Linking development to defense: auxin in plant–pathogen interactions

Linking development to defense:auxin in plant–pathogen interactionsKemal Kazan and John M. Manners

Commonwealth Scientific and Industrial Research Organisation (CSIRO) Plant Industry, Queensland Bioscience Precinct, St Lucia,

QLD 4067, Australia

Review

Although the plant growth hormone auxin has long beenrecognized as a regulator of plant defense, the molecularmechanisms involved are still largely unknown. Recentstudies reviewed here reveal new insights into the role ofauxin in plant defense. Similar to the signaling pathwaysof the defense-associated plant hormones salicylic acid(SA) and jasmonic acid (JA), auxin signaling differen-tially affects resistance to separate pathogen groups.Recent evidence suggests that the auxin and SA path-ways act in a mutually antagonistic manner during plantdefense, whereas auxin and JA signaling share manycommonalities. Auxin also affects disease outcomesindirectly through effects on development. Here, wediscuss the multiple ways in which auxin regulation ofplant growth and development might be intimatelylinked to plant defense.

Auxin: linking development to defensePlant hormones have essential roles in integrating devel-opmental and environmental cues into an elaborate sig-naling network that not only shapes plant architecture butalso prepares the plant to respond to potential stressesappropriately. The roles of salicylic acid (SA), jasmonic acid(JA) and ethylene in plant defense are well established, butthese so-called ‘defense hormones’ also affect amultitude ofdevelopmental processes, such as growth repression,flower development and fertility (JA) [1], flowering timeregulation (SA) [2], and senescence, fruit ripening, roothair growth and germination (ethylene) [3]. Other planthormones, such as gibberellins, auxins and brassinoster-oids, although considered to be ‘plant growth regulators’,have also been associated with plant defense andmicrobialpathogenesis [4–6]. The effects of pathogen infection onplant development (e.g. Figure 1a) have frequently beenshown to be mediated, at least in part, through planthormones [4]. These examples support the view [7–9] thatan intimate interplay exists between the hormonal regu-lation of plant growth and development and defenseagainst pathogens.

Because many plant pathogenic microorganisms pro-duce auxin (indole acetic acid [IAA]) during their inter-actions with plants, the involvement of this hormone inplant disease development has long been suspected [4,10].For instance, high levels of IAA were found in the culturemedia of the tomato (Lycopersicum esculentum) bacterialpathogenPseudomonas solanaceraumand in tobacco plantsinfected with P. solanaceraum [11,12]. After investigating

Corresponding author: Kazan, K. ([email protected]).

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the origin of IAA found in P. solanaceraum-infected tobaccoplants, it was concluded that ‘. . .during the initial criticalinteraction between host and parasite, most of the IAA iscontributed by the host’ [13]. This conclusion was based onthe then available experimental evidence that only extractsof the host plant, but not of the pathogen, could converttryptamine, an auxin precursor, to IAA. Subsequently,auxin has been shown to modulate the plant defenseresponse, and several reports have shown that auxinrepresses the expression of pathogenesis-related (PR) genes(e.g. Refs [14,15]).

Here, we review recent developments in our under-standing of how auxin might regulate host defense sig-naling and resistance mechanisms, which have beenderived from studies in model plant species such as Ara-bidopsis thaliana and rice (Oryza sativa). The involvementof auxin produced by pathogens or plants during theirinteraction with beneficial microbes will not be coveredhere, and readers interested in these aspects of auxinsignaling should consult the recent reviews on this topic[10,16].

Pathogen-elicited auxin modulates host defensePathogens have evolved sophisticated strategies to colo-nize their hosts successfully. Both animal- and plant-pathogenic bacteria use the so-called ‘type III secretionsystem’, a membrane-associated multi-protein complexthat delivers various effector proteins directly into thecytoplasm of host cells. One of the best-studied bacterialeffectors, produced by the plant-pathogenic bacteria Pseu-domonas syringae, is the AvrRpt2 avirulence or effectorprotein. Disease occurs when Arabidopsis plants areunable to recognize AvrRpt2 owing to the lack of thecorresponding disease resistance gene RESISTANT TOP. SYRINGAE2 (RPS2) [17]. Recent work has shown thatAvrRpt2, when delivered into plant cells, promotes auxinproduction [18], and this might be one of the mechanismsused by the pathogen to colonize its host (Figure 2). Evi-dence linking AvrRpt2 to the elicitation of host auxinbiosynthesis comes from rps2 Arabidopsis plants constitu-tively expressing AvrRpt2 [18]. These plants exhibit longerprimary roots, an increased number of lateral roots,reduced gravitropism and increased sensitivity to exogen-ous auxin, phenotypes that are reminiscent of auxin-over-producing plants [18]. The AvrRpt2-expressing rps2 plantsalso had elevated levels of free IAA and showed increasedsusceptibility to P. syringae compared with untransformedrps2 plants [18]. Further supporting the role of auxin in

reserved. doi:10.1016/j.tplants.2009.04.005 Available online 24 June 2009 373

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Figure 1. Reshaping of plant architecture by pathogen infection. (a) The roots of

the wild-type plant shown in (i) were treated with water, whereas the roots of the

wild-type plant shown in (ii) were inoculated with the root-infecting fungal

pathogen Fusarium oxysporum. The photographs were taken 15 days after the

inoculations. Although both plants contain a similar number of rosette leaves, leaf

sizes and petiole lengths are reduced in the inoculated plant (ii). (b) The role of auxin

transport in plant development and disease resistance. The BIG/TIR3 (TRANSPORT

INHIBITOR RESPONSE3)/ASA1 (ATTENUATED SHADE AVOIDANCE1) gene of

Arabidopsis encodes a calossin-like protein that is required for polar auxin

transport [60]. The big/tir3/asa1 mutant (i) shows morphological defects, but

compared with wild-type plants (ii), it also shows increased resistance to the root-

infecting fungal pathogen F. oxysporum, which suggests a link between auxin

transport and disease resistance.

Review Trends in Plant Science Vol.14 No.7

P. syringae pathogenesis, the treatment of wild-type Ara-bidopsis plants with auxin during inoculation with P.syringae led to a substantial increase in disease symptomdevelopment [18].

Although these findings indicate that AvrRpt2-elicitedauxin biosynthesis in the host might be one of the strat-egies used by P. syringae to promote disease on Arabidop-sis, the precise mechanism(s) of how AvrRpt2 triggersauxin production is currently unknown. It has beensuggested [18] that the effect of AvrRpt2-elicited auxinon disease development occurs independently from SAsignaling or accumulation because a previous report indi-cated that AvrRpt2 virulence activity functions indepen-dently or downstream from SA [19]. However, AvrRpt2 isimplicated in the suppression of SA-responsive PR genesknown to be effective against this pathogen [19]. Therefore,one possibility would be that AvrRpt2, by causingelevations in auxin levels, effectively suppresses the SA-dependent defenses and promotes disease development(Figure 2). Indeed, several recent studies reviewed belowhave suggested an antagonistic crosstalk between auxinand SA signaling during plant defense.

Defense versus development: antagonistic crosstalkbetween SA and auxin signalingRecent evidence indicates that SA inhibits pathogengrowth partly through the suppression of auxin signaling.Several lines of evidence support this view. First, the SAanalog BTH (benzothiadiazole-s-methyl ester) downregu-lates the expression of a significant number of genes

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involved in auxin transport, reception and response [20].The expression of most of these BTH-responsive auxinresponsive genes also depends on NPR1 (NONEXPRES-SER OF PR GENES1), a gene regulating systemicacquired resistance (SAR) [20]. In addition, SA treatmentofDR5 GUS plants represses the b-glucuronidase reportergene expression driven by the auxin-responsive DR5 pro-moter, suggesting that SA suppresses auxin biosynthesis.Arabidopsis mutants with high levels of endogenous SAhad relatively low IAA levels and also showed reducedsensitivity to exogenous auxin [20]. Finally, the auxinsignalingmutant axr2 (auxin resistant2) (Figure 2) showedincreased resistance to P. syringae, suggesting that anintact auxin signaling pathway promotes susceptibilityto this pathogen [20].

Interestingly, SA and auxin signaling seem to bemutually antagonistic because auxin suppresses SA-de-pendent defenses, such as PR1 expression [20–22], andSA-deficient plants (i.e. nahG plants expressing the bac-terial gene for the SA-degrading enzyme salicylate hydox-ylase) show increased IAA levels [23]. The evolutionaryreasons behind the antagonistic interactions between SAand auxin signaling might be that plants divert limitedresources to defense-related processes at the expense ofplant growth when attacked by a pathogen.

Auxin receptors: a convenient target for modification bydefense signalsHow does SA repress or interfere with auxin signaling?One of the mechanisms involved in SA action seems tobe the transcriptional repression of the genes encodingauxin receptors, such as TIR1 (TRANSPORT INHIBITORRESPONSE1) and related F-box proteins [20]. Repressionof these auxin receptors, which facilitates auxin-dependentdegradation of the AUX/IAA (AUXIN/INDOLE ACETICACID) repressors, would lead to the stabilization of AUX/IAA and the maintenance of their repressive effects onauxin response genes and inhibition of disease develop-ment (Figure 2).

In addition to SA, at least one more pathogen-respon-sive plant component targets auxin receptors. A recentreport showed that the recognition of conserved bacterialflagellin (flg22) from P. syringae activates the expression ofthe microRNA miR393, which then downregulates theexpression of the auxin receptor genes TIR1 (Figure 2)and AUXIN F-BOX PROTEINS (AFB2 and AFB3) [24].This leads to the suppression of auxin-responsive geneexpression and reduced disease development. Furthersupporting the role of TIR1 and auxin signaling in bac-terial pathogenesis, the tir1 mutant shows increasedresistance to P. syringae [24] (Table 1). However, SA-mediated repression of TIR1 seems to be acting indepen-dently from that ofmiR393 because no induction ofmiR393by SA was observed [20].

The involvement of the auxin receptor in plant defenseis not restricted to the examples discussed above.When the3D structure of the auxin receptor was resolved, a singleinositol hexakisphosphate (InsP6) molecule was foundto be associated with the receptor, possibly acting as acofactor stabilizing the structure of the auxin-bindingpocket within the LRRs (leucine-rich repeats) of TIR1

Table 1. Auxin genes involved in regulating plant defense and disease resistance in Arabidopsis and rice

Gene Function in auxin signaling Function in plant defense Developmental phenotypes Refs

ALH1 ACC-RELATED LONG

HYPOCOTYL 1 is implicated in the

regulation of crosstalk between

auxin and ethylene at the level of

auxin transport

alh1 mutant shows increased resistance

to clubroot caused by

Plasmodiophora brassicae

alh1 mutant has long hypocotyls

in the absence of hormones and

shows reduced auxin sensitivity

[74,75]

AUX1 Encodes an auxin influx carrier

involved in polar auxin transport

aux1 mutant is compromised in its ability

to develop induced resistance against

Botrytis cinerea

aux1 mutant shows resistance

to auxin, slight increase in root

elongation and altered gravitropic

response

[58,59]

AXR1 Encodes a protein related to

ubiquitin-activating enzyme E1

axr1 mutant shows increased susceptibility

to B. cinerea and Pythium irregulare

but increased resistance to Pseudomonas

syringae and pathogenic Agrobacterium

tumefaciens and A. rhizogenes

axr1 mutants show developmental

defects, such as decreases in

plant height, root gravitropism,

hypocotyl elongation and fertility

[33,59,76,77]

AXR2/IAA7 Encodes IAA7, a member of the

AUX/IAA protein family

Increased susceptibility to the necrotrophic

fungi Plectosphaaerella cucumerina and

B. cinerea

axr2 mutation causes agravitropic

root and shoot growth, a short

hypocotyl and stem and

auxin-resistant root growth

[32,78,79]

AXR3 Encodes the AUX/IAA protein

IAA17

Increased tolerance to clubroot caused by

P. brassicae

axr3 mutant shows enhanced

apical dominance, reduced root

elongation and increased

adventitious rooting

[80,81]

AXR6/CUL1 Encodes CULLIN1, a component

of SCF ubiquitin ligase complex

Increased susceptibility to P. cucumerina

and B. cinerea

axr6 mutants show attenuated

auxin and jasmonate phenotypes,

lack roots and hypocotyl and

show severe vascular defects

in their cotyledons

[32,47,82]

BIG/TIR3 Encodes a calossin-like protein

functioning in auxin transport

Increased resistance to the root-infecting

fungal pathogen Fusarium oxysporum

Umbrella-like growth habit [60]

BUD1/MKK7 Encodes an MKK that is a negative

regulator of PAT

Positive regulator of SA biosynthesis and

signaling

Activated expression of MKK7

in the bud1 mutant results in

bushy and dwarf plants

[56,57]

GH3.5/WES1 Encodes an IAA-amido synthase

that conjugates IAA to amino acids

Required for elevated accumulation of SA

and increased expression of PR-1 in

response to pathogens. wes-D/gh3.5-1D

activation mutant accumulates high

levels of free IAA and shows increased

resistance to P. syringae

wes1-D/gh3.5-1D activation

mutant shows a dwarf growth

habit

[22,83]

GH3.6/DFL1 Encodes an IAA-amido synthase that

conjugates IAA to amino acids

dfl1-d with an activated GH3.6 gene shows

upregulated expression of PR genes and

increased resistance to P. syringae

dfl.1 mutant displays shorter

hypocotyls

[83]

GLIP2 Encodes a GDS-like lipase 2;

implicated in negative regulation

of auxin signaling

GLIP2 is required for resistance to

Erwinia carotovora

glip2 mutant shows increased

lateral root formation and

elevated AUX/IAA gene

expression and increased

susceptibility to E. carotovora

[84]

NIT1 and

NIT2

NIT1 catalyzes the terminal

activation step in IAA

biosynthesis; NIT2 catalyses

the hydrolysis of IAN to IAA

NIT1 and NIT2 are required for clubroot

(P. brassicae) susceptibility

No developmental alterations in

NIT1 and NIT2 antisense plants

[85]

OsGH3.1 Encodes an IAA-amido

synthetase that conjugates

IAA to amino acids

Required for pathogen-inducible PR1

expression and resistance to the fungal

pathogen M. grisea; overexpression of

GH3.1 results in enhanced disease

resistance to the bacterial pathogen

Xanthomonas oryzae pv oryzae

OsGH3.1-overexpressing plants

show severely reduced plant

height

[64]

OsGH3.8 Encodes a putative IAA-amido

synthetase

Required for pathogen-inducible PR1

expression and resistance to the fungal

pathogen M. grisea; overexpression of

GH3.8 results in enhanced disease

resistance to the bacterial pathogen

X. oryzae pv oryzae

OsGH3.8-overexpressing plants

show abnormal plant morphology

and retarded growth and

development

[21]

OsWRKY31 Encodes a WRKY transcription

factor

OsWRKY31 overexpression enhances

resistance against Magnaportha grisea

OsWRKY31-expressing lines

show reduced lateral root

formation and elongation

[86]

IAA26 Encodes IAA26, an AUX/IAA

repressor

Required for susceptibility to tobacco

mosaic virus

Inhibition of IAA26 expression by

RNAi leads to developmentally

altered plants

[50]

SGT1b Regulates auxin responses;

involved in TIR1-mediated

degradation of AUX/IAA proteins

Required for resistance to

Hyaloperonospora parasitica and

susceptibility to F. culmorum

Required for auxin sensitivity;

the sgt1b mutant is less sensitive

to root inhibition by auxin

[34–36]


375

Table 1 (Continued )Gene Function in auxin signaling Function in plant defense Developmental phenotypes Refs

TIR1 Encodes an F-box protein involved

in auxin reception

Required for susceptibility to

P. syringae

tir1 mutants show reduced auxin

sensitivity

[24,87]

TU3 and

TU8/TFL2

TU3 catalyzes the formation of

aliphatic glucosinolate chain

lengths. TU8 encodes

heterochromatin protein 1 homolog

TERMINAL FLOWER 2

TU3 and TU8 show decreased clubroot

disease development and decreased IAA

accumulation

tu8 mutant has shorter stems/dwarf

and altered branching pattern

[88,89]


376


[25]. A recent report found that Arabidopsis plantsdepleted in InsP6 owing to amutation in the gene encodingInsP5 2-kinase, an enzyme catalyzing the final step ofInsP6 biosynthesis, were hypersusceptible to several viral,bacterial and fungal pathogens [26]. Although, the exactmode of action of InsP6 in auxin or defense gene expressionis currently unknown, this observation suggests anotherputative link among auxin reception, signaling anddefense responses.

Defense versus development: biosynthetic pathwaybranch points for auxin and defense compoundsThe interplay between defense and auxin-mediated plantdevelopment is also evident in the way that auxin anddefense-related antimicrobial secondary metabolites, suchas indole-glucosinolates (IGs) and the phytoalexin cama-lexin, are produced through the same tryptophan pathway(Figure 2) [27]. Indole-3-acetaldoxime (IAOx) acts as anintermediate for IAA as well as for IGs and camalexinproduction, thus linking development to pathogen defense(Figure 2). Genetic analyses showed that when the IGbiosynthesis pathway is blocked downstream from IAOxowing to mutations in genes encoding the IG biosyntheticenzymes SUR1 (SUPERROOT1; 7:C-S lyase) and SUR2(SUPERROOT2; CYP83B1), IAOx is diverted to IAA pro-duction (Figure 2) [28,29]. TheArabidopsis sur1mutant, forinstance, cannot synthesize IGs and shows underaccumula-tion of camalexin but overaccumulation of IAA [28,29].

Finally, flavonoids, the plant secondary metabolitesthat accumulate in plant tissue under a variety of bioticand abiotic stress conditions, inhibit polar auxin transport(PAT) [30] and plant growth [31]. This further indicatesthat plants have developed branch points and interactionsin themetabolic pathways controlling the biosynthesis andaccumulation of growth hormones and antimicrobial com-pounds so that a sustained defense response can be main-tained at the expense of growth, which can then beresumed once a threat from a pest or pathogen is success-fully averted.

Differential effects of auxin signaling on different fungalpathogensThe modulation of host auxin signaling during plantdefense is not restricted to bacterial pathogens. Infection

Figure 2. Auxin biosynthesis, metabolism and signaling and their interaction with defen

meristematic tissues, and four auxin biosynthetic pathways have been identified in Arab

(tryptamine) pathway; and the IAM (indole-3-acetamide) pathway [90–92]. Cellular aux

auxin-inducible GH3 genes encoding auxin-conjugating IAA-amido synthetases mod

hydrolysis of IAA:aa by IAA amino acid hydrolyse (IAR) can rapidly generate free IAA and

such as IGs and camalexin, are also synthesized from the same tryptophan pathway. Elic

elicit auxin biosynthesis to promote disease development. Detection of the bacterial flag

receptor gene TIR1. This leads to the stabilization of AUX/IAA repressors and subsequ

disease development. Auxin transport: the movement of auxin from the initial point

development; interrupting auxin transport processes by genetic or chemical means lea

plant through the phloem (non-polar or bidirectional transport) and from cell to cell in a

transporter proteins located in the plasma membrane: (i) auxin efflux carriers, PIN and P

carriers (AUXs), which transport IAA into the cell. As discussed in main text, auxin

signaling: auxin is sensed through the redundantly acting F-box proteins TIR1, AFB1,

ubiquitin ligase complex, and mutations in genes encoding auxin receptors or core SCF

certain threshold, auxin responses are inhibited by a family of repressors called AUX/I

responsive gene expression through interaction with the ARE, a conserved sequence fo

binding of auxin to its receptor facilitates the ubiquitin-mediated degradation of AUX/I

auxin responses are activated. (See Refs [39,62,63,90–94] for additional information

RESISTANCE PROTEIN1; ASK1, ARABIDOPSIS SKP1 HOMOLOGUE1; E2-u, E2 UBIQ

acetonitrile; NIT, nitrilase; PAD3, PHYTOALEXIN DEFICIENT3; RBX1, RING-BOX1; TAA1,

2, TRYPTOPHAN AMINOTRANSFERASE RELATED1 and 2; TMO, tryptophan monooxyg

of Arabidopsis by Botrytis cinerea, a necrotrophic fungalpathogen, also leads to altered expression of key genesinvolved in auxin signaling [32]. In addition to repressingnumerous AUX/IAA- and ARF (AUXIN RESPONSE FAC-TOR)-encoding genes, B. cinerea repressed the auxin-re-ceptor-encoding gene TIR1 and the AUX/IAA-repressor-encoding genes AXR2 (AUXIN RESISTANT2)/IAA7 andAXR3 (AUXIN RESISTANT3)/IAA17 [32]. However, incontrast to the interaction between Arabidopsis and P.syringae, where host auxin signaling imparts susceptibility[20], an intact auxin signaling is required for resistance toB. cinerea and Plectosphaerella cucumerina, another leaf-infecting necrotrophic pathogen. The Arabidopsis auxin-signaling mutants axr1, axr2 and axr6, which are com-promised in the SCF (SKP1/CULLIN/F-box protein)-mediated ubiquitination pathway (Figure 2), also showan increased susceptibility to these necrotrophic pathogens[32]. The axr1 mutant was also shown to be susceptibleto the root-infecting necrotrophic oomycete pathogenPythium irregulare [33] (Table 1).

Another important component of auxin signaling that isrequired for the TIR1-mediated degradation of AUX/IAA isthe SGT1b (SUPPRESSOR OF G2 ALLELE OF SKP1)protein (Figure 2) [34]. SGT1b is required for resistance tothe biotrophic fungal pathogen Hyaloperonospora parasi-tica, because mutations in this gene cause increasedsusceptibility to this biotrophic pathogen [35]. By contrast,the sgt1b mutant shows increased susceptibility to thenecrotrophic fungal pathogen Fusarium culmorum [36].These examples suggest that auxin signaling is requiredfor resistance against necrotrophs but imparts suscepti-bility against biotrophs (Figure 3).

Defensive roles of auxin and JA signaling: both for oneand one for both?In contrast to the antagonistic interaction between SA andauxin signaling, JA and auxin signaling share many com-monalities and interact positively in most instances wherethey have been studied. Similarly to auxin signaling, JAsignaling is known to be generally antagonistic to SAsignaling [37,38]. The requirement of auxin signaling inmediating resistance to necrotrophic pathogens is alsosimilar to that of JA signaling. Both JA and auxin signalsare perceived and transmitted through signaling pathways

se-related components in Arabidopsis. Auxin biosynthesis: auxin is synthesized in

idopsis so far: the IAOx pathway; the IPA (indole-3-pyruvic acid) pathway; the TAP

in homeostasis is also regulated by auxin metabolism and transport. A group of

ulates auxin levels by conjugating IAA to amino acids (IAA:aa). The enzymatic

help maintain auxin homeostasis. Certain defense-related secondary metabolites,

itors, such as AvrRpt2 derived from the bacterial pathogen Pseudomonas syringae,

ellin (flg22) activates a microRNA (miR393) that inhibits the expression of the auxin

ent suppression of the auxin-responsive gene expression that promotes bacterial

of synthesis to other parts of the plant is required for normal plant growth and

ds to altered auxin levels and growth defects. Auxin is distributed throughout the

polarity-dependent manner (PAT). PAT is mediated mainly by two major groups of

-glycoprotein (ABCB/PGP), which transport IAA out of the cell; and (ii) auxin influx

transport differentially affects defense against different pathogen groups. Auxin

AFB2 and AFB3. These auxin receptors function as part of a nuclear-located SCF

subunits reduce auxin sensitivity. When cellular auxin concentrations are below a

AA proteins. AUX/IAA repressors inhibit ARFs required for the activation of auxin-

und in the promoters of auxin responsive genes. Under high auxin concentrations,

AA repressors, and this releases ARFs from transcriptional repression. As a result,

.) Abbreviations: ABCB1/MDR1, ATP-binding cassette sub-family B/MULTIDRUG

UITIN-CONJUGATING ENZYME; FLS2, FLAGELLIN-SENSITIVE2; IAN, Indole-3-

TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1; TAM, tryptamine; TAR1,

enase; u, ubiquitin.

377

Figure 3. A proposed model of interactions between auxin and plant defense signaling and response pathways. The auxin pathway interacts with defense pathways at

multiple points. Both auxin and defense-related compounds, such as camalexin and IGs, are synthesized from tryptophan and, as discussed in the main text, mutations

blocking the synthesis of defense compounds, such as IGs, led to increased auxin production. Auxin biosynthesis, transport and signaling antagonize SA biosynthesis and

signaling that is required for resistance to biotrophic pathogens. By contrast, auxin and JA signaling share common components and both are required for resistance to

necrotrophic pathogens. Auxin responses also modulate disease development through their effects on development, such as cell wall modifications (see main text for

details).


where F-box proteins (TIR1 and COI1 [CORONATINEINSENSITIVE1] for auxin and JA, respectively) and sig-nal-mediated ubiquitination of repressors (AUX/IAA andJAZ [JASMONATE ZIM DOMAIN] proteins for auxin andJA signaling, respectively) are required for activation ofdownstream responses [39]. Both TIR1 and COI1 arerequired for resistance to necrotrophic pathogens and forsusceptibility to P. syringae [24,40]. Mutations in genesencoding components of the core SCF complex, such asAXR1 (AUXIN RESISTANT1), SGT1b and AXR6/CUL1(CULLIN1), and various signaling components, such asMYC2, ARF6 (AUXIN RESPONSE FACTOR6), ARF8,JAR1 (JASMONATE RESISTANT1; GH3.11) and GH3.9,affect both JA and auxin signaling [33,41–47]. Based on thisbody of evidence, models have been proposed [5,48] toexplain potential signaling interactions among SA, JAand auxin signaling during plant defense. As shown inFigure 3, SA and JA and SA and auxin act in a mutuallyantagonistic manner, whereas JA and auxin interact posi-tively with each other.

Modulation of host auxin signaling by viral pathogensand phytoplasmaPlants infected with viruses often show severe develop-mental abnormalities, such as stunting, leaf curling andloss of apical dominance. These developmental abnormal-ities often resemble mutants with compromised auxinbiosynthesis and/or signaling, leading to the view thatviral infection could alter host auxin homeostasis and/orsignaling in plant cells. Tobacco mosaic virus (TMV)

378

infection of Arabidopsis plants results in transcriptionalreprogramming of a large number of auxin-responsivegenes that contain the conserved TGTCTC-auxin respon-sive element (ARE) in their promoters [49]. The TMVreplicase protein responsible for cell-to-cell movement ofthe virus interacts with the Arabidopsis AUX/IAA proteinIAA26, preventing the localization of IAA26, as well as therelated AUX/IAAs IAA18 and IAA27, to the nucleus.Further supporting the role of IAA26 in plant develop-ment, RNA interference (RNAi)-mediated inhibition ofIAA26 results in similar morphological abnormalities tothose caused by TMV infection [49–51]. Because AUX/IAArepressors inhibit auxin-responsive gene expression in theabsence of auxin signal (Figure 2), the inability of IAA18,IAA26 and IAA27 to suppress auxin-responsive geneexpression seems to be one of the reasons behind theconstitutive expression of auxin-responsive genes andthe cause of at least some of the morphological abnormal-ities observed in TMV-infected plants [50,51].

Phytoplasma (phytopathogenic bacteria that requireliving plant tissue to survive) infection also leads to thedevelopment of small and short branches in the infectedplants. This distorted plant phenotype is known as ‘witch’sbroom’ [52]. More recently, a unique virulence factor,TENGU, named after the mythical Japanese goblin oncebelieved to make witch’s-broom-like nests, was identifiedfrom phytoplasma [53]. TENGU is a small secreted peptideof 38 amino acids and is able to move through the phloemtissue to the apical meristem [53], where auxin is synthes-ized. Transgenic expression of TENGU in Nicotiana


benthamiana andArabidopsis led to thewitch’s-broom-likephenotypes reminiscent of phytoplasma-infected plants.Several auxin-related genes were also found to be down-regulated in TENGU-expressing Arabidopsis plants, lead-ing to the proposal that TENGU interferes with the auxinsignaling pathway to produce the plant architecture seenin phytoplasma-infected plants [53].

Auxin transport and disease resistanceEmerging evidence indicates that the inhibition of auxintransport, either by the application of auxin transportinhibitors or by the use of mutants affected in auxintransport, also differentially affects resistance to differentpathogen groups. As early as 1954, it was observed [54]that the application of the auxin transport inhibitor 2,3,5-triiodobenzoic acid (TIBA) prior to inoculations increasedthe resistance of tomato plants to Fusarium wilt diseasecaused by the root-infecting hemibiotrophic pathogen F.oxysporum. By contrast, the inhibition of auxin transportby TIBA prior to inoculation by the leaf-infecting necro-troph P. cucumerina increases the susceptibility of plantsto this pathogen [32]. The differential effect of TIBA ondifferent pathogens seems to be associated with its differ-ential effect on SA and JA signaling pathways. In wild-typeArabidopsis, TIBA treatment leads to a stronger inductionof PR1 upon inoculation in an SA-dependent mannerbecause the induction of PR1 in nahG plants that areunable to accumulate SA was abolished after either TIBAtreatment or P. cucumerina inoculation. By contrast,pathogen-dependent expression of PDF1.2, a marker genefor the JA pathway, was suppressed by TIBA [32]. BecauseJA signaling often conditions resistance to necrotrophicpathogens [55], negative effects of TIBA on JA-responsivedefense gene expression might provide a plausible expla-nation for why TIBA-treated plants show an increasedsusceptibility to necrotrophic pathogens.

Genetic analysis also supports a role for auxin transportin modulating plant defense. BUD1/MKK7 (BUSHYDWARF1/MAP KINASE KINASE7) is a negative regula-tor of PAT [56] but positively affects SA signaling [57]. Thebud1 mutant containing an activation-tagged BUD1/MKK7 allele shows increased SA levels, constitutiveexpression of PR genes and increased resistance to bothP. syringae andH. parasitica. By contrast, reducing BUD1expression by RNAi compromised basal resistance topathogens and induction of SAR [57]. The Arabidopsisaux1 (auxin resistant1) mutant, which is compromised inAUX1-mediated auxin influx [58], was unable to developTrichoderma-mediated induced resistance against B.cinerea [59]. Finally, mutations in the BIG gene (alsoknown as TIR3 and ASA1), which encodes a calossin-likeprotein involved in auxin transport, increase [60] resist-ance to F. oxysporum (Figure 1b). Thus, in agreement withthe model proposed in Figure 3, interfering with auxintransport seems to positively affect SA signaling andresistance to biotrophic pathogens but to negatively affectJA signaling and resistance to necrotrophic pathogens.

Several proteins function in auxin efflux transport(Figure 2). So far, there has not been any report showinga role for these proteins in disease resistance. This mightbe due to the functional redundancy of auxin efflux

proteins. Nevertheless, a recent report shows that the cystnematode Heterodera schachtii takes advantage of theauxin distribution network of the host, as modulated bythe PIN1 (PIN-FORMED1), PIN3 and PIN4 proteins, tofacilitate the infestation of plant roots and cause gallformation [61].

Auxin metabolism and disease resistanceAs discussed earlier, conjugating IAA to amino acids is oneof the ways that plants maintain auxin homeostasis [62].IAA–amino acid conjugates are either stored and thenconverted to free IAA when needed or, depending on theparticular amino acid used in conjugation, are sent fordegradation [63]. Several members of theGH3 gene familyencode IAA-conjugating enzymes, and plants constitu-tively expressing some of these genes show activateddefense responses. For instance, the wes1-D Arabidopsismutant, in which expression of the WES1 gene (whichencodes the GH3.5 enzyme) is activated, shows growthretardation, increased auxin and SA levels, increasedexpression of the PR1 gene and increased resistance toP. syringae [22]. Increased PR1 expression in this mutantwas SA-independent because PR1 expression remainedhigh in a wes1-D nahG cross [22]. However, co-treatmentof wild-type plants with auxin and SA resulted in theattenuation of SA-induced PR1 expression, providingfurther support for the proposed antagonism betweenSA and auxin pathways [22] (Figures 2,3).

A similar effect of a GH3 gene on endogenous auxinlevels and disease resistance has also been recentlyobserved in rice. Overexpression of the OsGH3.8 generesulted in reduced levels of free IAA and enhanced diseaseresistance to the bacterial rice pathogen Xanthomonasoryzae pv. oryzae (Table 1). Like the disease-promotingeffects of endogenous auxin during P. syringae pathogen-esis in Arabidopsis, exogenous auxin treatment increasedthe susceptibility of rice to X. oryzae [21]. However, theOsGH3.8-mediated resistance to X. oryzae seems to beindependent from SA- and JA-dependent defenses [21].It was proposed thatX. oryzae-induced auxin accumulationwould cause loosening of the plant cell wall by activatingexpansins, a group of cell-wall-modifying enzymes. Whenendogenous auxin levels are low, the reduced ability ofexpansins to modify the cell wall would also be comprom-ised. This, in turn, would reduce the ability of the host cellwall to defend the plant successfully during pathogenattack [21].

More recently, the effect of another GH3 gene in themodulation of auxin levels and disease resistance has beeninvestigated in rice. Similarly to the OsGH3.8 gene dis-cussed above, the constitutive expression ofOsGH3.1 led toreduced auxin levels, severely shortened plant height andenhanced resistance to the fungal pathogen Magnaporthagrisea [64]. However, in contrast to the overexpression ofOsGH3.8, where no effect of overexpression on defensegene expression was found, OsGH3.1-overexpressingplants showed upregulated expression of PR genes [64].Again, these results are consistent with a role of auxin innegatively regulating SA-dependent defenses. Interest-ingly, however, exogenous application of auxin onto wild-type plants did not affectM. grisea lesion development. This

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finding led the authors to propose that the increaseddiseaseresistance observed in OsGH3.1-expressing plants was notdirectly caused by activated defense responses [64].

Conclusions and future questionsRecent studies reviewed here provide strong support forthe view that several aspects of the auxin pathway cross-talk with those of the SA and JA pathways, leading toeither increased resistance or susceptibility to differentpathogens. The availability of large-scale gene expressiondata that show cross-regulation of auxin-responsive genesduring plant defense [20,65] and the availability of a largenumber of Arabidopsis mutants defective in almost everyaspect of auxin-related processes have been instrumentalfor testing these new hypotheses. In addition, transgenicplants expressing the auxin responsive promoter–reportergene constructs (e.g. DR5 GUS) [20] have provided aconvenient way to monitor changes in auxin responsesduring plant defense. As a result, a convincing case forauxin signaling in the modulation of plant defense isemerging. However, several questions, some of whichare briefly outlined below, still need to be answered.

What is the molecular mechanism(s) of auxin action in

plant defense?

It is likely that auxin and/or its signaling pathway modu-lates plant disease resistance both directly and indirectly.Direct effects of auxin might involve interference withplant defense circuitry (e.g. SA signaling), whereas indirecteffects might involve changes in the progression of host–pathogen interactions and disease resistance caused by theeffect of auxin on plant development. In fact, most, if notall, auxin mutants, as well as plants overexpressing var-ious regulators of auxin signaling with altered diseaseresistance phenotypes, also show developmental altera-tions (Table 1). Because auxin promotes cell elongation,several auxin mutants show defects in this process. Suchdefects could interfere with the infection processes ofpathogens that interact with the cell wall and colonizethe extracellular spaces. The influence of auxin signalingon the distribution and opening of stomata has also beenreported [66,67]. Stomata are potential entry points forpathogens [68], and alterations in the stromata could havea significant effect on the plant’s resistance to pathogens,such as P. syringae, that enter through the stomata [69].Also, several auxin mutants show defects in lateral root,root hair and vascular tissue development. Many soil-borne pathogens infect the roots through auxin-richregions, such as root tips and lateral root initials [68].Therefore, such developmental alterations in plant rootarchitecture or vascular tissue could restrict pathogenentry into the roots and/or movement within the plant.

How does crosstalk of auxin with other defense

signaling pathways affect plant disease resistance?

The potential crosstalk between auxin and other hormonalsignaling pathways, such as SA, JA, ethylene, cytokinins,gibberellins and brassinosteroids, presents another layerof complexity and can affect both plant defense anddevelopment. A recent comprehensive transcriptomeanalysis of auxin responses in Arabidopsis has shown that

380

auxin regulates the expression of genes associated with thebiosynthesis, catabolism and signaling pathways of otherhormonal pathways [70]. Thus, it is possible that at leastsome of the defensive effects attributed to auxin signalingare at least partly executed by the signaling pathway(s) ofanother plant hormone.

How does auxin transport affect plant disease

resistance?

The mechanism by which TIBA or auxin transport inhibi-tors might alter defense gene expression and diseaseresistance also requires further investigation. Inhibitorsof PAT would affect disease resistance not only throughtheir effects on defense gene expression but also by alteringcell wall properties, which can then lead to the simul-taneous activation of defense responses [71]. A recentreport showed that auxin transport inhibitors, includingTIBA, act to impair vesicle trafficking and cytoskeletondynamics in plant cell walls [72]. This might interfere withthe polarized trafficking and secretion of defense-relatedcompounds known to be important during pathogenpenetration [73].

In conclusion, despite some significant progress madeover the recent years, we are only just beginning to under-stand how plants might integrate diverse endogenous andexogenous signals during their adaptive responses.Undoubtedly, future research on auxin and other hormo-nal signaling pathways involved in plant development willreveal the innovative ways that plants adapt their bioticenvironment and maximize their chances of survival.

AcknowledgementsWe apologize to colleagues whose work could not be cited owing to spacerestrictions and thank Narendra Kadoo, Brendan Kidd and LouiseThatcher for useful comments on the manuscript.

References1 Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal

transduction and action in plant stress response, growth anddevelopment. Ann. Bot. (Lond.) 100, 681–697

2 Martınez, C. et al. (2004) Salicylic acid regulates flowering time andlinks defense responses and reproductive development. Plant J. 37,209–217

3 Abeles, F.B. et al. (1992)Ethylene in Plant Biology. (2nd edn), AcademicPress

4 Yamada, T. (1993) The role of auxin in plant-disease development.Annu. Rev. Phytopathol. 31, 253–273

5 Robert-Seilaniantz, A. et al. (2007) Pathological hormone imbalances.Curr. Opin. Plant Biol. 10, 372–379

6 Navarro, L. et al. (2008) DELLAs control plant immune responses bymodulating the balance of jasmonic acid and salicylic acid signaling.Curr. Biol. 18, 650–655

7 Potters, G. et al. (2007) Stress-induced morphogenic responses:growing out of trouble? Trends Plant Sci. 12, 98–105

8 Agnew, P. et al. (2000) Host life history responses to parasitism.Microbes Infect. 2, 891–896

9 Korves, T.M. and Bergelson, J. (2003) A developmental response topathogen infection in Arabidopsis. Plant Physiol. 133, 339–347

10 Spaepen, S. et al. (2007) Indole-3-acetic acid in microbial andmicroorganism-plant signaling. FEMS Microbiol. Rev. 31, 425–448

11 Sequeira, L. and Kelman, A. (1962) Accumulation of growth substancesin plants infected by Pseudomonas solanacearum. Phytopathology 52,439–448

12 Sequeira, L. andWilliams, P.H. (1964) Synthesis of indoleacetic acid byPseudomonas solanacearum. Phytopathology 54, 1240–1246

13 Sequeira, L. (1965) Origin of indoleacetic acid in tobacco plants infectedby Pseudomonas solanacearum. Phytopathology 55, 1232–1236


14 Shinshi, H. et al. (1987) Regulation of a plant pathogenesis-relatedenzyme: inhibition of chitinase and chitinase mRNA accumulation incultured tobacco tissues by auxin and cytokinin. Proc. Natl. Acad. Sci.U. S. A. 84, 89–93

15 Jouanneau, J.P. et al. (1991) In plant protoplasts, the spontaneousexpression of defense reactions and the responsiveness to exogenouselicitors are under auxin control. Plant Physiol. 96, 459–466

16 Mathesius, U. (2008) Auxin:at the root of nodule development? Funct.Plant Biol. 35, 651–668

17 Kunkel, B.N. et al. (1993) RPS2, an Arabidopsis disease resistancelocus specifying recognition of Pseudomonas syringae strainsexpressing the avirulence gene avrRpt2. Plant Cell 5, 865–875

18 Chen, Z. et al. (2007) Pseudomonas syringae type III effector AvrRpt2alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. U.S. A. 104, 20131–20136

19 Chen, Z. et al. (2004) The Pseudomonas syringae type III effectorAvrRpt2 functions downstream or independently of SA to promotevirulence on Arabidopsis thaliana. Plant J. 37, 494–504

20 Wang, D. et al. (2007) Salicylic acid inhibits pathogen growth in plantsthrough repression of the auxin signaling pathway. Curr. Biol. 17,1784–1790

21 Ding, X. et al. (2008) Activation of the indole-3-acetic acid amidosynthetase GH3-8 suppresses expansin expression and promotessalicylate- and jasmonate-independent basal immunity in rice. PlantCell 20, 228–240

22 Park, J.E. et al. (2007) GH3-mediated auxin homeostasis links growthregulation with stress adaptation response in Arabidopsis. J. Biol.Chem. 282, 10036–10046

23 Abreu, M.E. and Munne-Bosch, S. (2009) Salicylic acid deficiency inNahG transgenic lines and sid2 mutants increases seed yield in theannual plant Arabidopsis thaliana. J. Exp. Bot. 60, 1261–1271

24 Navarro, L. et al. (2006) A plant miRNA contributes to antibacterialresistance by repressing auxin signaling. Science 312, 436–439

25 Tan, X. et al. (2007) Mechanism of auxin perception by the TIR1ubiquitin ligase. Nature 446, 640–645

26 Murphy, A.M. et al. (2008) A role for inositol hexakisphosphate in themaintenance of basal resistance to plant pathogens. Plant J. 56, 638–

65227 Grubb, C.D. and Abel, S. (2006) Glucosinolate metabolism and its

control. Trends Plant Sci. 11, 89–10028 Mikkelsen, M.D. et al. (2004) Arabidopsis mutants in the C-S lyase of

glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J. 37, 770–777

29 Glawischnig, E. et al. (2004) Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondarymetabolism in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 101, 8245–

825030 Peer, W.A. and Murphy, A.S. (2007) Flavonoids and auxin transport:

modulators or regulators? Trends Plant Sci. 12, 556–56331 Besseau, S. et al. (2007) Flavonoid accumulation in Arabidopsis

repressed in lignin synthesis affects auxin transport and plantgrowth. Plant Cell 19, 148–162

32 Llorente, F. et al. (2008) Repression of the auxin response pathwayincreasesArabidopsis susceptibility to necrotrophic fungi.Mol. Plant 1,496–509

33 Tiryaki, I. and Staswick, P.E. (2002) An Arabidopsis mutant defectivein jasmonate response is allelic to the auxin-signaling mutant axr1.Plant Physiol. 130, 887–894

34 Gray, W.M. et al. (2003) Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell 15, 1310–1319

35 Tor, M. et al. (2002) Arabidopsis SGT1b is required for defensesignaling conferred by several downy mildew resistance genes. PlantCell 14, 993–1003

36 Cuzick, A. et al. (2009) Lack of the plant signalling component SGT1benhances disease resistance to Fusarium culmorum in Arabidopsisbuds and flowers. New Phytol. 181, 901–912

37 Kazan, K. and Manners, J.M. (2008) Jasmonate signaling: toward anintegrated view. Plant Physiol. 146, 1459–1468

38 Koornneef, A. and Pieterse, C.M. (2008) Cross talk in defense signaling.Plant Physiol. 146, 839–844

39 Mockaitis, K. and Estelle, M. (2008) Auxin receptors and plantdevelopment: a new signaling paradigm. Annu. Rev. Cell Dev. Biol.24, 55–80

40 Thomma, B.P. et al. (1998) Separate jasmonate-dependent andsalicylate-dependent defense-response pathways in Arabidopsis areessential for resistance to distinct microbial pathogens. Proc. Natl.Acad. Sci. U. S. A. 95, 15107–15111

41 Staswick, P.E. et al. (2002) Jasmonate response locus JAR1 and severalrelated Arabidopsis genes encode enzymes of the firefly luciferasesuperfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14, 1405–1415

42 Lorenzo, O. and Solano, R. (2005) Molecular players regulating thejasmonate signaling network. Curr. Opin. Plant Biol. 8, 532–540

43 Nagpal, P. et al. (2005) Auxin response factors ARF6 and ARF8promote jasmonic acid production and flower maturation.Development 132, 4107–4118

44 Khan, S. and Stone, J.M. (2007) Arabidopsis thaliana GH3.9 in auxinand jasmonate cross talk. Plant Signal. Behav. 2, 483–485

45 Dombrecht, B. et al. (2007) MYC2 differentially modulates diversejasmonate-dependent functions in Arabidopsis. Plant Cell 19, 2225–

224546 Quint, M. et al. (2005) Characterization of a novel temperature-

sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases.Plant J. 43, 371–383

47 Ren, C. et al. (2005) Point mutations in Arabidopsis Cullin1 reveal itsessential role in jasmonate response. Plant J. 42, 514–524

48 Bari, R. and Jones, J.D.G. (2009) Role of plant hormones in plantdefense responses. Plant Mol. Biol. 69, 473–488

49 Padmanabhan, M.S. et al. (2008) TMV-Aux/IAA interactions:reprogramming the auxin response pathway to enhance virusinfection. J. Virol. 82, 2477–2485

50 Padmanabhan, M.S. et al. (2005) Interaction of the tobacco mosaicvirus replicase protein with the Aux/IAA protein PAP1/IAA26 isassociated with disease development. J. Virol. 79, 2549–2558

51 Padmanabhan, M.S. et al. (2006) The tobacco mosaic virus replicaseprotein disrupts the localization and function of interacting Aux/IAAproteins. Mol. Plant Microbe Interact. 19, 864–873

52 Lee, I.M. et al. (2000) Phytoplasma: phytopathogenic mollicutes. Annu.Rev. Microbiol. 54, 221–255

53 Hoshi, A. et al. (2009) A unique virulence factor for proliferation anddwarfism in plants identified from a phytopathogenic bacterium. Proc.Natl. Acad. Sci. U. S. A. 106, 6416–6421

54 Davis, D. and Dimond, A.E. (1953) Inducing disease resistance withplant growth-regulators. Phytopathology 43, 137–140

55 Thomma, B.P. et al. (2001) The complexity of disease signaling inArabidopsis. Curr. Opin. Immunol. 13, 63–68

56 Dai, Y. et al. (2006) Increased expression of MAP KINASE KINASE7causes deficiency in polar auxin transport and leads to plantarchitectural abnormality in Arabidopsis. Plant Cell 18, 308–320

57 Zhang, X. et al. (2007) Overexpression of Arabidopsis MAP kinasekinase 7 leads to activation of plant basal and systemic acquiredresistance. Plant J. 52, 1066–1079

58 Bennett, M.J. et al. (1996) Arabidopsis AUX1 gene: a permease-likeregulator of root gravitropism. Science 273, 948–950

59 Korolev, N. et al. (2008) The role of phytohormones in basal resistanceand Trichoderma-induced systemic resistance to Botrytis cinerea inArabidopsis thaliana. BioControl 53, 667–683

60 Gil, P. et al. (2001) BIG: a calossin-like protein required for polar auxintransport in Arabidopsis. Genes Dev. 15, 1985–1997

61 Grunewald, W. et al. (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog. 5,e1000266

62 Woodward, A.W. and Bartel, B. (2005) Auxin: regulation, action, andinteraction. Ann. Bot. (Lond.) 95, 707–735

63 Chandler, J.W. (2009) Local auxin production: a small contribution to abig field. Bioessays 31, 60–70

64 Domingo, C. et al. (2009) Constitutive expression of OsGH3.1 reducesauxin content and enhances defense response and resistance to afungal pathogen in rice. Mol. Plant Microbe Interact. 22, 201–210

65 van Esse, H.P. et al. (2009) Tomato transcriptional responses to a foliarand a vascular fungal pathogen are distinct. Mol. Plant MicrobeInteract. 22, 245–258

66 Vandenbussche, F. andVanDerStraeten, D. (2004) Shaping the shoot: acircuitry that integrates multiple signals. Trends Plant Sci. 9, 499–506

67 Acharya, B.R. and Assmann, S.M. (2009) Hormone interactions instomatal function. Plant Mol. Biol. 69, 451–462

381


68 Agrios, G.N. (2005) Plant Pathology. (5th edn), Elsevier AcademicPress

69 Melotto, M. et al. (2006) Plant stomata function in innate immunityagainst bacterial invasion. Cell 126, 969–980

70 Paponov, I.A. et al. (2008) Comprehensive transcriptome analysis ofauxin responses in Arabidopsis. Mol. Plant 1, 321–337

71 Hernandez-Blanco, C. et al. (2007) Impairment of cellulose synthasesrequired for Arabidopsis secondary cell wall formation enhancesdisease resistance. Plant Cell 19, 890–903

72 Dhonukshe, P. et al. (2008) Auxin transport inhibitors impair vesiclemotility and actin cytoskeleton dynamics in diverse eukaryotes. Proc.Natl. Acad. Sci. U. S. A. 105, 4489–4494

73 Hardham, A.R. et al. (2007) Cytoskeleton and cell wall function inpenetration resistance. Curr. Opin. Plant Biol. 10, 342–348

74 Vandenbussche, F. et al. (2003) The Arabidopsis mutant alh1illustrates a cross talk between ethylene and auxin. Plant Physiol.131, 1228–1238

75 Devos, S. et al. (2006) A hormone and proteome approach to picturingthe initial metabolic events during Plasmodiophora brassicae infectionon Arabidopsis. Mol. Plant Microbe Interact. 19, 1431–1443

76 Lincoln, C. et al. (1992) Hormone-resistant mutants of Arabidopsishave an attenuated response to Agrobacterium strains. Plant Physiol.98, 979–983

77 Leyser, H.M. et al. (1993) Arabidopsis auxin-resistance gene AXR1encodes a protein related to ubiquitin-activating enzyme E1. Nature364, 161–164

78 Nagpal, P. et al. (2000)AXR2 encodes amember of the Aux/IAA proteinfamily. Plant Physiol. 123, 563–574

79 Gray, W.M. et al. (2001) Auxin regulates SCFTIR1-dependentdegradation of AUX/IAA proteins. Nature 414, 271–276

80 Leyser, H.M. et al. (1996) Mutations in the AXR3 gene of Arabidopsisresult in altered auxin response including ectopic expression from theSAUR-AC1 promoter. Plant J. 10, 403–413

81 Alix, K. et al. (2007) Exploiting natural genetic diversity and mutantresources of Arabidopsis thaliana to study the A. thaliana–

Plasmodiophora brassicae interaction. Plant Breed. 126, 218–221

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Plant Growth Regulation Society o2–6 Augus

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82 Hobbie, L. et al. (2000) The axr6mutants ofArabidopsis thaliana definea gene involved in auxin response and early development.Development127, 23–32

83 Zhang, Z. et al. (2007) Dual regulation role of GH3.5 in salicylic acid andauxin signaling during Arabidopsis–Pseudomonas syringaeinteraction. Plant Physiol. 145, 450–464

84 Lee, D.S. et al. (2009) Arabidopsis GDSL lipase 2 plays a role inpathogen defense via negative regulation of auxin signaling.Biochem. Biophys. Res. Commun. 379, 1038–1042

85 Neuhaus, K. et al. (2000)Arabidopsis plants transformed with nitrilase1 or 2 in antisense direction are delayed in clubroot development. J.Plant Physiol. 156, 756–761

86 Zhang, J. et al. (2007) Constitutive expression of pathogen-inducibleOsWRKY31 enhances disease resistance and affects root growth andauxin response in transgenic rice plants. Cell Res. 18, 508–521

87 Ruegger, M. et al. (1998) The TIR1 protein of Arabidopsis functions inauxin response and is related to human SKP2 and yeast grr1p. GenesDev. 12, 198–207

88 Ludwig-Muller, J. et al. (1999) Indole glucosinolate and auxinbiosynthesis in Arabidopsis thaliana (L.) Heynh. glucosinolatemutants and the development of clubroot disease. Planta 208, 409–

41989 Bennett, R.N. et al. (2000) The tu8 mutation of Arabidopsis thaliana

encoding a heterochromatin protein 1 homolog causes defects in theinduction of secondary metabolite biosynthesis. Plant Biol. 7, 348–357

90 Strader, L.C. and Bartel, B. (2008) A new path to auxin. Nat. Chem.Biol. 4, 337–339

91 Delker, C. et al. (2008) Auxin dynamics: the dazzling complexity of asmall molecule’s message. Planta 227, 929–941

92 Sugawara, S. et al. (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis. Proc. Natl. Acad. Sci.U. S. A. 106, 5430–5435

93 Vieten, A. et al. (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 12, 160–168

94 Paciorek, T. and Friml, J. (2006) Auxin signaling. J. Cell Sci. 119, 1199–

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Linking development to defense: auxin in plant–pathogen interactions