Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks

Crosstalk between abiotic and biotic stress responses:a current view from the points of convergence in the stresssignaling networksMiki Fujita1,2,3, Yasunari Fujita4, Yoshiteru Noutoshi5,6,Fuminori Takahashi1,3,7, Yoshihiro Narusaka8,Kazuko Yamaguchi-Shinozaki2,4,9 and Kazuo Shinozaki1,2,3

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.

Addresses1 Gene Discovery Research Group, RIKEN Plant Science Center,

1-7-22 Suehiro-cho, Yokohama, Kanagawa 203-0045, Japan2 Core Research for Evolutional Science and Technology (CREST),

Japan Science and Technology Agency (JST), Kawaguchi,

Saitama 332-0012, Japan3 Laboratory of Plant Molecular Biology, RIKEN Tsukuba Institute,

3-1-1 Kouyadai, Tsukuba, Ibaraki 305-0074, Japan4 Biological Resources Division, Japan International Research Center

for Agricultural Sciences, 1-1 Ohwashi, Tsukuba, Ibaraki 305-8686,

Japan5 Plant Immunity Research Group, RIKEN Plant Science Center,

1-7-22 Suehiro-cho, Yokohama, Kanagawa 203-0045, Japan6 The Sainsbury Laboratory, John Innes Centre, Colney Lane,

Norwich NR4 7UH, UK7 Institute of Biological Sciences, Tsukuba University, Tennodai,

Tsukuba, Ibaraki, 305-8572, Japan8 Department of Biology, Tokyo Gakugei University, 4-1-1

Nukuikita-machi, Koganei-shi, Tokyo 184-8501, Japan9 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 ([email protected])

Current Opinion in Plant Biology 2006, 9:436–442

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


IntroductionPlants 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 [6–9,10��]. 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 (CuSO4) stress, and with incompatible necrotrophic

pathogen infection reveals significant 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 identified 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 bioticand abiotic stress responsesABA 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

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Crosstalk between abiotic and biotic stress responses Fujita et al. 437

Figure 1

Convergence points in abiotic and biotic stress signaling networks.

pathogen infection. In many cases, ABA acts as a negative

regulator of disease resistance [3��]. For example, the

ABA-deficient tomato mutant sitiens has increased resis-

tance to pathogens and application of exogenous ABA

restored the susceptibility of sitiens [12,13]. The sitiensmutant 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-

deficient mutants without any treatments [16��]. Taken

together with the findings 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 first identified

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 significantly reduced ABA-

responsive gene expression [18]. In addition, AtMYC2

deficiency 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 NAC transcription factor,

is another viable candidate molecule that potentially reg-

ulates aspects of both biotic and abiotic signaling. RD26expression is induced by JA, hydrogen peroxide (H2O2)

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 detoxification of ROS, defense, or senes-

cence. These findings 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 NAC gene 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


438 Biotic interactions

the repression of pathogenesis-related proteins and in

elevated susceptibility to soil-borne fungal pathogens.

Additionally, recent studies identified other molecular

entities that significantly impact crosstalk among stress-

response pathways via hormone signaling. For instance,

both nitric oxide [24] and Ca2+ 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

[25–27]. In addition, fungal elicitors can activate a branch

of the ABA signaling pathway in guard cells that regulates

plasma membrane Ca2+ channels [28]. Moreover, a bat-

tery of studies examining the induction of resistance by

the non-protein amino acid b-aminobutyric acid revealed

that ABA considerably enhances plant resistance to fungal

pathogens through its positive effect on callose deposition

[3��,29,30].

MAP-kinase cascades mediate stresssignaling crosstalkProtein phosphorylation and dephosphorylation signifi-

cantly influence 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, MEKK1–MAPK kinase 2

(MKK2)–MPK4/MPK6 cascade has been shown to func-

tion as part of cold and salt stress signaling [34��,35]. By

contrast, MEKK1–MKK4/MKK5–MPK3/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 Arabidopsiscultured cells [42]. MPK3 and MPK6 activities in ROS

signaling are affected by an Arabidopsis serine/threonine

kinase, OXI1, whose kinase activity is induced by H2O2

[43]. Also, ANP1, an Arabidopsis MAPKKK, activates

MPK3 and MPK6 via H2O2. Tobacco plants that over-

expressed constitutively active tobacco NPK1 (Nicotianaprotein 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 H2O2, specifically 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 convergencebetween biotic and abiotic stress responsepathwaysThe 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 C2H2-type zinc-

finger transcription factor, Zat12, might be a regulator in

the ROS scavenging mechanism that is involved in biotic

and abiotic stress responses. Deficiency 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



PEROXIDASE 1 (APX1) gene, which is induced by

H2O2 and increases the level of H2O2-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 [54–57]. 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 H2O2 that accumulates in

response to various stresses [10��]. These findings suggest

that the ROS might mediate crosstalk between biotic and

abiotic stress-responsive gene-expression networks.

Effects of high humidity and hightemperature upon biotic stress responsesHigh 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 [58–63], 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

H2O2 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.

ConclusionsCurrent evidence supports the concept that ROS repre-

sent a significant 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 significant 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 finding 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 significantly threatens

plant survival than does pathogen infection. To date, the

biological significance 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.

AcknowledgementsWe thank Dr K Shirasu for critical reading of the manuscript. This workwas supported in part by a grant for Genome and Plant Research fromRIKEN, by the Program for Promotion of Basic Research Activities forInnovative Biosciences from the Bio-oriented Technology ResearchAdvancement Institution of Japan (BRAIN), and by a Grant-in-Aid fromthe Ministry of Education, Culture, Sports, Science and Technology ofJapan (MEXT) to KS and KY-S.

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39. Lu C, Han MH, Guevara-Garcia A, Fedoroff NV: Mitogen-activated protein kinase signaling in post-germinationarrest of development by abscisic acid. Proc Natl Acad SciUSA 2002, 99:15812-15817.

40.��

Liu Y, Zhang S: Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsivemitogen-activated protein kinase, induces ethylenebiosynthesis in Arabidopsis. Plant Cell 2004, 16:3386-3399.

Using a sophisticated approach that encompasses biochemical andgenetic methods, the authors describe a biological function for theMKK4–MPK6 cascade in a pathogen response that regulates ethylenebiosynthesis. They found that two ACS molecules act as substrates ofMPK6, which is activated by MKK4. Phosphorylation by MPK6 leads tothe accumulation of ACS protein and to elevated levels of ACS activity invivo, consequently increasing ethylene production. This represents thefirst evidence of a direct plant MAPK phosphorylation target, and demon-strates that ethylene is biosynthesized in response to stress signaling.

41. Xiong L, Yang Y: Disease resistance and abiotic stresstolerance in rice are inversely modulated by an abscisicacid-inducible mitogen-activated protein kinase. Plant Cell2003, 15:745-759.

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43. Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L,Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H et al.:OXI1 kinase is necessary for oxidative burst-mediatedsignaling in Arabidopsis. Nature 2004, 427:858-861.

44. Kovtun Y, Chiu WL, Tena G, Sheen J: Functional analysisof oxidative stress-activated mitogen-activated proteinkinase cascade in plants. Proc Natl Acad Sci USA 2000,97:2940-2945.

45. Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS,Kim DH, Nam J, Bahk J et al.: NDP kinase 2 interacts with twooxidative stress-activated MAPKs to regulate cellular redoxstate and enhances multiple stress tolerance in transgenicplants. Proc Natl Acad Sci USA 2003, 100:358-363.

46. Laloi C, Apel K, Danon A: Reactive oxygen signaling: the latestnews. Curr Opin Plant Biol 2004, 7:323-328.

47. Guan LM, Zhao J, Scandalios JG: Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidantgene in response to ABA and osmotic stress: H2O2 is the likelyintermediary signaling molecule for the response. Plant J 2000,22:87-95.

48. Torres MA, Dangl JL, Jones JD: Arabidopsis gp91phoxhomologues AtrbohD and AtrbohF are required foraccumulation of reactive oxygen intermediates in the plantdefense response. Proc Natl Acad Sci USA 2002, 99:517-522.


49. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA,Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI:NADPH oxidase AtrbohD and AtrbohF genes function inROS-dependent ABA signaling in Arabidopsis. EMBO J2003, 22:2623-2633.

50. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F:Reactive oxygen gene network of plants. Trends Plant Sci2004, 9:490-498.

51. Bartels D, Sunkar R: Drought and salt tolerance in plants.Crit Rev Plant Sci 2005, 24:23-58.

52. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K,Shinozaki K: Engineering drought tolerance in plants:discovering and tailoring genes to unlock the future.Curr Opin Biotechnol 2006, 17:113-122.

53. Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M,Kamiya A, Nakajima M, Enju A, Akiyama K et al.: Monitoring theexpression profiles of genes induced by hyperosmotic, highsalinity, and oxidative stress and abscisic acid treatment inArabidopsis cell culture using a full-length cDNA microarray.Plant Mol Biol 2004, 56:29-55.

54. Davletova S, Schlauch K, Coutu J, Mittler R: The zinc-fingerprotein Zat12 plays a central role in reactive oxygen andabiotic stress signaling in Arabidopsis. Plant Physiol 2005,139:847-856.

55. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF:Roles of the CBF2 and ZAT12 transcription factors inconfiguring the low temperature transcriptome ofArabidopsis. Plant J 2005, 41:195-211.

56. Rizhsky L, Davletova S, Liang H, Mittler R: The zinc fingerprotein Zat12 is required for cytosolic ASCORBATEPEROXIDASE 1 expression during oxidative stress inArabidopsis. J Biol Chem 2004, 279:11736-11743.

57. Iida A, Kazuoka T, Torikai S, Kikuchi H, Oeda K: A zinc fingerprotein RHL41 mediates the light acclimatization responsein Arabidopsis. Plant J 2000, 24:191-203.

58. Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM:Evidence for a role of the N terminus and leucine-rich repeatregion of the Mi gene product in regulation of localized celldeath. Plant Cell 2000, 12:1319-1329.

59. Zhou F, Menke FL, Yoshioka K, Moder W, Shirano Y, Klessig DF:High humidity suppresses ssi4-mediated cell death anddisease resistance upstream of MAP kinase activation,H2O2 production and defense gene expression. Plant J2004, 39:920-932.

60. Xiao S, Brown S, Patrick E, Brearley C, Turner JG: Enhancedtranscription of the Arabidopsis disease resistance genesRPW8.1 and RPW8.2 via a salicylic acid-dependentamplification circuit is required for hypersensitive celldeath. Plant Cell 2003, 15:33-45.

61. Noutoshi Y, Ito T, Seki M, Nakashita H, Yoshida S, Marco Y,Shirasu K, Shinozaki K: A single amino acid insertion in theWRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-typedisease resistance protein SLH1 (SENSITIVE TO LOWHUMIDITY 1) causes activation of defense responses andhypersensitive cell death. Plant J 2005, 43:873-888.

62. Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J,Klessig DF: Environmentally sensitive, SA-dependentdefense responses in the cpr22 mutant of Arabidopsis.Plant J 2001, 26:447-459.

63. Jambunathan N, Siani JM, McNellis TW: A humidity-sensitiveArabidopsis copine mutant exhibits precocious cell deathand increased disease resistance. Plant Cell 2001,13:2225-2240.

64.�

Bieri S, Mauch S, Shen QH, Peart J, Devoto A, Casais C,Ceron F, Schulze S, Steinbiss HH, Shirasu K et al.: RAR1positively controls steady state levels of barley MLAresistance proteins and enables sufficient MLA6accumulation for effective resistance. Plant Cell 2004,16:3480-3495.

Transgenic plants expressing epitope-tagged Mla variants are used todescribe the effects of the rar1 (required for Mla resistance1) mutation upon



the abundance of the barley powdery mildew resistance R proteins MLA1and MLA6. This analysis of rar1 mutants led the authors to propose that aneffective resistance response requires a threshold level of R protein. Inaddition, the authors demonstrate that MLA protein stability decreasedunder high-temperature conditions. Transgene transcription levels and theamounts of RAR1 and SGT1 (SUPPRESSOR OF THE G2 ALLELE OF skp1-4) proteins remained unchanged during stress treatment.


65. Wang C, Cai X, Zheng Z: High humidity represses Cf-4/Avr4-and Cf-9/Avr9-dependent hypersensitive cell death anddefense gene expression. Planta 2005, 222:947-956.

66. Zimmermann P, Hennig L, Gruissem W: Gene-expressionanalysis and network discovery using Genevestigator.Trends Plant Sci 2005, 10:407-409.


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