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Crosstalk between abiotic and biotic stress responses:

a current view from the points of convergence in the stress


signaling networks
Miki Fujita
1,2,3
, Yasunari Fujita
4
, Yoshiteru Noutoshi
5,6
,
Fuminori Takahashi
1,3,7
, Yoshihiro Narusaka
8
,
Kazuko Yamaguchi-Shinozaki
2,4,9
and Kazuo Shinozaki
1,2,3
Plants have evolved a wide range of mechanisms to cope with
biotic and abiotic stresses. To date, the molecular mechanisms
that are involved in each stress has been revealed
comparatively independently, and so our understanding of
convergence points between biotic and abiotic stress signaling
pathways remain rudimentary. However, recent studies have
revealed several molecules, including transcription factors and
kinases, as promising candidates for common players that are
involved in crosstalk between stress signaling pathways.
Emerging evidence suggests that hormone signaling pathways
regulated by abscisic acid, salicylic acid, jasmonic acid and
ethylene, as well as ROS signaling pathways, play key roles in
the crosstalk between biotic and abiotic stress signaling.
Addresses
1
Gene Discovery Research Group, RIKEN Plant Science Center,
1-7-22 Suehiro-cho, Yokohama, Kanagawa 203-0045, Japan
2
Core Research for Evolutional Science and Technology (CREST),
Japan Science and Technology Agency (JST), Kawaguchi,
Saitama 332-0012, Japan
3
Laboratory of Plant Molecular Biology, RIKEN Tsukuba Institute,
3-1-1 Kouyadai, Tsukuba, Ibaraki 305-0074, Japan
4
Biological Resources Division, Japan International Research Center
for Agricultural Sciences, 1-1 Ohwashi, Tsukuba, Ibaraki 305-8686,
Japan
5
Plant Immunity Research Group, RIKEN Plant Science Center,
1-7-22 Suehiro-cho, Yokohama, Kanagawa 203-0045, Japan
6
The Sainsbury Laboratory, John Innes Centre, Colney Lane,
Norwich NR4 7UH, UK
7
Institute of Biological Sciences, Tsukuba University, Tennodai,
Tsukuba, Ibaraki, 305-8572, Japan
8
Department of Biology, Tokyo Gakugei University, 4-1-1
Nukuikita-machi, Koganei-shi, Tokyo 184-8501, Japan
9
Laboratory of Plant Molecular Physiology, Graduate School of
Agricultural and Life Sciences, The University of Tokyo, 1-1 Yayoi,
Bunkyo-ku, Tokyo 113-8657, Japan
Corresponding author: Shinozaki, Kazuo (sinozaki@rtc.riken.jp)
Current Opinion in Plant Biology 2006, 9:436442
This review comes from a themed issue on
Biotic interactions
Edited by Anne Osbourn and Sheng Yang He
Available online 8th June 2006
1369-5266/$ see front matter
# 2006 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2006.05.014
Introduction
Plants undergo continuous exposure to various biotic and
abiotic stresses in their natural environment. To survive
under such conditions, plants have evolved intricate
mechanisms to perceive external signals, allowing opti-
mal response to environmental conditions. Phytohor-
mones such as salicylic acid (SA), jasmonic acid (JA),
ethylene (ET), and abscisic acid (ABA) are endogenous,
low-molecular-weight molecules that primarily regulate
the protective responses of plants against both biotic and
abiotic stresses via synergistic and antagonistic actions,
which are referred to as signaling crosstalk [1,2,3

].
Moreover, the generation of reactive oxygen species
(ROS) has been proposed as a key process that is shared
between biotic and abiotic stress responses [4,5

]. Rapidly
accumulating data, resulting from large-scale transcrip-
tome analyses with DNA microarray technology, strongly
support the existence of such crosstalk between signaling
networks [69,10

]. Biotic and abiotic stresses regulate


the expression of different but overlapping suites of
genes. For example, the correlation of transcriptional
regulation with environmental challenges, such as heavy
metal (CuSO
4
) stress, and with incompatible necrotrophic
pathogen infection reveals signicant overlap between
responses to biotic and abiotic stresses. These data sug-
gest that ROS are a common signal that trigger down-
stream stress responses [11]. Thus, a growing body of
evidence supports the notion that plant signaling path-
ways consist of elaborate networks with frequent cross-
talk, thereby allowing plants to regulate both abiotic
stress tolerance and disease resistance. This review
focuses upon recent studies that have identied and
characterized the function of genes that are involved in
this crosstalk, subsequently shedding light on the mole-
cular convergence points between biotic and abiotic stress
signaling pathways (Figure 1).
Hormone signaling pathways govern biotic
and abiotic stress responses
ABA is a phytohormone that is extensively involved in
responses to abiotic stresses such as drought, low tem-
perature, and osmotic stress. ABA also governs a variety of
growth and developmental processes, including seed
development, dormancy, germination, and stomatal
movement. By contrast, the phytohormones SA, JA,
and ET play central roles in biotic stress signaling upon
Current Opinion in Plant Biology 2006, 9:436442 www.sciencedirect.com
pathogen infection. In many cases, ABA acts as a negative
regulator of disease resistance [3

]. For example, the


ABA-decient tomato mutant sitiens has increased resis-
tance to pathogens and application of exogenous ABA
restored the susceptibility of sitiens [12,13]. The sitiens
mutant has greater SA-mediated responses, suggesting
that high ABA concentrations inhibit the SA-dependent
defense response in tomato. ABA and ET are well known
to interact, mostly antagonistically, in a number of devel-
opmental processes and in vegetative tissues [14,15].
Genetic analysis of enhanced response to ABA3 (era3) alleles
revealed that ERA3 is allelic to ETHYLENE INSENSI-
TIVE2 (EIN2), which encodes a membrane-bound puta-
tive divalent cation sensor that may represent a crosstalk
point that intersects the ABA and ET signaling pathways
[15]. Furthermore, jasmonic acid resistance1 (jar1) and
jasmonic acid insensitive4 (jin4) mutants, which are hyper-
sensitive to ABA-mediated inhibition of germination,
exhibit antagonistic effects of ABA and JA [2,16

]. Addi-
tionally, exogenous application of ABA resulted in the
downregulation of JA- or ET-responsive defense gene
expression in wildtype plants, whereas higher expression
levels of these defense genes were observed in ABA-
decient mutants without any treatments [16

]. Taken
together with the ndings that exogenous application of
methyl-JA and ET cannot restore the defense gene
expression that is suppressed by exogenous ABA applica-
tion, these data suggest that the ABA-mediated abiotic
stress response is a dominant process [16

].
Recent studies demonstrate that the basic helix-loop-helix
(bHLH) transcription factor AtMYC2 plays a role in multi-
ple hormone signaling pathways. Genetic analysis of the
jasmonate-insensitive jin1 mutant revealed that JIN1 is
allelic to AtMYC2 [17]. AtMYC2, which was rst identied
as a transcriptional activator that is involved in the ABA-
mediated drought stress signaling pathway [18], upregu-
lates the expression of genes that are involved in the JA-
mediated wounding response and negatively regulates
the expression of JA/ET-mediated pathogen defense
genes [16

,17,19]. AtMYC2 knockout mutants are less


sensitive to ABA and exhibit signicantly reduced ABA-
responsive gene expression [18]. In addition, AtMYC2
deciency results in increased JA- or ET-regulated
defense gene expression and in enhanced resistance to
a necrotrophic pathogen [16

,17]. Although ABA-


mediated AtMYC2 activation cannot solely account for
the inhibitory effect of ABA on JA-regulated expression
of defense genes, AtMYC2 might be a key regulator of
crosstalk via hormone signaling between biotic and abio-
tic stress responses.
Both AtMYC2 and the R2R3MYB-type transcription factor
AtMYB2 bind cis-elements in the dehydration-inducible
RD22 gene and cooperatively activate its expression [18].
Interestingly, transgenic plants that overexpress both
AtMYC2 and AtMYB2 display greater sensitivity to ABA
and enhanced osmotic stress tolerance when compared to
wildtype plants [18]. In addition, Botrytis infection
induces the expression of Botrytis SUSCEPTIBLE 1
(BOS1), which shares high sequence similarity with
AtMYB2, through a JA-mediated defense signaling path-
way [20]. Disruption of BOS1 results in increased sensi-
tivity to necrotrophic pathogens and impaired drought,
salinity, and oxidative stress tolerance. Furthermore,
other data suggested that BOS1 mediates both biotic
and abiotic stress signaling via ROS. Therefore,
R2R3MYB transcription factors might serve as important
mediators of stress responses that have complex activities
spanning multiple stress signaling pathways.
RD26, a dehydration-responsive NACtranscription factor,
is another viable candidate molecule that potentially reg-
ulates aspects of both biotic and abiotic signaling. RD26
expression is induced by JA, hydrogen peroxide (H
2
O
2
)
and pathogen infections, as well as by drought, high
salinity and ABA treatment [21,22]. Large-scale transcrip-
tome analysis revealed that RD26-regulated genes are
involved in the detoxication of ROS, defense, or senes-
cence. These ndings suggest that RD26 functions at the
convergence point between the pathways for pathogen
defense, senescence, and ABA-mediated signaling [21].
Recent research revealed that ATAF2, a NACgene that is
similar to RD26, functions as a repressor of pathogenesis-
related proteins in Arabidopsis [23]. Overexpression of the
ATAF2 gene, which responds to wounding, to exogenous
SA and JA application and to high-salinity stress, results in
Crosstalk between abiotic and biotic stress responses Fujita et al. 437
Figure 1
Convergence points in abiotic and biotic stress signaling networks.
www.sciencedirect.com Current Opinion in Plant Biology 2006, 9:436442
the repression of pathogenesis-related proteins and in
elevated susceptibility to soil-borne fungal pathogens.
Additionally, recent studies identied other molecular
entities that signicantly impact crosstalk among stress-
response pathways via hormone signaling. For instance,
both nitric oxide [24] and Ca
2+
signaling play an important
role in plant defense responses, ABA-dependent stomatal
movements, and drought stress responses [3

]. Calcium-
dependent protein kinases in tobacco might control biotic
and abiotic stress responses via signaling pathways that
are mediated by hormones such as SA, ET, JA, and ABA
[2527]. In addition, fungal elicitors can activate a branch
of the ABA signaling pathway in guard cells that regulates
plasma membrane Ca
2+
channels [28]. Moreover, a bat-
tery of studies examining the induction of resistance by
the non-protein amino acid b-aminobutyric acid revealed
that ABAconsiderably enhances plant resistance to fungal
pathogens through its positive effect on callose deposition
[3

,29,30].
MAP-kinase cascades mediate stress
signaling crosstalk
Protein phosphorylation and dephosphorylation signi-
cantly inuence both the regulation of physiological
morphology and gene expression that is associated with
basic cellular activities. In all eukaryotes, mitogen-acti-
vated protein (MAP) kinase (MAPK/MPK) cascades are
highly conserved central regulators of diverse cellular
processes, such as differentiation, proliferation, growth,
death, and stress responses. In plants, the MAPK cascade
plays a crucial role in various biotic and abiotic stress
responses and in hormone responses that include ROS
signaling [31,32

].
The Arabidopsis MAP kinase kinase 1 (MEKK1) is tran-
scriptionally induced by cold, salt, drought, touch, and
wounding [33]. In particular, MEKK1MAPK kinase 2
(MKK2)MPK4/MPK6 cascade has been shown to func-
tion as part of cold and salt stress signaling [34

,35]. By
contrast, MEKK1MKK4/MKK5MPK3/MPK6 cascades
have been reported to regulate the pathogen defense
response pathway via the expression of WRKY22 and
WRKY29 [36,37]. MPK3 and MPK6 are also activated
by abiotic stresses [35,38] and involved in hormone
signaling pathways. MPK3 has been shown to function
in ABA signaling at the post-germination stage [39].
MPK6 is thought to be involved in ET production
through phosphorylation of the rate-limiting enzymes
of ET biosynthesis, the 1-aminocyclopropane-1-car-
boxylic acid (ACC) synthases ACS2 and ACS6 [40

],
in JA-dependent root growth and in AtMYC2 gene expres-
sion (F Takahashi, unpublished). The rice OsMPK5 gene
is an ortholog of Arabidopsis MPK3. The gene expression
and kinase activity of OsMPK5 is also induced by ABA,
various abiotic stresses and pathogen infection [41]. Gain-
and loss-of-function analyses revealed that OsMPK5
positively regulates tolerance of drought, salt, and cold
stresses and negatively regulates PR gene expression and
broad-spectrum disease resistance in rice.
MPK6 is activated by oxidative stress in Arabidopsis
cultured cells [42]. MPK3 and MPK6 activities in ROS
signaling are affected by an Arabidopsis serine/threonine
kinase, OXI1, whose kinase activity is induced by H
2
O
2
[43]. Also, ANP1, an Arabidopsis MAPKKK, activates
MPK3 and MPK6 via H
2
O
2
. Tobacco plants that over-
expressed constitutively active tobacco NPK1 (Nicotiana
protein kinase 1), a homolog of ANP1, exhibited
improved tolerance of freezing, heat, drought and high-
salt conditions [44]. A. thaliana NUCLEOSIDE-DIPHO-
SPHATE KINASE 2 (AtNDPK2), whose expression is
induced by H
2
O
2
, specically interacts with MPK3 and
MPK6, thereby activating MPK3 in vitro [45]. Overex-
pression of AtNDPK2 enhances tolerance of cold, salt, and
oxidative stresses. Thus, MAPK cascades apparently
mediate ROS signaling, and consequently control toler-
ance of environmental stresses in each transgenic plant by
improving ROS scavenging capacity.
Roles of ROS at points of convergence
between biotic and abiotic stress response
pathways
The tight regulation of the steady-state levels of ROS is
involved in multiple cellular processes in plants [4]. Some
ROS species are toxic byproducts of aerobic metabolism,
whereas ROS also function as signaling molecules [4].
Rapid ROS production plays a pivotal role in both ABA
signaling and disease resistance responses [46,47]. Several
lines of evidence suggests that the NADPH-dependent
respiratory burst oxidase homolog genes (AtrbohD and
AtrbohF) are required for ROS generation, leading to
ABA-induced stomatal closure and to hypersensitive cell
death in response to avirulent pathogen attack [5

,48,49].
ROS scavengers are thought to detoxify the cytotoxic
effects of ROS under various stress conditions [4,50].
Large-scale transcriptome analyses of plants that had
been subjected to various abiotic and biotic stress treat-
ments revealed the induction of a large set of genes that
encode ROS-scavenging enzymes under these conditions
[6,8,50]. Moreover, scavenging enzymes (e.g. superoxide
dismutase, glutathione peroxidase and ascorbate perox-
idase) have been utilized to engineer plants that are
tolerant of abiotic stresses [51,52]. Microarray analysis
using Arabidopsis cultured cells reveal that many ABA-
inducible genes are induced by oxidative stress [53].
Recently, it has been suggested that a C
2
H
2
-type zinc-
nger transcription factor, Zat12, might be a regulator in
the ROS scavenging mechanism that is involved in biotic
and abiotic stress responses. Deciency in Zat12, which is
highly responsive to multiple stresses including wound-
ing, pathogen infection and abiotic stresses [6,22,54,55],
suppresses the expression of the ASCORBATE
438 Biotic interactions
Current Opinion in Plant Biology 2006, 9:436442 www.sciencedirect.com
PEROXIDASE 1 (APX1) gene, which is induced by
H
2
O
2
and increases the level of H
2
O
2
-induced protein
oxidation [56]. Overexpression of Zat12 results in upre-
gulation of oxidative- and light-stress-responsive genes
and in enhanced tolerance of high light, freezing, and
oxidative stresses [5457]. Interestingly, the expression of
Zat12 is regulated by a redox-sensitive transcription fac-
tor, HEAT SHOCK FACTOR (HSF) 21, which is likely
to be an initial sensor for H
2
O
2
that accumulates in
response to various stresses [10

]. These ndings suggest


that the ROS might mediate crosstalk between biotic and
abiotic stress-responsive gene-expression networks.
Effects of high humidity and high
temperature upon biotic stress responses
High humidity and high temperature both affect plant
disease development, attenuating plant disease resistance
while promoting pathogen growth. Consistently, pheno-
types of several lesion-mimic mutants, which are caused
by misregulated R genes (e.g. chimeric Mi, overexpres-
sion of the powdery mildew R gene RPW8, SA-insensitiv-
ity4 [ssi4], bonzai1/copine1 [bon1/cpn1] and slh1), are also
suppressed by environmental cues [5863], suggesting
the existence of crosstalk between R-gene-mediated dis-
ease resistance responses and abiotic stress responses. For
example, the cell death phenotypes of the overexpressor
of RPW8 [60] and slh1 [61] mutants of Arabidopsis are
suppressed by both high temperature and high humidity.
In the ssi4 mutant, high humidity conditions inhibited the
constitutive activation of MPK3 and MPK6 as well as
H
2
O
2
production, suggesting that a high humidity sensor
acts early in the signaling cascade [59]. Recently, it has
been revealed that abundance of the barley R proteins
MLA1 and MLA6 decreased dramatically within several
hours after subjection to a temperature shift from 18 8C to
37 8C, without reduction of the MLA1 and MLA6 tran-
scripts [64

]. Thus, R protein instability that is imposed


by environmental stresses might represent a solid cross
point between disease resistance and abiotic stress
response. High humidity and high temperature both
affect disease resistance that is mediated by receptor-like
kinase type R genes [65]; therefore, abiotic stresses might
also destabilize receptor-like kinase (RLK)-type R pro-
teins and/or signaling components that are common to
cytosolic- and membrane-anchored-type R proteins.
Conclusions
Current evidence supports the concept that ROS repre-
sent a signicant point of convergence between pathways
that respond to biotic and abiotic stresses. Nevertheless,
our current understanding of ROS participation in cross-
talk between these pathways is very limited. Thus, dis-
secting the genetic network that regulates ROS signaling
in response to biotic and abiotic stresses merits extensive
future study. When combined, the results of large-scale
transcriptome, proteome, and metabolome analyses in
plants will enable the elucidation of the ROS network
components that govern multiple stress signaling path-
ways. In particular, the Genevestigator software should
yield powerful clues, allowing us to connect these key
molecular players and to discover novel crosstalk net-
works [66].
A signicant body of research suggests an antagonistic
interaction between ABA-mediated abiotic stress signal-
ing and disease resistance. This relationship may simply
suggest that plants have developed strategies to avoid
simultaneously producing proteins that are involved in
abiotic stress and disease resistance responses [16

]. In
nature, simultaneous exposure of plants to drought and
necrotrophic pathogen attack is actually rare, as successful
pathogen infection requires relatively humid conditions.
The nding that high humidity and high temperature
weaken plant resistance to pathogen attack is consistent
with this concept. Moreover, the view that the ABA-
mediated abiotic stress signaling potentially takes pre-
cedence over biotic stress signaling [16

] also supports
the notion that water stress more signicantly threatens
plant survival than does pathogen infection. To date, the
biological signicance of crosstalk between signaling
pathways that operate under stress conditions and the
mechanisms that underlie this crosstalk remain obscure.
We are just beginning to dissect key factors governing the
crosstalk between these signaling pathways under various
stress conditions.
Acknowledgements
We thank Dr K Shirasu for critical reading of the manuscript. This work
was supported in part by a grant for Genome and Plant Research from
RIKEN, by the Program for Promotion of Basic Research Activities for
Innovative Biosciences from the Bio-oriented Technology Research
Advancement Institution of Japan (BRAIN), and by a Grant-in-Aid from
the Ministry of Education, Culture, Sports, Science and Technology of
Japan (MEXT) to KS and KY-S.
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www.sciencedirect.com Current Opinion in Plant Biology 2006, 9:436442
the abundance of the barley powdery mildew resistance R proteins MLA1
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