (Chung et al.
Transgenic rice plants over-expressing OsNAC6 2013; Xue et al. 2015). For instance, several HSF
exhibited enhanced tolerance to drought and high genes were significantly induced in strawberry
salinity and some tolerance to hemibiotrophic fungal Fragaria vesca by heat, drought, cold, and salt
pathogen Magnaporthe oryzae. Further, microarray stresses and by biotic stress powdery mildew
analysis revealed that many stress-responsive infection, and biotrophic fungus Podosphaera
genes were up-regulated in OsNAC6- aphanis (Hu et al. 2015). Further, the level of
overexpressing rice plants, though OsNAC6 has a AtHsfA6a transcript highly increased under high
negative effect on growth and productivity in rice salinity and dehydration conditions (Hwang et al.
(Nakashima et al. 2007) (Figure 3). Interestingly, 2014). In addition, HSF4 was induced by salinity
OsNAC5 homolog of OsNAC6 was induced by and/or osmotic stress and fungal pathogen Botrytis
drought, cold, high-salinity, abscisic acid and methyl cinerea in A. thaliana (Sham et al. 2015) while
jasmonic acid and augmented stress tolerance by HsfA3 was reported to be associated with response
overexpression of stress-responsive genes such as to drought and salt stress (Li et al. 2013). Moreover,
OsLEA3 with no negative effect on rice growth several Hsf genes were highly over-expressed by
(Takasaki et al. 2010). Notwithstanding, the exogenous ABA (Hwang et al. 2014; Hu et al. 2015).
crosstalk between OsNAC6/OsNAC5 and hormone These studies thus provide a link between ABA and
signaling underlying tolerance to multiple biotic and Hsfs activation and indicate that HSFs, as a point of
abiotic stresses requires further investigation. cross-tolerance, act as the transcriptional activators
of several stress-responsive genes which could be
Heat shock proteins and heat shock trans- via ABA-dependent signaling pathway. They also
cription factors suggest the involvement of HSFs-activated stress-
A family of highly conserved genes encodes heat responsive genes in HSFs-mediated stress
shock proteins (HSPs) across all cells of both, tolerance.
prokaryotes and eukaryotes. These stress response
proteins are constitutively expressed in cells under Recent studies identified melatonin (N-acetyl-5-
normal conditions, in the absence of environmental methoxytryptamine) as an important secondary
stresses, and function as molecular chaperones messenger that conferred resistance to heat, salt,
regulating protein synthesis, folding, assembly, drought, cold and pathogen Pseudomonas syringe
translocation, and degradation (Wang et al. 2004). pv. tomato in Arabidopsis (Shi et al. 2015 a,b). It
Their expression is increased upon exposure to a positively regulated the expression of class A1 heat-

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Plant Immune System Nejat and Mantri

shock factors (HSFA1s) as the master regulators of stresses and their target genes (Xin et al. 2010;
heat stress response and several stress-responsive Raghuram et al., 2014; Omidvar et al. 2015).
genes such as COR15A, RD22, and KIN1. Hence,
melatonin may remarkably impact crosstalk among Only a few studies have been conducted on the role
stress responses, and control biotic and abiotic of miRNA in plant responses to both, biotic and
stress response as a regulator of HSFs (Shi et al. abiotic stresses. Using Solexa high-throughput
2015 a,b). sequencing, Xin et al. define the role of miRNAs in
regulating the response of wheat to heat stress and
There is also evidence to suggest a crosstalk powdery mildew infection caused by Erysiphe
between HSFs and oxidative stress signaling, and graminis f.sp. tritici (Egt). They identified 24 and 12
HSPs and TIR-NBS-LRR genes (Scarpeci et al. miRNAs that were expressed with different
2008; Prasch and Sonnewald 2013). Scarpeci et al. expression patterns in response to powdery mildew
identified heat shock transcription factors HsfA2 and infection and heat stress, respectively. Further, 9
HsfA4A that can sense oxidative stress caused miRNAs were co-regulated by both, powdery
during heat and pathogen attack via direct sensing mildew and heat, of which miR827 and miR2005
of H2O2 in Arabidopsis (Scarpeci et al. 2008). were overexpressed in both, Egt and heat stress.
Prasch and Sonnewald investigated the response of This exhibits their important role in wheat response
Arabidopsis plants to heat, drought, and Turnip to biotic and abiotic stresses. Further, miR156 was
mosaic virus (TuMV) by transcriptome and down-regulated in Egt susceptible (Jindong8) and
metabolome analysis. Their results revealed that the resistant (Jindong8-Pm30) wheat lines after Egt
highest number of TIR-NBS-LRR resistance genes inoculation whilst it was up-regulated in both, heat
is induced under heat and combined heat and susceptible (Chinese Spring) and tolerant (TAM107)
drought stress, whilst only a few TIR-NBS-LRR genotypes, after heat treatment. In addition,
genes were regulated under combined triple stress. negative correlations were identified between
These findings suggest that HSPs regulate the miR156 and its target genes Ta3711 and Ta7012
function of NBS-LRR genes in response to biotic (Xin et al. 2010). These studies reveal cross-talk
and abiotic stresses (Prasch and Sonnewald 2013). and functional interactions among stress-induced
wheat miRNAs and corroborate the stress-specific
MicroRNAs role of miRNAs.
MicroRNAs (miRNAs) are a class of endogenous
small non-coding, single-stranded RNAs of Kulcheski et al. (2011) using Solexa sequencing
approximately 20-24 nucleotides in length. They technology analyzsed the miRNA expression pattern
regulate expression of their target genes in plants of soybean cultivars susceptible and resistant to
as key post-transcriptional gene regulators through Asian soybean rust, Phakopsora pachyrhizi, to
translational repression or transcript cleavage pathogen infection and drought stress. Their results
(Mantri et al. 2013; Kamthan et al. 2015). miRNAs revealed that many miRNAs are involved in
have been implicated in plant growth and response to both, biotic and abiotic stresses, though
development, cell proliferation and cell death, they exhibited completely different and contrasting
organogenesis, auxin signaling and also established expression profiles in the response to rust infection
to perform key roles in response to a wide array of and drought stress. In addition, some miRNAs
biotic and abiotic stresses. (Khraiwesh et al. 2012; respond to the same stress differently depending on
Mantri et al. 2013). miRNAs target transcription the soybean genotypes. Of these, MIR-Seq11
factors comprising AP2, bHLH, MYB, TCP, NAC, predicted to target peroxidase precursor mRNAs,
NFY, and HD-Zip and diverse range of defence- was significantly induced in the roots of drought
related genes such as receptor-like kinase, MAPK susceptible genotype (BR 16) compared to the
genes, peroxidase, NB-LRRs, and ABC transporters controls, although it responds similarly in the treated
(Kulcheski et al. 2011; Khraiwesh et al. 2012; Kumar and untreated drought-tolerant cultivar (Embrapa
2014; Raghuram et al., 2014; Omidvar et al. 2015). 48). Further, expression of MIR-Seq11 was
Recent studies revealed that miRNAs respond to remarkably different between the mock and rust
abiotic stresses in a genotype-, tissue-, stress-, and inoculated susceptible genotype (Embrapa 48),
miRNA-dependent manner (Omidvar et al. 2015; while it responds in a similar manner in the soybean
Zhang 2015). Negative correlation, however, has rust resistant genotype (PI561356) (Kulcheski et al.
prevailed between the expression levels of miRNAs 2011). These findings suggest that miRNAs may
implicated in the response to biotic and abiotic respond to stresses in a not only stress- but also
genotype-specific manner.

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Plant Immune System Nejat and Mantri

methylation, histone posttranslational modification,

The results also indicate that miRNAs may target chromatin remodeling complexes, small non-coding
only one locus or several loci in response to biotic RNAs (miRNAs and small interfering RNAs,
and abiotic stresses. MIR-Seq10, MIR-Seq15, and siRNAs), and long non-coding RNAs.
MIR-Seq18 targeted only one locus, although, MIR-
Seq05, MIR-Seq11, MIR-Seq16 and MIR-Seq19 DNA methylomes profiling of Arabidopsis thaliana
presented several loci as targets (Kulcheski et al. plants challenged with a bacterial pathogen,
2011). Pseudomonas syringae pv. tomato, nonpathogenic
bacteria or salicylic acid (SA) revealed that stress-
Recently, Omidvar et al. (2015) used Illumina induced differentially methylated regions (DMRs)
Hiseq2000 platform to investigate the simultaneous can regulate the expression of proximal stress-
impact of ABA and mannitol treatments on the wild- responsive genes as general regulatory hubs for
type and abiotic stress-tolerant 7B-1 tomato mutant. defence-responsive genes. Moreover, their results
They also analyzsed the expression of 6 selected exhibited that SA-induced demethylation, along with
miRNAs (including miR159, miR166, miR472, up-regulation of transposable elements and 21-nt
miR482, miR#A, and miR#D) in response to ABA, small RNAs produced from these elements
mannitol, NaCl and cold treatments. Their results increased the expression of neighboring protein-
revealed that miRNAs were differentially expressed coding genes in SA-treated plants (Dowen et al.
in response to abiotic stresses. miRNA159 and 2012).
miRNA166 were inversely expressed in response to
cold, while they showed the same pattern in The results of another study indicate the
response to ABA, mannitol, and NaCl. Likewise, involvement of AhHDA1, an RPD3/HDA1-like
different levels of expression were revealed superfamily histone deacetylase (HDAC), in the
between hypocotyl and root tissues. miR159, regulation of stress resistance genes in response to
miR472, and miR482 were remarkably down- osmotic stress and ABA in peanut (Arachis
regulated in roots compared with hypocotyl. These hypogaea) (Su et al. 2015).
results support previous studies that found miRNAs
react to abiotic stresses in a stress-, miRNA-specific The review by Liu et al (2015) describe the major
and plant tissue-dependent manner. epigenetic mechanisms contributing to the control of
plant heat responses, highlighting epigenetic
While there is currently no published study on modifications comprising DNA methylation, histone
miRNA responses to combined stresses and modifications, histone chaperones, histone variants,
crosstalk between miRNAs in response to a ATP-dependent chromatin remodeling, small non-
combination of stresses, it is indispensable to coding RNAs and long non-coding RNAs in
dissect their responses, functions, and regulatory modulating the expression of heat-responsive genes
mechanisms in response to the combination of under high temperature. In another review, Kim et al
biotic and abiotic stresses. (2015) highlight the role of histone modification in
stress memory and modulating stress-responsive
Epigenetics and stress response gene networks in response to drought, salinity, heat,
The term epigenetics describes heritable changes in and cold.
gene expression patterns that transpire without
altering the underlying DNA sequence (Iwasaki and Further, another finding unravelled that when plants
Paszkowski 2014). In the recent past, numerous confront stressful environmental conditions, the first
studies have corroborated the crucial role of experience of stress can be memorized and
epigenetic mechanisms in plant immunity and stress inherited to the next generation as a trans-
adaptation (Ding and Wang 2015; Iwasaki and generational epigenetic inheritance (Molinier et al.
Paszkowski 2014; Kim et al. 2015; Kinoshita and 2006). Recent studies revealed epigenetic
Seki 2014) and ample progress has been made in mechanisms underlying this stress-driven phen-
elaborating epigenetic regulation of plant responses omenon, although are not fully understood. The
to stressors (Álvarez-Venegas and De-la-Peña evidence suggests full-scale reprogramming of the
2015; Ding and Wang 2015; Dowen et al. 2012; Su epigenome does not occur during gametogenesis
et al. 2015). The results of these studies due to escaping reprogramming of epigenetic marks
demonstrated that plants have evolved intricate (Bilichak and Kovalchuk 2016).
epigenetic mechanisms in regulating plant
responses to environmental factors comprising DNA

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Plant Immune System Nejat and Mantri

Nevertheless, stress-responsive epigenomes have identification of multifunctional genes and genes

thus far been studied in response to single biotic/or responsible for biotic and abiotic stress resistance
abiotic stresses. Studies of the epigenome, would help accelerate development of resistant crop
however, are scarce in simultaneous biotic and plants through precise genome editing using
abiotic stresses. Extending our knowledge of emerging technologies for targeted genome editing
epigenetic mechanisms to simultaneous combined such as Transcription Activator-Like Effector
stresses is not only essential for understanding the Nucleases (TALENs) and CRISPR (Clustered
crosstalk between epigenetic components, and Regulatory Interspaced Short Palin-dromic
epigenome and transcriptome but to also providing Repeats)/Cas9 systems.
vital information for epigenetic engineering and crop
improvement. Though, we are still far from being Declaration of interest
able to incorporate it in plant breeding for crop The authors report no declarations of interest.
improvement.
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