MOLECULAR PLANT PATHOLOGY

(2003)

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(5 ) , 421–425 DOI : 10 .1046/ J .1364-3703.2003.00179.X

© 2003 BLACKWELL PUBL ISH ING LTD

421

Blackwell Publishing Ltd.

MicroReview

The role of lipopolysaccharides in induction of plant defence responses

G I TTE ERBS AND MAR I -ANNE NEWMAN*

Plant Pathology, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark

SUMMARY

Lipopolysaccharides (LPS) are ubiquitous, indispensable compon-ents of the cell surface of Gram-negative bacteria that appar-ently have diverse roles in bacterial pathogenesis of plants. As anouter membrane component, LPS may contribute to the exclusionof plant-derived antimicrobial compounds promoting the abilityof a bacterial plant pathogen to infect plants. In contrast, LPS canbe recognized by plants to directly trigger some plant defence-related responses. LPS also sensitize plant tissue to respond morerapidly or to a greater extent to subsequently inoculated phy-topathogenic bacteria. Sensitization is manifested by an accel-erated synthesis of antimicrobial hydroxycinnamoyl-tyramineconjugates, in the expression patterns of genes coding for somepathogenesis-related (PR) proteins, and prevention of the hyper-sensitive reaction caused by avirulent bacteria. The description atthe molecular level of the various effects of LPS on plants is a nec-essary step towards an understanding of the signal transductionmechanisms through which LPS triggers these responses. A defi-nition of these signal transduction pathways should allow anassessment of the contribution that LPS signalling makes to plant

disease resistance in both natural infections and biocontrol.

INTRODUCTION

Lipopolysaccharides (LPS) are cell surface components of Gram-negative bacteria that are associated with the outer membraneof the cell envelope. LPS is a tri-partite molecule consisting of alipid, a core oligosaccharide and an O-polysaccharide part. Thelipid, called lipid A, is embedded in the outer part of the phos-pholipid bilayer. The lipid A part is linked to a core oligosaccharideusually by the sugar 3-deoxy-

D

-manno-2-octulosonate (KDO). Thecore oligosaccharide consists of a short series of sugars and endsin the O-antigen, which is composed of repeating oligosaccharide

units. Unlike the lipid A-core part, variation is commonly seen inthe structure of the O-antigen part of the molecule and is for thatreason often used in serotype classification of Gram-negativebacteria (Lüderitz

et al

., 1971).LPS may play a number of important roles in the interactions

of bacterial pathogens with eukaryotic hosts. LPS are thought tocontribute to the restrictive membrane permeability properties ofthe outer membrane, allowing bacterial growth and survival inharsh environments. In the context of bacterial pathogenesis ofplants, LPS may serve to exclude pre-formed or induced antimi-crobial substances of plant origin. This role is consistent with theincreased antibiotic sensitivity of bacterial mutants with defectsin LPS synthesis and the growth and survival kinetics of thesemutants

in planta

(Dow

et al

., 1995; Kingsley

et al

., 1993). As acell surface component however, LPS are also available for inter-actions with eukaryotic host cells. This can occur either by directcontact or as a consequence of the release of micelles or blebscontaining LPS from the bacterial cell surface (Beveridge, 1999).

There is a considerable body of information on the effects ofLPS on mammalian and insect cells. In contrast, the effects of LPSon plant cells have been far less studied. It has been known forsome time that LPS treatment can affect the triggering of thehypersensitive response in plants by avirulent bacteria. Morerecently, LPS has been shown to induce some plant defenceresponses and to potentiate the induction of others. Nothing isknown of the mechanism by which LPS is perceived by plants andhow it activates these different plant responses. Recent evidencesupports the idea that plants may have evolved systems of innateimmunity which are perhaps analogous to the Toll-like receptorsystem for lipid A in animals (reviewed by Medzhitov andJaneway, 2000; Nürnberger and Brunner, 2002; Nürnberger andScheel, 2001). The definition of the components of the signaltransduction pathways that link the perception of LPS to the trig-gering or modulation of plant defence responses is a major aimof research in this area. Analysis of plants with mutations in sig-nalling components should allow an assessment of the contribu-tion of LPS signalling to plant disease resistance. A necessary stepin this process is to define the effects of isolated LPS on plants at

*

Correspondence

: Tel.: +45 35283303; Fax: +45 35283310; E-mail: mari@kvl.dk

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the phenotypic and molecular levels in order to develop screensfor plants with altered responses. In this review we will summar-ize the current state of knowledge of the effects of LPS in trig-gering plant defence.

Pre-treatment with LPS prevents the hypersensitive response in plants

The most studied effect of LPS or LPS–protein complexes on plantcells is its ability to prevent the hypersensitive response (HR)induced in plants by avirulent bacteria (reviewed by Sequeira,1983). The discovery of this effect of LPS on plants arose fromobservations that the infiltration of heat-killed

Ralstoniasolanacearum

bacteria into leaves of tobacco (

Nicotiana taba-cum

) delayed or prevented the appearance of disease symptomsor the HR when the leaves were subsequently inoculated withlive bacteria in compatible or incompatible interactions. LPSappeared to bind to the host plant mesophyll cell wall and withthat restrict the multiplication of a potential pathogen (Graham

et al

., 1977; Sequeira and Graham, 1977). This mechanism isreferred to as Localized Induced Resistance or Response (LIR)(reviewed by Dow

et al

., 2000). LIR requires several hours tobecome established, suggesting that the protective mechanismdepends on a plant response to LPS. The activity responsible forthe prevention of HR was subsequently shown to reside in the LPSof

Ralstonia solanacearum

, specifically in the lipid A-core struc-ture (Graham

et al

., 1977). The effects of LPS have since beenstudied in several plant /pathogen systems. Pre-treatment of pep-per cultivar ECW10R (

Capsicum annuum

) carrying the resistancegene

Bs1

with LPS from several phytopathogenic xanthomonadsas well as from enteric bacteria caused a suppression of the HRin the leaves induced by

Xanthomonas axonopodis

pv

. vesicato-ria

(

Xav

), carrying the cognate avirulence gene

avrBs1

. HR sup-pression was also seen in non-host reactions with

Xanthomonascampestris

pv.

campestris

(

Xcc

), a pathogen of

Brassica

. Theseresults indicate both that the origin of LPS is irrelevant for HR sup-pression, and that LPS pre-treatment leads to an HR suppressionin both host and non-host incompatible reactions (Newman

et al

., 1997, 2002). This response is not only restricted to tobaccoand pepper but can also be observed in non-solanaceous plantssuch as turnip (

Brassica campestris

) and

Arabidopsis thaliana

(M.-A. Newman, unpublished data). As far as we are aware,effects in monocots have not been reported. Interestingly, usingLPS from defined mutants of

Salmonella minnesota

(

Sm

) andpurified LPS from

Xcc

Newman

et al

. (1997), found that the lipidA attached to a truncated core oligosaccharide (at a concentra-tion of 50

µ

g/mL) from the enteric bacteria was the minimalstructure of LPS required for prevention of HR in the pepper–

Xcc

interaction. These findings are consistent with the earlierobservations of Graham

et al

. (1977). The ability of lipid A-core oligosaccharides from different bacteria to trigger HR

suppression may reflect the conserved nature of lipid A structuresbetween bacteria, and could provide an explanation for the abil-ity of LPS from many different bacteria to induce LIR. In contrast,the core oligosaccharide from

Xcc

was also fully active in induc-ing LIR at concentrations as low as 5

µ

g /mL. These results sug-gest that pepper cells may recognize more than one structurewithin the

Xcc

LPS to trigger LIR, this structure within the core oli-gosaccharide is yet to be defined. In these experiments lipid Aalone, which is responsible for most of the biological effects ofLPS in animal cells, was not effective in inducing LIR. However, itcannot be ruled out that attachment to an oligosaccharide isrequired to allow the insoluble lipid A to cross the plant cell wall.

Effects of LPS pre-treatment on bacterial growth in plants

The onset of the HR response is generally associated with a declinein the number of viable bacteria that can be recovered from thetissue. Pre-treatment of pepper leaves with purified LPS from

Xcc

,

E. coli

or

Sm

could prevent the HR associated with both gene-for-gene determined and non-host resistance to

Xav/avrBs1

and

Xcc

,respectively. LPS pre-treatment and following HR suppression causedalterations in the bacterial growth kinetics in these incompatibleinteractions. In both cases the numbers of viable bacteria decreasedin the first 24 h after inoculation into LPS pre-treated plants.Subsequently the numbers of viable bacteria were maintainedthroughout the course of the experiment, although no net increasein bacterial numbers was observed (Newman

et al

., 2002). Simi-larly, pre-treatment of tobacco with protein–lipopolysaccharidecomplexes from

Pseudomonas syringae

pv.

aptata

leaves pre-vented the HR subsequently induced by the incompatible bacteria

Erwinia amylovora

, and did not eliminate the avirulent bacteria(Minardi, 1995). Minardi further showed that the expression of

hrp

genes (a set of genes required for both the hypersensitivereaction and pathogenicity and essential for delivery of aviru-lence products) in the challenging bacteria was reduced in plantspre-inoculated with LPS–protein complexes, leaving these bacte-ria unable to trigger the HR response and the following necrosis.The effects of LPS treatment on the growth of bacteria in compati-ble plant–bacterial interactions are less pronounced. Pre-treatmentof pepper leaves with purified LPS causes some restriction inthe growth of the virulent

Xav

when inoculated at 10

7

cfu/mL,whereas using a lower start inoculum (10

4

cfu/mL), bacterialnumbers were approximately 100-fold lower than in non-treatedtissue 72 h after inoculation (Newman

et al

., 2000, 2002).

Defence-related responses induced by LPS in plants

There have been a few reports of the ability of LPS from plantpathogenic bacteria to directly induce or activate defence-relatedresponses in plants (reviewed by Dow

et al

., 2000). More recently

LPS and plant defence responses

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Coventry and Dubery (2001) investigated the effect of LPS ontobacco and found that when tobacco cuttings were inoculatedwith

Burkholderia cepacia

or purified

Burkholderia cepacia

LPS ata concentration of 50

µ

g/mL, an accumulation of various patho-genesis related (PR) proteins were observed in the leaves after4 days. They have further shown that at concentrations of200

µ

g/mL, purified

B. cepacia

LPS increased the membranepermeability of tobacco cells, and an even higher concentration(up to 1000

µ

g/mL) of purified

B. cepacia

LPS resulted in loss ofcell viability. The enhanced membrane permeability could leadto a

trans

-membrane flux of Ca

2+

ions across the plasmalemmaand it could trigger a cascade of defence responses. Meyer

et al

.(2001) examined the effect of

Xcc

LPS on plant defence in cell cul-tures of the non-host plant tobacco. They measured the amountof H

2

O

2

produced when cell cultures of tobacco were treated with

Xcc

LPS, and found an increase in H

2

O

2

production shortly afterthe addition of

Xcc

LPS, indicating an oxidative burst. Takentogether this may indicate a role for LPS as a signal for the induc-tion of plant defence responses.

Additionally, LPS has been implicated in the induction of sys-temic resistance (Dow

et al

., 2000; Leeman

et al

., 1995; Van Loon

et al

., 1998). Reitz

et al

. (2000) showed that the LPS from thebacteria

Rhizobium etli

strain G12 acts as the inducing factorof systemic resistance in potato (

Solanum tuberosum

) cultivarHansa to infection by the cyst nematode

Globodera pallida

. Whenpotato roots were pre-treated with LPS from

R. etli

G12 solution,a reduction was observed in the extent of

G. pallida

infection.

LPS pre-treatment potentiates the induction of defence-related responses in plant tissue

In addition to direct effects on plant tissue, treatment with LPScan affect the pattern of accumulation of gene expression andaccumulation of some phenolics in plants in response to subse-quent inoculation with virulent or avirulent bacteria. Newman

et al

. (2002) examined the effects of LPS pre-treatment on theaccumulation of salicylic acid (SA) and the synthesis of the phe-nolic conjugates coumaroyl tyramine (CT) and feruloyl tyramine(FT). SA acts as a signal molecule for the induction of a numberof plant defence-related genes in many plants (Klessig

et al

.,2000). CT and FT are suggested to have two possible roles inplant defence, as direct antimicrobial agents and in cell-wall rein-forcement (Keller

et al

., 1996; Newman

et al

., 2001).The HR response in pepper is associated with increased levels

of SA (Newman

et al

., 2001). In LPS-pretreated tissue, SA wasinduced in response to bacterial challenge with similar kinetics tountreated plants, but the levels of SA were fivefold less than inplants without prior treatment. LPS treatment alone did notinduce SA accumulation. In compatible interactions with

Xav

, noSA accumulation was detected. This result was not altered by LPSpre-treatment of the leaves.

Although LPS had apparently little effect on the timing of accu-mulation of SA, the timing of accumulation of FT and CT was con-siderably altered. The accumulation of soluble CT and FT wasassociated with incompatible interactions of pepper with

Xcc

and

Xav/avrBs1

. LPS pre-treatment caused these two compounds toaccumulate much more rapidly, at 2–4 h after inoculation com-pared with 12–24 h in untreated tissue. Importantly LPS alonedid not induce CT and FT synthesis over a 40 h time course. In thecompatible interaction between pepper and

Xav

, FT and CT wereinduced to a very low level. In LPS pre-treated plants, these com-pounds were induced more rapidly and to a higher level than inthe untreated plants. The observed level of response was lowerthan in either of the incompatible plant /bacteria interactionsstudied, however.

The synthesis of CT and FT is a result of a condensation cata-lysed by the enzyme tyramine hydroxycinnamoyl transferase(THT) of tyramine, derived from tyrosine controlled by the enzymetyrosine decarboxylase (TyDC), and coumaroyl- or feruloyl-CoAderived from the phenylpropanoid pathway. The first step ofthe phenylpropanoid pathway is catalysed by the enzyme pheny-lalanine ammonia lyase (PAL). TyDC enzyme activity and tran-scription of the

THT

and

PAL

genes are induced in pepper inresponse to

Xcc

inoculation (Newman

et al

., 2001). Both

Xcc

and

Sm

LPS induced an accumulation of the THT transcript togetherwith a major increase in TyDC enzyme activity, while no PAL tran-script was induced by LPS alone. The LPS treatment appears tohave ‘sensitised’ the pepper tissue to respond more rapidlyand to a greater extent to a subsequently inoculated phytopatho-genic bacteria. In addition, LPS pre-treatment potentiated theexpression of genes encoding PR proteins, in particular acidic

β

-1,3-glucanase, following bacterial inoculation (Newman

et al

.,2002).

It is becoming increasingly clear that a number of biotic andabiotic agents that induce plant disease resistance act to poten-tiate the induction of plant defence responses rather than todirectly induce them (reviewed by Conrath

et al

., 2001). Exam-ples include induced systemic resistance (ISR) induced by rhizo-sphere bacteria (Pieterse

et al

., 1998) and the induction ofresistance by

β

-aminobutyric acid (BABA) (Zimmerli

et al

., 2000).In contrast, systemic acquired resistance (SAR) is associated withthe expression (in the absence of any challenging pathogen)of SAR genes which can include PR1, acidic and basic

β

-1,3-glucanases (reviewed by Ryals

et al

., 1996; Schneider

et al

., 1996).Induction of SAR by biotic agents usually involves a necrotic reac-tion in the inoculated leaf. The LPS-induced localized resistance ofplant tissue resembles ISR and BABA-induced systemic resist-ance, and differs from SAR in that the establishment of the sen-sitized state does not require necrosis and in the involvement ofSA. SA has been implicated as a signal molecule in SAR, butapparently has no role in potentiation by BABA and in ISR, and isnot induced by LPS treatment.

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Could LPS modulation of defence responses play a role inresistance to natural infections? LPS may be continuously avail-able to plant cells in a freely diffusible form in natural infections.The release of LPS in soluble form, perhaps complexed with pro-tein, occurs in cultures of the plant pathogens

Erwinia amylovora

(Mazzuchi and Pupillo, 1976) and

Pseudomonas syringae

pv.

mors-prunorum

(Hodson

et al

., 1995), and may occur

in planta

,as has been suggested by work on

Rhizobium

spp. by Dazzo

et al

.(1991) and on

X. campestris

by Robinson (1987). It is thereforeconceivable that LPS released from these bacteria acts in a similarfashion to the model system described by Newman and colleagues.The sensitization of plant tissue by LPS from a few bacteria mayprevent a bacterial colonization in compatible interactions andallow the expression of resistance in the absence of HR in incom-patible interactions. Recognition of bacterial LPS by plant cellsmay also have a role in the restriction of growth of saprophytesin wounded plant tissue and for the control of bacterial diseasesof plants by general nonspecific mechanisms, i.e. mechanismsnot requiring the recognition of particular avirulence determinantsin the pathogen. The bacterial determinants of these generalmechanisms of plant resistance remain poorly defined (Dow

et al

.,2000).

CONCLUDING REMARKS

By analogy with other defence responses, the perception of LPSby a receptor is likely to generate a signal that is transduced bya series of proteins leading to the final biochemical response.Identification of these signal transduction pathways and of theassociated responses in

Arabidopsis

is a major aim of our ownwork. Experiments are in progress to determine whether knownsignal transduction components are involved in LIR in

Arabidop-sis

and to comprehensively survey alterations in plant geneexpression which occur in response to application of LPS usingthe

Arabidopsis

microarray chip. That information should allowthe development of a plant screen to identify components of theLPS signalling and response system through mutational analysis.A receptor for a conserved domain of bacterial flagellin has beenidentified in

Arabidopsis

(Felix

et al

., 1999; Gomez-Gomez

et al.

,2001; Gomez-Gomez and Boller, 2000), using a similar approachthis may provide a model for the experimental approach to betaken. An understanding of the effects that LPS has on plants hasimplications for both the control of bacterial diseases through generalnonspecific mechanisms and also in the biocontrol of bacterialand fungal diseases by beneficial bacteria, which in some casesis believed to occur as a consequence of the recognition of LPS.

ACKNOWLEDGEMENTS

We thank Dr Max Dow (Department of Microbiology, UniversityCollege Cork, Ireland) for helpful discussions and critical comments

on the manuscript. Our work at RVAU is supported by a grantfrom the Danish Agricultural and Veterinary Research Council.We also acknowledge financial support from Carlsbergfondet,Copenhagen, Denmark.

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