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pathogen infection. In many case s, ABA acts as a negativeregulator of disease resistance [ 3 ]. For example, theABA-decient tomato mutant sitiens has increased resis-tance to pathogens and application of exogenous ABArestored the susceptibility of sitiens [12,13 ]. The sitiensmutant has greater SA-mediated responses, suggestingthat high ABA concentrations inhibit the SA-dependentdefense response in tomato. ABA and ET are well knownto interact, mostly antagonistically, in a number of devel-opmental processes and in vegetative tissues [ 14,15 ].Genetic analysis of enhanced response to ABA3 (era3 ) allelesrevealed that ERA3 is allelic to ETHYLENE INSENSI-TIVE2 ( EIN2 ), which encodes a membrane-bound puta-tive divalent cation sensor that may represent a crosstalkpoint that intersects the ABA and ET signaling pathways. 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 thedownregulation of JA- or ET-responsive defense geneexpression in wildtype plants, whereas higher expressionlevels of these defense genes were obser ve d in ABA-decient mutants without any treatments [ 16 ]. Takentogether with the ndings that exogenous application of methyl-JA and ET cannot restore the defense geneexpression that is suppressed by exogenous ABA applica-tion, these data suggest that the ABA -m ediated abioticstress response is a dominant process [ 16 ].
Recent studies demonstrate that the basic helix-loop-helix(bHLH) transcription factor AtMYC2plays a role in multi-ple hormone signaling pathways. Genetic analysis of the jasmonate-insensitive jin1 mutant revealed that JIN1 isallelic to AtMYC2 . AtMYC2, which was rst identied
as a transcriptional activator that is involved in the ABA-mediated drought stress s ignaling pathway [ 18], upregu-lates the expression of genes that are involved in the JA-mediated wounding response and negatively regulatesthe ex pre ssion of JA/ET-mediated pathogen defensegenes [ 16 ,17,19 ]. AtMYC2 knockout mutants are lesssensitive to ABA and exhibit signicantly reduced ABA-responsive gene expression [ 18]. In addition, AtMYC2deciency results in increased JA- or ET-regulateddefense gene expression an d in enhanced resistance toa necrotrophic pathogen [ 16 ,17]. Although ABA-mediated AtMYC2 activation cannot solely account forthe inhibitory effect of ABA on JA-regulated expressionof 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 ABAand enhanced osmotic stress tolerance when compared towildtype plants [ 18]. In addition, Botrytis infectioninduces the expression of Botrytis SUSCEPTIBLE 1( BOS1), which shares high sequence similarity with AtMYB2 , through a JA-mediated defense signaling path-way . 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 bioticand abiotic stress signaling via ROS. Therefore, R2R3MYB transcription factors might serve as importantmediators of stress responses that have complex activitiesspanning multiple stress signaling pathways.
RD26,a dehydration-responsiveNAC transcription 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, highsalinity and ABA treatment [ 21,22 ]. Large-scale transcrip-tome analysis revealed that RD26-regulated genes areinvolved in the detoxication of ROS, defense, or senes-cence. These ndings suggest that RD26 functions at theconvergence point between the pathways for pathogendefense, senescence, and ABA-mediated signaling [ 21].Recent research revealed that ATAF2, a NAC gene that issimilar to RD26, functions as a repressor of pathogenesis-related proteins in Arabidopsis . Overexpression of the ATAF2 gene, which responds to wounding, to exogenousSA and JA application and to high-salinity stress, results in
Crosstalk between abiotic and biotic stress responses Fujita et al. 437
Convergence points in abiotic and biotic stress signaling networks.
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the repression of pathogenesis-related proteins and inelevated susceptibility to soil-borne fungal pathogens.
Additionally, recent studies identied other molecularentities that signicantly impact crosstalk among stress-
response pathways via hormone signaling. For instance,both nitricoxide [ 24]andCa 2+ signaling play an importantrole in plant defense responses, ABA-depe nd ent stomatalmovements, and drought stress responses [ 3 ]. Calcium-dependent protein kinases in tobacco might control bioticand abiotic stress responses via signaling pathways thatare mediated by hormones such as SA, ET, JA, and ABA[2527 ]. In addition, fungal elicitors can activate a branchof the ABA signaling pathway in guard cells that regulatesplasma membrane Ca 2+ channels [ 28]. Moreover, a bat-tery of studies examining the induction of resistance bythe non-protein amino acid b -aminobutyric acid revealedthat ABA considerably enhances plant resistance to fungalpathogens through its positive effect on callose deposition[3 ,29,30 ].
MAP-kinase cascades mediate stresssignaling crosstalk Protein phosphorylation and dephosphorylation signi-cantly inuence both the regulation of physiologicalmorphology and gene expression that is associated withbasic cellular activities. In all eukaryotes, mitogen-acti-vated protein (MAP) kinase (MAPK/MPK) cascades arehighly conserved central regulators of diverse cellularprocesses, such as differentiation, proliferation, growth,death, and stress responses. In plants, the MAPK cascadeplays a crucial role in various biotic and abiotic stressresponses and i n hormone responses that include ROSsignaling [ 31,32 ].
The Arabidopsis MAP kinase kinase 1 (MEKK1) is tran-scriptionally induced by cold, salt, drought, touch, andwounding [ 33]. In particular, MEKK1MAPK kinase 2(MKK2)MPK4/MPK6 cascade has been sho wn to func-tion as part of cold and salt stress signaling [ 34 ,35]. Bycontrast, MEKK1MKK4/MKK5MPK3/MPK6 cascadeshave been reported to regulate the pathogen defenseresponse pathway via the expression of WRKY22 andWRKY29 [36,37 ]. MPK3 and MPK6 are also activatedby abiotic stresses [ 35,38 ] and involved in hormone
signaling pathways. MPK3 has been shown to functionin ABA signaling at the post-germination stage [ 39].MPK6 is thought to be involved in ET productionthrough phosphorylation of the rate-limiting enzymesof 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 geneis an ortholog of Arabidopsis MPK3. The gene expressionand 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 coldstresses and negatively regulates PR gene expression andbroad-spectrum disease resistance in rice.
MPK6 is activated by oxidative stress in Arabidopsis
cultured cells [ 42]. MPK3 and MPK6 activities in ROSsignaling are affected by an Arabidopsis serine/threoninekinase, OXI1, whose kinase activity is induced by H 2 O 2. Also, ANP1, an Arabidopsis MAPKKK, activatesMPK3 and MPK6 via H 2 O 2 . Tobacco plants that over-expressed constitutively active tobacco NPK1 ( Nicotianaprotein kinase 1), a homolog of ANP1, exhibitedimproved tolerance of freezing, heat, drought and high-salt conditions [ 44]. A. thaliana NUCLEOSIDE-DIPHO- SPHATE KINASE 2 ( AtNDPK2 ), whose expression isinduced by H 2 O 2 , specically interacts with MPK3 andMPK6, thereby activating MPK3 in vitro . Overex-pression of AtNDPK2 enhances tolerance of cold, salt, andoxidative stresses. Thus, MAPK cascades apparentlymediate ROS signaling, and consequently control toler-ance of environmental stresses in each transgenic plant byimproving ROS scavenging capacity.
Roles of ROS at points of convergencebetween biotic and abiotic stress responsepathwaysThe tight regulation of the steady-state levels of ROS isinvolved in multiple cellular processes in plants [ 4]. SomeROS species are toxic byproducts of aerobic metabolism,whereas ROS also function as signaling molecules [ 4].Rapid ROS production plays a pivotal role in both ABAsignaling and disease resistance responses [ 46,47 ]. Severallines of evidence suggests that the NADPH-dependentrespiratory burst oxidase homolog genes ( AtrbohD and AtrbohF ) are required for ROS generation, leading toABA-induced stomatal closure and to hypersen sitive celldeath in response to avirulent pathogen attack [ 5 ,48,49 ].
ROS scavengers are thought to detoxify the cytotoxiceffects of ROS under various stress conditions [ 4,50 ].Large-scale transcriptome analyses of plants that hadbeen subjected to various abiotic and biotic stress treat-ments revealed the induction of a large set of genes thatencode 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 aretolerant of abiotic stresses [ 51,52 ]. Microarray analysisusing 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 inthe ROS scavenging mechanism that is involved in bioticand abiotic stress responses. Deciency in Zat12, which ishighly responsive to multiple stresses including wound-ing, pathogen infection and abiotic stresses [ 6,22,54,55 ],suppresses the expression of the ASCORBATE
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PEROXIDASE 1 ( APX1) gene, which is induced byH 2 O 2 and increases the level of H 2 O 2 -induced proteinoxidation [ 56]. Overexpression of Zat12 results in upre-gulation of oxidative- and light-stress-responsive genesand 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 likelyto be an initial sensor for H 2 O 2 that accumulates inresponse to various stresses [ 10 ]. These ndings suggestthat the ROS might mediate crosstalk between biotic andabiotic stress-responsive gene-expression networks.
Effects of high humidity and hightemperature upon biotic stress responsesHigh humidity and high temperature both affect plantdisease development, attenuating plantdisease resistancewhile promoting pathogen growth. Consistently, pheno-types of several lesion-mimic mutants, which are causedby 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 alsosuppressed by environmental cues [ 5863 ], suggestingthe existence of crosstalk between R-gene-mediated dis-ease resistance responses and abiotic stress responses. Forexample, the cell death phenotypes of the overexpressorof RPW8  and slh1  mutants of Arabidopsis aresuppressed by both high temperature and high humidity.In the ssi4 mutant, high humidity conditions inhibited theconstitutive activation of MPK3 and MPK6 as well asH 2 O 2 production, suggesting that a high humidity sensoracts early in the signaling cascade [ 59]. Recently, it hasbeen revealed that abundance of the barley R proteinsMLA1 and MLA6 decreased dramatically within severalhours after subjection to a temperature shift from 18 8 C to37 8 C, without reduction of the MLA1 and MLA6 tran-scripts [ 64 ]. Thus, R protein instability that is imposedby environmental stresses might represent a solid crosspoint between disease resistance and abiotic stressresponse. High humidity and high temperature bothaffect disease resistance that is mediated by receptor-likekinase type R genes [ 65]; therefore, abiotic stresses mightalso destabilize receptor-like kinase (RLK)-type R pro-teins and/or signaling components that are common tocytosolic- and membrane-anchored-type R proteins.
ConclusionsCurrent evidence supports the concept that ROS repre-sent a signicant point of convergence between pathwaysthat 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 signalingin response to biotic and abiotic stresses merits extensivefuture study. When combined, the results of large-scaletranscriptome, proteome, and metabolome analyses inplants will enable the elucidation of the ROS network
components that govern multiple stress signaling path-ways. In particular, the Genevestigator software shouldyield powerful clues, allowing us to connect these keymolecular players and to discover novel crosstalk net-works [ 66].
A signicant body of research suggests an antagonisticinteraction between ABA-mediated abiotic stress signal-ing and disease resistance. This relationship may simplysuggest that plants have developed strategies to avoidsimultaneously producing proteins that are inv olved inabiotic stress and disease resistance responses [ 16 ]. Innature, simultaneous exposure of plants to drought andnecrotrophic pathogen attack is actually rare, as successfulpathogen infection requires relatively humid conditions.The nding that high humidity and high temperatureweaken plant resistance to pathogen attack is consistentwith this concept. Moreover, the view that the ABA-mediated abiotic stress signaling pot en tially takes pre-cedence over biotic stress signaling [ 16 ] also supportsthe notion that water stress more signicantly threatensplant survival than does pathogen infection. To date, thebiological signicance of crosstalk between signalingpathways that operate under stress conditions and themechanisms that underlie this crosstalk rem...