Annual Review of Phytopathology Volume 51 Issue 1 2013 [Doi 10.1146%2Fannurev-Phyto-082712-102239] Venturi, Vittorio; Fuqua, Clay -- Chemical Signaling Between Plants and Plant-Pathogenic

PY51CH02-Venturi ARI 1 July 2013 18:30

Chemical Signaling BetweenPlants and Plant-PathogenicBacteriaVittorio Venturi1,∗ and Clay Fuqua2

1International Center for Genetic Engineering and Biotechnology, 34149 Trieste, Italy;email: [email protected] of Biology, Indiana University, Bloomington, Indiana 47405-1847;email: [email protected]

Annu. Rev. Phytopathol. 2013. 51:17–37

The Annual Review of Phytopathology is online atphyto.annualreviews.org

This article’s doi:10.1146/annurev-phyto-082712-102239

Copyright c© 2013 by Annual Reviews.All rights reserved

∗Corresponding author

Keywords

plant-bacteria interactions, interkingdom signaling, plant phenoliccompounds, quorum sensing, agrobacterium plant signaling,acylhomoserine lactones, diketopiperazines

Abstract

Studies of chemical signaling between plants and bacteria in the pasthave been largely confined to two models: the rhizobial-legume symbi-otic association and pathogenesis between agrobacteria and their hostplants. Recent studies are beginning to provide evidence that manyplant-associated bacteria undergo chemical signaling with the plant hostvia low-molecular-weight compounds. Plant-produced compounds in-teract with bacterial regulatory proteins that then affect gene expression.Similarly, bacterial quorum-sensing signals result in a range of func-tional responses in plants. This review attempts to highlight currentknowledge in chemical signaling that takes place between pathogenicbacteria and plants. This chemical communication between plant andbacteria, also referred to as interkingdom signaling, will likely becomea major research field in the future, as it allows the design of specificstrategies to create plants that are resistant to plant pathogens.

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INTRODUCTION

It is estimated that land plants evolved morethan 700 mya and that their emergence wasassisted by fungal associations, indicating thatthey coevolved with microorganisms (47). Inaddition, it is believed that molecular inter-actions with epiphytic, beneficial rhizospheric,symbiotic, and pathogenic bacteria also playedand continue to play an important role in theirevolution. During the course of these inter-actions, plants constantly monitor changes inspecific bacterial activities, whereas bacteria re-spond to variations in plant physiology, withboth organisms continuously making adjust-ments. This close association for millions ofyears has therefore allowed bacteria and plantsto develop mechanisms of production and re-sponse for many signaling molecules releasedby the host plant and its bacterial community.

Plants release large amounts of chemicalcompounds (especially through their roots)at a significant cost; in some cases, thesecombat pathogenic microorganisms and attractbeneficial ones (4). Studies involving severalplant-pathogenic bacterial species have alsoshown that they have evolved systems to senseand respond to low-molecular-weight plantcompounds in order to regulate virulence-associated traits (8). In fact, bacteria-to-plantchemical signaling is increasingly recognizedas an important aspect of both beneficial andpathogenic interactions, although the details ofthis communication are currently poorly un-derstood. Chemical communication betweenplant and bacteria (also called interkingdomsignaling) is an emerging research area thatis likely to continue expanding and representsa major challenge for the future, with theunderlying reason for this being the largenumber of different associations taking placebetween plants and bacteria. Understandingthis signaling is pivotal to devising new waysto improve disease resistance.

Plant compounds potentially involved inchemical signaling with bacteria are thoughtto include sugars, amino acids, and phenolics;however, current knowledge of secondary plant

metabolites that can serve as chemical signalsand trigger a bacterial response is very limited.In addition, many plant compounds are likelyto be produced in trace amounts that are belowthe current level of detection. Recent researchhas provided evidence that bacteria produceseveral compounds that are involved in cell-cellcommunication within a bacterial population.This process is known as quorum sensing (QS)and is critical for the infection and invasionprocesses of many phytopathogens (119). Arethese chemical signals perceived by plants ordo plants produce mimic signals that interferewith this important bacterial communicationsystem? Researchers are asking these questions,and results are beginning to reveal that bacterialQS signals can behave as interkingdom chemi-cal signals and furthermore that plants producecompounds that interfere with bacterial QS.

This review focuses on interkingdomchemical signaling that takes place betweenpathogenic bacteria and plants and more specif-ically on the role of (a) low-molecular-weightplant compounds in influencing gene expres-sion via bacterial signal transduction pathwaysand of (b) bacterial signaling molecules in in-fluencing plant responses and gene expression.We do not attempt to comprehensively reviewlocal or contact-dependent responses by theplant during pathogen attack (16) or the in-duction of bacterial gene expression in responseto physical contact with plant tissues or in re-sponse to the local nutritional and physical envi-ronment (e.g., nitrogen source, carbon source,and pH temperature), as these have been exten-sively covered elsewhere (8).

Interkingdom signaling via chemical signalshas been extensively studied in the rhizobia-legume symbiosis and between agrobacterialpathogens and their host (8). Of these two sys-tems only the chemical signaling between plantsand pathogenic Agrobacterium is discussed be-low, as this review focuses on plant pathogens.In addition, recent studies have shown (a) therole of plant phenolic compounds in the regula-tion of gene expression of virulence-associatedgenes in pathogenic bacteria, (b) the role ofbacterial QS signals in regulating plant gene

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expression, and (c) the role of low-molecular-weight plant compounds in the interference ofbacterial QS.

A BACTERIAL SUBFAMILY OFLUXR PROTEINS THAT BINDAND RESPOND TO PLANTCHEMICAL SIGNALS

QS via N-acylhomoserine lactones (AHLs) isused by many proteobacteria to regulate the ex-pression of virulence-associated factors that or-chestrate their temporal and spatial productionin the plant (12, 20, 41, 81, 119). QS via AHLsis thus far the most common system found ingram-negative bacteria, specifically those in theproteobacteria group. A typical system is com-posed of a LuxI-family synthase responsiblefor synthesizing the AHL signal, which theninteracts at quorum concentrations with thecognate LuxR-family transcription factors andaffects gene expression (33). AHLs vary in theirstructure; they have different acyl chain lengths(from 4 to 18 carbons) and show variation in theoxidation state of the C3 position on this acylchain (which can be a methylene or a ketone,or can be hydroxylated). Extensive studies onAHL-QS have also revealed the presence ofproteins closely related to AHL-QS LuxRsthat specifically interact with and respond toplant signals. This unidirectional interkingdomsignaling circuit has evolved from canonicalAHL-QS systems in which the LuxR proteinno longer responds to endogenously producedAHLs but rather to plant signals.

Features of Quorum Sensing LuxRFamily Proteins

Members of the family of QS LuxR-typeproteins are transcriptional regulators thatrespond to AHLs; most commonly, they are ap-proximately 250 amino acids long and have twodomains separated by a short linker region. Theautoinducer-binding domain is located withinthe N-terminal region of the protein (99, 103),and a DNA-binding helix-turn-helix (HTH)domain is positioned within the C-terminal

region (17, 18). LuxR-type proteins bind toDNA at a conserved site called a lux box, whichoften consists of an inverted repeat recognitionsequence of a 18–20-bp palindrome that is usu-ally located at –42.5 from the transcriptionalstart site (25, 107). Many QS LuxR-type pro-teins are transcriptional activators, but somecan act as repressors (33). The position of theDNA-binding site dictates whether associationwith the protein blocks or stimulates transcrip-tion. Most LuxR-type proteins are inactivein the absence of the AHL. However, thereis a growing list of LuxR-type proteins thatfunction in the apo-form and are inactivated byAHL binding. For those LuxR-type proteinsthat are AHL-dependent activators, AHLbinding results in a conformational changethat allows the HTH domain to bind DNAupstream of the –35 site of its target promoters;the LuxR-AHL complex then recruits RNApolymerase to the promoter by interacting withthe carboxy-terminal domain (CTD) of its α-subunit (107), thereby activating transcription(136). However, binding of the LuxR-AHLcomplex within the target promoter can blocktranscription. For many of the LuxR-typerepressors, the apo AHL-free form bindswithin the target promoter, blocking accessto RNA polymerase, repressing transcription.When AHL binds to the LuxR-type protein,conformational changes cause it to release thepromoter and in turn relieve repression (76).Structural analysis of TraR of Agrobacteriumtumefaciens (118, 136) and SdiA of Escherichiacoli (129) have shown that the AHL-bindingcavity is composed of a β-sheet that comprisesfive antiparallel strands with three α-helixes oneach side. Binding of the AHL can be crucialfor LuxR protein stability and correct folding;when TraR is expressed in E. coli in the absenceof its cognate AHL (3-oxo-octanoyl-HSL),it is quickly proteolized or forms inclusionbodies (138). However, when 3-oxo-C8-HSLis present, TraR dimerizes and is folded andsoluble. Similar biochemical properties havebeen observed for SdiA and other LuxRproteins (80, 129), although binding of theacyl side chain can differ between LuxR-type

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proteins with different cognate AHL ligands(67). QS LuxR-family proteins show surpris-ingly low homologies (18% to 25%); however,95% of them share nine highly conservedamino acid residues (124, 136). Six of theseare hydrophobic or aromatic and form thecavity of the AHL-binding domain. Withrespect to TraR these are tryptophan 57 (W57),tyrosine 61 (Y61), asparagine 70 (D70), proline71 (P71), tryptophan 85 (W85), and glycine113 (G113). The remaining three highly con-served residues, glutamine 178 (E178), leucine182 (L182), and glycine 188 (G188), are in theHTH domain.

LuxR Solos and Bacterial Response toPlant Chemical Signals

Many of the genes for LuxR and LuxI regu-lators are located adjacent to each other, andin almost all systems studied these geneticallylinked regulators function together in QS.However, many proteobacteria also possessLuxR-type proteins that are unpaired to acognate LuxI synthase. In 2008, an analysis of265 proteobacterial genomes showed that 68had a canonical, paired LuxI/LuxR system, andof these, 45 contained more LuxRs than LuxIs.Another set of 45 genomes contained only QSLuxRs (11). These QS LuxR proteins that lacka genetically linked LuxI have been termedorphans (31) and, more recently, solos (109).QS LuxR solos also possess an AHL-bindingdomain in the N terminus and a DNA-bindingHTH in the C terminus; they have beenreported to expand the regulatory targetsof the canonical QS systems by respondingto endogenous or exogenous AHLs. Forthe latter, they can regulate target genes byeavesdropping on externally provided AHLsignals produced by neighboring bacteria (1) orvia interkingdom signaling when respondingto eukaryotic signals (28, 42, 108, 134). Twowell-studied solos are QscR from Pseudomonasaeruginosa, which responds to endogenouslyproduced AHLs (64), and SdiA from Salmonellaenterica and E. coli, which eavesdrops on AHLsproduced by neighboring bacteria (1, 50, 93).

A subgroup of LuxR solos has been discov-ered that is found in plant-associated bacteriathat bind to plant-produced compounds ratherthan to AHLs (43, 108, 109). These have differ-ences in one or two of the conserved residues inthe AHL-binding domain, more precisely, W57

and Y61 (positions with respect to TraR), whichare substituted by methionine (M) and trypto-phan (W), respectively. It is likely that the evo-lution of these changes corresponds with theability of these proteins to bind low-molecular-weight compounds produced by plants ratherthan AHLs (17, 28, 29, 134). Members ofthis subfamily include XccR of Xanthomonascampestris, OryR of Xanthomonas oryzae, PsoRof Pseudomonas fluorescens, XagR of Xanthomonasaxonopodis, and NesR in Sinorhizobium meliloti(87). Interestingly, the luxR solo genes are al-ways found adjacent to the virulence-associatedproline iminopeptidase ( pip) gene (15, 28, 134).In addition, the promoter region of pip almostalways contains a lux-box-like sequence. Al-though the exact biological function of thesespecific proline iminopeptidase homologs is notentirely clear, in general these enzymes cleavethe proline from the N terminus of proteins (95)and can also hydrolyze D-alanine but do so at alower level of efficiency (3).

OryR of the Rice PathogenXanthomonas oryzae

X. oryzae pv. oryzae (Xoo) is a γ-proteobacteriumthat is a vascular pathogen that causes leaf blightdisease on rice plants (Oryza sativa). Xoo doesnot produce AHLs (28) but possesses OryR,which is part of the subfamily of QS-relatedLuxR solo proteins that bind plant compounds.OryR was indirectly shown to bind to plantcompound(s) since it was found to be insolublewhen overexpressed in the presence of a widerange of AHLs, but it can be solubilized if riceplant macerate is provided to the growth media.In addition, OryR was shown to regulate thegenetically linked pip gene, which possesses alux-type box in its promoter region, in responseto plant signals (28). Interestingly, this pip acti-vation increases if macerate from Xoo-infected

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rice is provided to the media, indicating that theplant compound(s) is more abundant in infectedrice; plants are known to increase production ofmany compounds upon pathogen attack (29).Genome-wide gene expression studies haveshown that OryR is a global regulator, and itregulates the expression of 8% of the open read-ing frames (ORFs) in Xoo (42). Strikingly, ap-proximately 20% of the genes that are positivelyregulated are implicated in motility or chemo-taxis (42). OryR was shown to regulate expres-sion of the gene encoding the flagellar regulatorFlhF in response to plant signals via a lux-typebox element in its promoter region. The cur-rent working model is that OryR plays a rolein the early phases of infection, allowing Xoo tosense its arrival on/in the plant; detection of thesignal then results in hypermotility that enablesXoo to rapidly colonize the vascular system (42).

XccR of the Crucifer PathogenXanthomonas campestris

X. campestris pv. campestris (Xcc) is an importantpathogen infecting a wide variety of brassicasworldwide. Xcc also contains a gene coding for aLuxR solo protein called XccR, which is orthol-ogous to OryR of Xoo and also responds to anas yet unidentified plant compound (134). Justas in Xoo, pip encodes a proline iminopeptidasethat possesses a lux-type box 20-bp palindromicsequence in its promoter region and is adjacentto xccR. Both pip and xccR have been shown to beimportant for pathogenicity because null mu-tants show reduced virulence. Importantly, ithas been observed that activation of pip by XccRoccurs in planta, suggesting that a plant com-pound(s) is important for this regulation (134).Induction of pip transcription increases almosteightfold in planta and has been shown to re-quire the presence of the lux-type box.

XagR of the Soybean PathogenXanthomonas axonopodis

X. axonopodis pv. glycines (Xag) causes bacterialleaf pustule on soybean (Glycine max). Xag alsocontains a LuxR solo called XagR that is orthol-ogous to XccR and OryR and is linked to the

adjacent pip gene (15). Both xagR and pip havebeen shown to be important for virulence, andXagR activates pip transcription in planta. Tem-poral studies have indicated that pip transcrip-tion in planta gradually increases after infec-tion, reaching greatest activity after 72 hours,before slowly decreasing. This induction ofpip has been suggested to be due to a plantcompound(s) that accumulates in response topathogen infection–inducing/activating XagR.Transcriptome analysis revealed that XagRregulates 77 ORFs; one of these is yapH, whichis involved in adhesion. It has been postulatedthat XagR plays a role in Xag invasion by nega-tively regulating adhesion via yapH in responseto a plant compound(s) that accumulates uponinfection. The current working model showsthat when no plant signal molecule is detected,YapH is not repressed and bacterial cells are at-tached to the plant. As the infection progresses,XagR accumulates, activating pip transcriptionand biosurfactant-related genes and repressingyapH; this results in a decrease in adhesion,allowing the cells to spread within the apoplastand thereby increasing the bacterial load (15).

The LuxR-Solo Family Responding toPlant Signals is Common AmongPlant-Associated Bacteria

Proteins highly homologous to OryR/XccR/XagR are also present in the major gen-era of plant-associated bacteria, includingXanthomonas, Pseudomonas, Dickeya, Rhodospir-illum, Citreicella, Rhizobium, Sinorhizobium,and Agrobacterium (43). Interestingly, suchLuxR solos are only found in plant-associatedbacteria, reinforcing the model that they areinvolved in interkingdom signaling betweenplants and bacteria. In addition, all of the geneshave an adjacent pip gene, and the proteins havesimilar substitutions in their AHL-binding do-mains when compared with AHL-binding QSLuxR-family proteins. Two of these proteinshave been studied in plant-beneficial bacteria,namely PsoR of P. fluorescens and NesR of S.meliloti (86, 108). PsoR of P. fluorescens has beenshown to respond to rice and wheat (Triticumaestivum) but not to cucumber (Cucumis


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sativus), indicating some level of specificity.PsoR plays a role in biocontrol in rhizosphericP. fluorescens by controlling transcriptionalregulation in response to plant compound(s)of various antimicrobial-related genes (108).NesR of S. meliloti has not yet been studied forits ability to respond to plant compounds buthas been associated with survival under stressand utilization of various carbon sources (86).

BACTERIALN-ACYLHOMOSERINELACTONES AS PLANTCHEMICAL SIGNALS

The long-term close association of AHL-producing bacteria with plants provides anexplanation as to why AHLs have been foundto influence plant gene expression. AHLs havethus evolved into interkingdom signals. Inparallel, plants have also evolved the ability toinfluence bacterial AHL-QS systems by pro-ducing low-molecular-weight compounds thatinterfere by acting as agonists or antagonistsof canonical AHLs in bacteria. The role ofAHLs in plant gene expression, resistance, anddevelopment as well as plant interference, viaAHL mimic compounds, to bacterial AHL-QSis recently being intensively investigated andcurrent results and direction are discussed.

N-Acylhomoserine Lactones as Signalsfor Plant Gene Expression

Many phytopathogenic bacteria employAHL-QS in order to spatially and temporallyexpress virulence-associated factors in theplant (119). An outstanding question relatedto AHL bacterial signals that has been and iscurrently being investigated is whether plantscan also recognize and respond to AHLs. Thisphenomenon was first investigated in depthin 2003 by Mathesius et al. (74) through aglobal proteomic study of the model legumeMedicago truncatula in response to AHLs.M. truncatula is a close relative of alfalfathat forms a symbiotic relationship with thenitrogen-fixing symbiont S. meliloti. Axenicallygrown M. truncatula roots were exposed to low

AHL concentrations (10 nM–2000 nM), androot parts were then analyzed for their globalprotein content. Such a concentration windowreflects production of 3-oxo-C12-HSL (anAHL produced by several plant pathogens,including P. aeruginosa) and 3-oxo-C16:1-HSL(produced by S. meliloti ) in vitro. Exposure tothese AHLs significantly changed the levels of154 proteins variably at 48 h when comparedwith a 24-h exposure. The global proteomicresponse to AHLs represents approximately6% of the total identifiable proteins; of these,23% had functions possibly related to plantdefenses and stress response, 14% to proteindegradation or processing, 5% to flavonoidbiosynthesis, 5% to plant hormone responsesor synthesis, 10% to regulatory functions, 6%to cytoskeletal elements, and 37% to primarymetabolism.

A similar global response to AHL exposurehas also been observed using Arabidopsisthaliana (120). In this case, roots were exposedto 10 μM of C6-HSL, and gene expression viamicroarrays was then assayed in leaf and roottissue at different time points (4 h; 1 and 4 d).In total, the expression of 721 and 1,095 geneschanged in leaf and root tissue, respectively.Importantly, 6% of differentially regulatedgenes in leaf tissue and 3% in root tissue areinvolved in plant hormone response, especiallygenes implicated in auxin and cytokinin, whichplay critical roles in the control of plant growthand several developmental responses. In agree-ment, measurement of auxin and cytokininlevels after exposure to C6-HSL revealed thatconcentration of cytokinin declined, whereasthat of auxin increased compared with theuntreated control plants. Other differentiallytranscribed genes were grouped in severalfunctional categories, including energy andmetabolism (approximately 20%), transcrip-tion/translation (approximately 11%), andlipid/protein/nucleic acid–related (approxi-mately 8%), as well as category for the remain-ing genes for which no clear annotated functioncould yet be assigned. Surprisingly, exposureto C6-HSL did not result in the differentialexpression of typical/known defense-related

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genes. An earlier study reported that foliarexposure of A. thaliana to 3-oxo-C8-HSL didnot result in significant changes in gene ex-pression (130). It therefore appears that plantsdisplay specificity toward AHLs and responddifferently to structurally distinct AHLs.

N-Acylhomoserine Lactones andInduction of Plant Systemic Resistance

Many AHL-producing bacteria colonize therhizosphere of plant roots (26). Most of thesebacteria are beneficial [also known as plantgrowth–promoting rhizobacteria (PGPR)] tothe plant, resulting in plant growth promotionand/or protection from microbial pathogens(71). Mechanisms of disease suppression ofmicrobial pathogens by PGPR strains includeniche exclusion by competition for nutrients,production of antimicrobial compounds, andinduction of systemic resistance (ISR), inwhich the inducing PGPR and pathogen donot undergo any type of direct interaction.ISR is different from pathogen-induced andsalicylate-mediated systemic acquired re-sistance (SAR) (117, 133). ISR that followscolonization of PGPR strains leads to enhancedexpression of various signaling pathways, in-cluding jasmonate and ethylene. Using aPGPR Serratia liquefaciens strain that producesAHLs (C4- and C6-HSL), it was determinedthat when gnotobiotically grown tomato plantswere inoculated with the wild-type strain,the appearance of necrotic cell death andthe presence of fungal DNA after infectionwith the fungal leaf pathogen Alternariaalternata were reduced by more than 70% (98).However, inoculation with the AHL-negativemutant also reduced the development ofA. alternata–induced cell death, suggestingthat AHL signaling was in part responsible forthe observed ISR. Importantly, the coloniza-tion of the rhizosphere of tomato by both thewild-type and AHL-negative mutants was com-parable. Similar experiments were performedin tomato and the pathogen A. alternata using aPseudomonas putida PGPR strain that producesat least four different 3-oxo-HSLs with acyl

chains ranging in size from 6 to 12 carbons.Results showed that P. putida AHLs are alsoinvolved in systemic resistance but to a lesserextent (98). It was further established that phys-iological concentrations of C4- and C6-HSLs,which are produced by S. liquefaciens, resultedin elevated levels of salicylic acid and increasedexpression of several defense loci, includingsalicylic acid– and ethylene-dependent genes aswell as antioxidant-related loci. ISR by AHLswas also recently reported in A. thaliana andbarley (Hordeum vulgare) (97). Root exposureto 3-oxo-C14-HSL led to higher resistancetoward the fungal pathogen Bumeria gramininsin barley and in A. thaliana to the fungus Golovi-nomyces orontii and the bacterial pathogen Pseu-domonas syringae. Further studies on the possiblemechanism revealed that exposure to certainlong-chain-3-substituted AHLs prolongs theactivities of several mitogen-activated proteinkinases (MAPKs) and related cascades involvedin pathogen perception (97). AHLs thereforeneed to be further investigated and should beconsidered as potential candidates for elicitorsof plant defense as they induce expression oftypical defense-related proteins resulting inincreased resistance against pathogens.

N-Acylhomoserine Lactones AffectPlant Growth and Development

As described above, AHLs affect gene ex-pression, altering the levels of many proteins,including those involved in hormonal anddefense functions. Consequently, AHLs havealso been reported to affect plant growthand development. The growth responses ofA. thaliana to many different bacterial AHLssuggested that C10-HSL was particularlyactive in modifying root system architectureby affecting primary root growth, lateral rootformation, and root hair development. It wasfurther established that C10-HSL modulatesprimary root growth by influencing cell divisionin the meristem (84). A recent study comparedthe effects of exposure to several different AHLson the growth of roots and shoots in A. thaliana(96). Exposure of seedlings to 6-μM C6-HSL


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resulted in a significant increase in root andshoot biomass after 11 days. This effect on theshoot biomass decreased as AHLs with longeracyl side chains were utilized. Root biomasswas only significantly altered in response toC6-HSL. In contrast, root length decreasedin response to AHLs with longer acyl sidechains. These experiments also raise the issueof internalization and transport of AHLs intothe plant. Although transport of short-chainC4- and C6-HSL from the root to the shoot inbarley and A. thaliana has been demonstrated,this was not the case for either C10-HSL or3-oxo-C14-HSL (44, 97, 120). Understandingthe uptake and transport of AHLs needs tobe clarified and will be an important aspect ofthis interkingdom chemical signaling betweenplants and plant-associated bacteria.

Transgenic Plants ProducingN-Acylhomoserine Lactones andBacterial Pathogenesis

As many phytopathogenic bacteria employAHL-QS to temporally express virulence-associated factors in the plant followingsuccessful colonization, several studies haveexamined whether providing high exoge-nous concentrations of AHLs affect bacterialpathogenicity. Experiments have been per-formed with transgenic plants that produceAHLs by expressing a bacterial luxI-typegene and studying plant susceptibility af-ter challenge with a bacterial pathogen(s).AHL-producing plants interfere with the QS-regulated phenotypes of pathogenic bacteria,thereby affecting the course of the disease. Forexample, transgenic potato and tobacco plantswere engineered to harbor and express the yenIgene of Yersina enterocolitica, resulting in theproduction of C6-HSL and 3-oxo-C6-HSL(30, 72, 113); both of these AHLs are naturallyproduced by the pathogen Erwinia carotovora.This soft-rot pathogen uses AHL-QS toregulate the expression of a cocktail of plantcell wall–degrading enzymes (PCWDE) in-volved in virulence. Upon infection of potatostems with E. carotovora, differences in disease

development between the wild-type and trans-genic plant were observed, including diseaseseverity and time of onset: The transgenicplant displayed a level of disease significantlyhigher than the control. This difference inpathogenicity was, however, seen only whenthe inoculum was below a certain level: Noobservable differences were present when thebacterial inoculum exceeded 106 cells per in-oculation site (113). Several experiments haveconfirmed that more disease development isseen in transgenic potatoes than in the controlplants as the level of bacterial inoculum in theplants is reduced. These data have suggested animportant role for the correct timing of expres-sion of PCWDE via QS either via triggeringhost defenses or by another mechanism.

Interestingly, provision of exogenous AHLsin another plant-pathogen model resulted inthe transgenic plant that produced the AHLsthat were resistant to the bacterial pathogen atdifferent inoculum levels. These data were ob-tained using the tobacco pathogen P. syringaepv. tabaci (Pst), transgenic tobacco that also con-tained the yenI bacterial gene that directs pro-duction of 3-oxo-C6-HSL, and an AHL recog-nized by Pst (100). Several experiments showedthat providing exogenous AHLs in transgenictobacco conferred a decreased susceptibility toPst, particularly in the early stages of infec-tion when using a low inoculum concentra-tion (102 cfu leaf disc−1) (92). It has been pro-posed that AHL production by the transgenicplant could induce the expression of virulence-associated traits even at low population densi-ties, enabling the recognition of the pathogenby the plant, which consequently initiates a suc-cessful defense reaction. The scenario changeswhen large numbers of cells are inoculated intoplants, as they are present in sufficient numbersto better overcome plant defenses and switchon virulence gene expression.

Plant Interference of BacterialQuorum Sensing viaN-Acylhomoserine Lactone Mimics

Several studies have demonstrated that plantsare able to synthesize compounds that mimic

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AHL compounds and interfere with bacterialQS. This has been observed using plants andplant extracts (for example, from pea, Medicagotruncatula, and rice) that appear to stimulateor inhibit AHL-mediated gene expression asjudged using bacterial sensors that do not pro-duce AHLs (5, 23, 37, 54, 106, 112). Most ofthe experiments using extracts from plants stim-ulated rather than inhibited QS-gene expres-sion; however, none of these plant compoundshave yet been chemically identified. Many ofthese compounds have been detected in rootexudates, and their chemical properties suggestthat they are distinct from AHLs. Plant mim-ics acting as agonists of AHL-QS might lead topathogen confusion and decreased pathogenic-ity because they can stimulate premature ex-pression of virulence genes, as indicated by thework using transgenic plants expressing AHLs(see above). More progress with respect to AHLmimics has been achieved using algae, especiallyfor compounds that inhibit AHL-QS systems(40, 48, 60, 73, 94, 111). Some of these inhibit-ing compounds have been identified as halo-genated furanones produced by algae (48, 73)and lumichrome (a derivative of the vitamin ri-boflavin) produced by the alga Chlamydomonas.A compound inhibiting AHL-QS has also beenidentified from leguminous plants and has beenidentified as L-canavanine (an arginine analog)(56). All of these inhibiting compounds havebeen implicated in enhancing the proteolyticdegradation of QS LuxR receptors, thus affect-ing the QS response (60, 94). Research is con-tinuing to focus on identifying QS inhibitors,as it is believed these will have considerable ap-plications in medicine and agriculture for con-trolling bacterial populations (7).

CHEMICAL SIGNALINGBETWEEN AGROBACTERIUMSPECIES AND HOST PLANTS

A. tumefaciens and Agrobacterium rhizogenes areclosely related terrestrial bacteria within thefamily Rhizobiaceae of the α-proteobacterialgroup. The Agrobacterium genus is in factpolyphyletic with rhizobial genera (including

species of Sinorhizobium, Mesorhizobium, andRhizobium), which are symbionts of legumi-nous plants that supply organic nitrogen totheir hosts (131). However, A. tumefaciens andA. rhizogenes are pathogenic to plants, oftento those from a wide range of dicotyledonousspecies, and cause the diseases known as crowngall and hairy root. Crown gall is a site of un-controlled, tumorous tissue growth, typicallyat the plant crown (the subterranean-to-aerialtransition zone), whereas hairy root is a largeentangled mass of roots (2, 45). Developmentof both diseases on plants requires large viru-lence plasmids, the tumor-inducing (Ti) plas-mid for crown gall and the root-inducing (Ri)plasmid for hairy root (55, 110). These plas-mids encode many of the virulence functionsrequired for disease, and Agrobacterium deriva-tives cured of these plasmids (historically de-scribed as Agrobacterium radiobacter) are com-pletely avirulent.

The mechanism by which agrobacteriacause disease is remarkable and relies oncross-kingdom horizontal gene transfer. Thegenes required to drive this process are clus-tered on each plasmid and are known as vir(virulence) genes. These vir genes encode asmany as 30 proteins and are organized in upto 10 operons (137). During pathogenesis,a specific segment or multiple segments ofthe Ti or Ri plasmid are copied from theso-called T-region (transferred region) of theplasmid via a conjugation-type mechanism togenerate a single-stranded intermediate calledthe T-DNA. The T-DNA and associatedVir proteins are transferred through a typeIV secretion system from the bacteria intoplant cells at the site of infection (19) andare ushered into the plant nucleus, where theT-DNA is stably integrated into the plantchromosomal DNA (115). T-DNA-specifiedgene products drive hormonal imbalanceswithin the infected tissues, which causes thevisible manifestation of the diseases crown galland hairy root. Other T-DNA genes cause thesynthesis and release of unusual metabolitesthat are collectively known as opines, which areconsumed by agrobacteria in and around the


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infection site as sources of carbon, nitrogen,and, in some cases, phosphorus (24). Multi-ple opine types can be specified by a singleT-DNA, and virulent agrobacteria havehistorically been subclassified by the specificopines that they cause plants to produce uponinfection (131). Genes for opine catabolism arealso encoded on the virulence plasmids. Opineproduction from infected tissues provides aselective benefit to the bacteria harboring thecorresponding virulence plasmid, improvingtheir competitive advantage (91).

The complex processes that lead to agrobac-terial disease are tightly regulated, as is thecontrol circuitry that mediates the transition ofthe bacteria to colonizing the opine-producing,transformed plant tissue (8). The overall pro-cess may be viewed as a series of signalexchanges between the plant and the infectingagrobacteria. The initial stages of infection,culminating in T-DNA transfer, are activatedprimarily by phenolic compounds, consideredto be lignin precursors, released from woundedplant tissue, that can be augmented by certainsugars, low phosphorus levels, and acidicpH at the site of infection (104). Followingsuccessful transformation of the plant cells,release of opines is perceived by bacteria inor around the infected tissue, stimulatingcatabolism of the opine(s) and also inducing aQS process that ultimately results in increasedcopy number and conjugation of the virulenceplasmid (58, 123). The intricate, multistageinterplay between pathogenic agrobacteria andplants is among the best-studied examples ofhost-microbe interactions.

A. tumefaciens and A. rhizogenes cause plantdisease via a similar horizontal gene transfermechanism. However, the plant-microbesignaling mechanisms are best studied for A.tumefaciens. Therefore, the sections that followare based primarily on experimental findingsfrom A. tumefaciens, but much of it can bebroadly generalized to both species.

Activation of Virulence Functions

The primary regulators of Ti plasmid virulencegene expression make up a two-component reg-

ulatory system, with VirA functioning as a histi-dine sensor kinase and VirG as a DNA-bindingresponse regulator (105, 126). PhosphorylatedVirG activates expression of most vir geneswith the exception of virA. At least four signalsproduced by plant tissues are thought to influ-ence virulence activation through VirA-VirG.Phenolic compounds are the primary signalbut are augmented by certain sugars, acidicconditions, and low levels of phosphorus (125).

A. tumefaciens can respond to a broadrange of phenolic compounds producedby plants. The optimal phenolic signalscan vary depending on the A. tumefaciensisolate, but acetosyringone (4′-hydroxy-3′,5′-dimethoxyacetophenone) was one of the firstcharacterized vir inducers and is used as amodel phenolic inducer (104). These phenolicsgenerally share a benzene ring with a hydroxylgroup at position 4 and a methoxy group atposition 3 on the ring (75). Inducing activityis enhanced by a second methoxy group at ringposition 5. There is significant variation tol-erated at position 1 among active compounds.Some of the plant-released phenolics can alsobe inhibitory to the growth of A. tumefaciens,and consequently virH2 encodes a cytochromeP450 that can decrease the toxicity of thesecompounds by O-demethylation, in some casesallowing metabolism of the products (53).

The response to phenolics requires theVirA-VirG system. VirA is a sensor kinase thathas two transmembrane segments that flank alarge periplasmic domain. On the cytoplasmicside of the second transmembrane segment isa so-called linker domain, initially thought toplay a passive connecting function in the pro-tein but now considered to comprise a smallligand-binding GAF (cGMP-specific phospho-diesterases, adenylyl cyclases and FhlA)-typemotif implicated in the perception of pheno-lics (39). Associated with the C-terminal por-tion of the linker domain is the canonical kinasedomain, including the conserved histidine (H)residue at which autophosphorylation occurs.Finally, there is a carboxy-terminal receiver do-main that is homologous to the aminoterminalphosphoreceiver domain in response regulators

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and contains a conserved aspartate (D) residue.Surprisingly, the phenolic inducers were foundto be perceived through interactions with thecytoplasmic linker domain rather than theperiplasmic domain (14). Although some dis-agreement remains whether VirA directly bindsto the phenolics (62), it is clear that the VirAlinker region is required for the phenolic re-sponse, and the simplest interpretation is thatthis is through direct binding to the presump-tive GAF domain. Consistent with this model,several lines of genetic evidence suggest thatVirA imparts specificity to phenolics (63, 68).

The presence of certain monosaccharidesugars can have a profound impact on VirA-VirG-dependent activation of virulence genes,potentiating the vir response at lower levelsof phenolics. Sugar perception is mediatedthrough the VirA periplasmic domain andits interaction with a specific binding proteinknown as chvE (chromosomal virulence) thatis similar to other periplasmic, sugar-bindingproteins (10, 101). Inducing sugars bind ChvEin the periplasm and transduce this informationto an alphahelical region of VirA thought toresemble sensory domains of methyl chemo-taxis proteins (79). There is specificity in thesugar inducers, and it is thought that the mostactive compounds are similar to plant cell wallcomponents.

Acidic pH also contributes to vir geneactivation in multiple ways. VirA is responsiveto acidic pH, via its periplasmic domain,through its interaction with ChvE and sugars(38). In addition, expression of the virG geneis activated under low pH via one of its twopromoters (125), presumably by the ChvG-ChvI two-component system, which is knownto mediate a transcriptional response to lowpH (132). VirG levels are limiting for vir geneinduction, so increases in VirG levels wouldboost the strength of the response to phenolics.Expression of virG is also activated by limitingphosphate availability through the activity of itsother promoter (125). This is presumed to bethrough the PhoR-PhoB, which is a phosphate-responsive two-component system. Activationof virG requires so called pho box promoter

sequences, but PhoR-PhoB-dependent reg-ulation has never been established, probablybecause of the essentiality of phoR and phoB inA. tumefaciens (21).

Response to Opines

Successful A. tumefaciens transformation ofplants with the natural T-DNA is a veryenergetically expensive process, but the payofffor the pathogen is access to opines, whichare a source of custom nutrients (90, 91). Forwild-type A. tumefaciens, catabolic functions foropines are largely encoded on the Ti plasmid.The presence of opines produced by crowngall tissue can be viewed as an indicator ofsuccessful transformation. Opines are generallytaken up via active transport, and once in thecytoplasm, can interact with opine-responsivetranscriptional regulators that control theplasmid-encoded catabolic functions (46, 116).These systems are regulated much like othercatabolic systems in bacteria, in which thegenes specifying uptake and degradation areonly strongly expressed in the presence of thecatabolite. Several opine-responsive repressorsand activators have been identified, repre-senting completely different protein families(6, 121). Opines derived from amino acids,such as octopine and nopaline, are recognizedby LysR-type transcription regulators. Forexample, in the presence of octopine, the OccRprotein activates a promoter upstream of alarge 15-kb operon that encodes the octopineuptake system and catabolic functions (35, 46).For other opines derived from sugars, such asthe agrocinopines and mannopine, LacI-typerepressors (AccR and MocR, respectively)function to limit catabolic gene function in theabsence of the catabolite, and these genes arederepressed when the inducing opine bindsand inactivates the repressor (6). In either case,catabolic capacity for the opine is stronglyelevated in the tumor environment.

Opine Signals ActivateQuorum Sensing

In addition to the regulation of opinecatabolism, interbacterial conjugation of the Ti


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plasmid from Ti-harboring strains to recipientagrobacteria lacking the Ti plasmid is activatedby a subset of the opines, known as conjugalopines, produced from infected tissues (27,58). Extensive studies have determined in thebest-studied A. tumefaciens strains that althoughopines are absolutely required for conjugation,they do not directly activate conjugal transfer(tra) genes. Rather, conjugal opines induce theexpression of the QS LuxR-type transcriptionalactivator called TraR (36, 88, 135). TraR wasone of the first LuxR-type proteins, in additionto LuxR itself, found to respond to AHLs andto drive the QS process. TraR responds to3-oxo-octanoyl-L-homoserine lactone (3-oxo-C8-HSL), the synthesis of which is directed bythe TraI AHL synthase, also encoded on theTi plasmid (36, 52, 78). TraR-AHL complexesactivate expression of the tra operons, drivingconjugation in response to the populationdensity of Ti plasmid–harboring bacteria (34).The traI gene is also activated by TraR, cre-ating a positive feedback loop. The Ti plasmidreplication genes are also under TraR control,and thus the plasmid copy number is increasedas a function of QS (65, 85). An antiactivatorprotein called TraM is required to keep TraRin the inactive configuration through formationof a heterocomplex, and traM itself is underTraR control, creating a negative feedbackloop (32, 51). Remarkably, the strict opine-dependent regulation of traR expression hasbeen maintained between different A. tumefa-ciens strains, even though the regulators, operonorganization, and regulatory mechanism canbe quite different. For example, the LysR-typeregulator OccR activates traR expression, andhence conjugation and increased copy numberin response to octopine, the conjugal opinefor octopine-type plasmids (35). In contrast,the LacI-type repressor AccR represses traRexpression, but is inactivated by agrocinopine,the conjugal opine for nopaline-type Ti plas-mids (89). There is clearly a strong selection forthe TraR-dependent QS control to be underthe strict regulation of plant-released opines.A further twist on opine control is found in theoctopine-type A. tumefaciens strains, in which

the mannityl opines that are also specified bythe T-DNA of this strain activate expression ofa truncated TraR homolog, known as TrlR (orTraS), and this serves as an additional inhibitorof TraR-dependent activation (13, 82). In thiscase, the mixture of opines produced by theinfected plant dictates the copy number ofthe Ti plasmid and the degree to which it ishorizontally transferred. It is not clear what ad-vantage, if any, this baroque opine-dependentcontrol of the Ti plasmid might provide.

PLANT PHENOLICS AS SIGNALSFOR PHYTOPATHOGENICBACTERIAL GENE EXPRESSIONIN OTHER BACTERIAL SPECIES

Studies on the induction of toxigenesis inthe plant pathogen P. syringae pv. syringae(a leaf pathogen of several crops) revealedthat virulence genes were induced by specificplant signal molecules. More precisely, thegenes involved in the biosynthesis of thetwo lipodepsipeptide phytotoxins (syringom-cyin and syringopeptin) that are synthesizednonribosomally are induced by plant signalmolecules (77, 122). The syr and syp geneclusters encoding for syringomycin and sy-ringopeptin biosynthesis, respectively, areadjacent, consisting of a genomic region ofapproximately 132 kb. These loci are underthe control of the SalA and SyrF regulators(69, 70, 122). Another element involved in theregulation of syr and syp expression is the globaltwo-component GacA/GacS signal transduc-tion system, which regulates salA and syrF (57,69). Importantly, induction of syr and syp genes,which leads to the phytotoxin synthesis, occursin the plant environment via a response to theplant signal molecules arbutin and D-fructose(122). The current working model shows thatP. syringae senses the signal molecules in theplant apoplast via the GacS transmembranesensor or some currently unidentified sensor.GacS then leads to activation of salA transcrip-tion via the GacA response regulator; finally,SalA activates expression of the syrF regulator,which then directly transcriptionally activates

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syr and syp genes. This model has several pointsof uncertainty, especially regarding which reg-ulatory protein(s) senses the plant compoundsand whether more plant signals are involved.Interestingly, the regulation of lipodepsipep-tide by plant compounds via GacA/GacS hasalso been reported for a beneficial rhizospherePGPR Pseudomonas strain (61).

Plant phenolic compounds have also beenshown to regulate virulence genes in plant-pathogenic Dickeya dadantii, the causative agentof soft-rot, wilt, and blight diseases on sev-eral plant species. Studies have shown thatplant phenolics o-coumaric acid (OCA) and t-cinnamic acid (TCA) affect expression of thetype III secretion system (T3SS) (66, 128). Asthe main role of the T3SS of phytopathogens isto neutralize the plant host defense system dur-ing bacterial invasion, it is important that it isactivated in planta. Three T3SS-related genes(dspE, which encodes a T3SS effector; hrpA,which encodes a structural protein of the T3SSpilus; and hrpN, which encodes for a T3SS hair-pin) are induced by TCA and OCA at concen-trations that mimic physiological in planta con-ditions. Just as with P. syringae, this regulationin response to plant phenolic compounds re-quires the GacA/GacS system. Evidence sug-gests that GacA/GacS regulates the levels of theregulatory RNA rsmB, which then modulatesthe activity of the RsmA posttranscriptionalregulator, affecting RNA levels of target genes(66, 128). Interestingly, very recently plant phe-nolic compounds that induce T3SS genes viaGacA/GacS have also been reported to act inthe human opportunistic pathogen P. aerugi-nosa, which can also associate with plants (127).

BACTERIALDIKETOPIPERAZINES ASPLANT SIGNALS

Diketopiperazines (DKPs) are cyclodipeptidesproduced by several bacterial species. Theircurrent biological role in bacteria is not clear,but they may represent a new class of bacterialQS signals (59, 102). Furthermore, in gram-negative bacteria they have also been reportedto interfere with AHL-QS, further highlight-ing their possible role in cell-cell signaling (9,22, 49). Recently, DKPs have been implicatedin interkingdom signaling between plants andbacteria, whereby bacterially produced DKPshave a role in plant signaling (83). ThreeDKPs produced by P. aeruginosa, cyclo(L-Pro-L-Tyr), cyclo(L-Pro-L-Val), and cyclo(L-Pro-L-Phe), stimulate root and shoot biomass andlateral root development in A. thaliana. Inter-estingly, production of these three compoundsin P. aeruginosa is negatively regulated by theLasI/R AHL-QS system (83). Importantly, thethree DKPs produced by P. aeruginosa pos-sess a heterocyclic system also found in auxin,and all three show a weak auxin-like activ-ity. Several lines of evidence, including com-putational molecular docking analysis with theTIR1 auxin receptor, indicate that DKPs couldact as auxin signal mimics (83). Interestingly,several plant growth–promoting Pseudomonasspp. release several DKPs (22, 49), hence thesecould be involved in plant growth promotion.It is therefore possible that further studies onDKPs will reveal that they represent a new classof molecules involved in bacterial and interk-ingdom signaling.

SUMMARY POINTS

1. Interkingdom chemical signaling has been extensively studied between agrobacterialpathogens and their host, and this has revealed complex and pervasive interkingdomcommunication.

2. The recent finding of a widespread bacterial LuxR subfamily of proteins that binds plantcompounds and regulates plant-bacteria interactions is evidence that the same family ofproteins that are involved in bacterial communication can also serve in interkingdomsignaling.


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3. Plant phenolic compounds affect gene expression in several bacterial species that directlyor indirectly involve the GacA/GacS two-component system.

4. Bacterial QS signals can behave as plant cues linking QS to interkingdom signaling.Plants have a range of functional responses to AHLs that might have important roles inpathogenic outcomes.

5. Plants produce AHL-mimic compounds that may be involved in QS interference, sug-gesting an important role in pathogenic interactions.

6. Bacterial DKPs may represent a new class of signaling molecules involved in bacterialand interkingdom signaling.

7. Current knowledge in interkingdom signaling is limited and will most probably becomea major research field in the future.

8. Many compounds produced by plants influence their interactions with bacteria.

9. The interaction of A. tumefaciens with plants represents a well-characterized series ofplant-microbe and microbe-microbe signaling processes.

10. Plant interkingdom signaling molecules can possibly result in temporal and spatial reg-ulation directing complex changes in bacterial gene expression affecting plant-bacteriainteraction.

11. Understanding interkingdom signaling will allow the future design of specific strategiesto create plants with enhanced resistance to plant pathogens.

FUTURE ISSUES

1. Are many of the low-molecular-weight compounds synthesized de novo by plants uponpathogen attack involved in interkingdom signaling?

2. Are plant interkingdom signals host-specific or conserved throughout the plant kingdom?

3. Do plant-beneficial and pathogenic bacteria respond to the same plant interkingdomsignals?

4. Strigolactones have been recently shown to be important interkingdom signals be-tween plant and mycorrhizal fungi. Are these molecules also involved in plant-bacteriacommunication?

5. Are specific host-pathogen signals, as are found in Agrobacterium, common among plant-associated bacteria?

6. Are there other unrecognized subfamilies of regulatory proteins widely found in plant-associated bacteria that bind and respond to plant signals?

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

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ACKNOWLEDGMENTS

The laboratory of V.V. is supported by Progetto AGER (grant number 2010–2369), by the ItalianInstitute of Technology via the project Inese, and by ICGEB core funding. Research on Agrobac-terium and quorum sensing in the laboratory of C.F. is supported by the U.S. National Institutesof Health (GM092660, GM080546) and the U.S. National Science Foundation (MCB-0703467).

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PY51-FrontMatter ARI 14 July 2013 9:7

Annual Review ofPhytopathology

Volume 51, 2013Contents

Will Decision-Support Systems Be Widely Used for the Managementof Plant Diseases?Dani Shtienberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Chemical Signaling Between Plants and Plant-Pathogenic BacteriaVittorio Venturi and Clay Fuqua � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �17

Biology, Epidemiology, and Control of HeterobasidionSpecies WorldwideMatteo Garbelotto and Paolo Gonthier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �39

Pine Wood Nematode, Bursaphelenchus xylophilusKazuyoshi Futai � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �61

The Life History of Pseudomonas syringae: Linking Agricultureto Earth System ProcessesCindy E. Morris, Caroline L. Monteil, and Odile Berge � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �85

Trichoderma Research in the Genome EraPrasun K. Mukherjee, Benjamin A. Horwitz, Alfredo Herrera-Estrella,

Monika Schmoll, and Charles M. Kenerley � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 105

Experimental Measures of Pathogen Competition and Relative FitnessJiasui Zhan and Bruce A. McDonald � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 131

Quiescent and Necrotrophic Lifestyle Choice During PostharvestDisease DevelopmentDov Prusky, Noam Alkan, Tesfaye Mengiste, and Robert Fluhr � � � � � � � � � � � � � � � � � � � � � � � � 155

Status and Prospects of Plant Virus Control Through Interferencewith Vector TransmissionC. Bragard, P. Caciagli, O. Lemaire, J.J. Lopez-Moya, S. MacFarlane, D. Peters,

P. Susi, and L. Torrance � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 177

Diversity and Evolution of Root-Knot Nematodes, Genus Meloidogyne:New Insights from the Genomic EraPhilippe Castagnone-Sereno, Etienne G.J. Danchin, Laetitia Perfus-Barbeoch,

and Pierre Abad � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 203

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Antimicrobial Defenses and Resistance in Forest Trees:Challenges and Perspectives in a Genomic EraAndriy Kovalchuk, Susanna Kerio, Abbot O. Oghenekaro, Emad Jaber,

Tommaso Raffaello, and Fred O. Asiegbu � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 221

MAPK Cascades in Plant Disease Resistance SignalingXiangzong Meng and Shuqun Zhang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 245

The Use and Role of Predictive Systems in Disease ManagementDavid H. Gent, Walter F. Mahaffee, Neil McRoberts, and William F. Pfender � � � � � � � 267

Impacts of Resistance Gene Genetics, Function, and Evolutionon a Durable FutureRichard W. Michelmore, Marilena Christopoulou, and Katherine S. Caldwell � � � � � � � � � 291

Virus-Based Transient Expression Vectors for Woody Crops: A NewFrontier for Vector Design and UseWilliam O. Dawson and Svetlana Y. Folimonova � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 321

Paradigms: Examples from the Bacterium Xylella fastidiosaAlexander Purcell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 339

Advances in Understanding Begomovirus SatellitesXueping Zhou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 357

Engineering Plant Disease Resistance Based on TAL EffectorsSebastian Schornack, Matthew J. Moscou, Eric R. Ward, and Diana M. Horvath � � � � 383

Nonhost Resistance Against Bacterial Pathogens: Retrospectivesand ProspectsMuthappa Senthil-Kumar and Kirankumar S. Mysore � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 407

The Role of Prophage in Plant-Pathogenic BacteriaAlessandro M. Varani, Claudia Barros Monteiro-Vitorello, Helder I. Nakaya,

and Marie-Anne Van Sluys � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 429

Considerations of Scale in the Analysis of Spatial Patternof Plant Disease EpidemicsWilliam W. Turechek and Neil McRoberts � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 453

Pseudomonas syringae pv. tomato DC3000: A Model Pathogen forProbing Disease Susceptibility and Hormone Signaling in PlantsXiu-Fang Xin and Sheng Yang He � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 473

Diseases in Intercropping SystemsMark A. Boudreau � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 499

Manipulation of Host Proteasomes as a Virulence Mechanism of PlantPathogensRobert Dudler � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 521

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Centrality of Host Cell Death in Plant-Microbe InteractionsMartin B. Dickman and Robert Fluhr � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 543

Continuous and Emerging Challenges of Potato virus Y in PotatoAlexander V. Karasev and Stewart M. Gray � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 571

Communication Between Filamentous Pathogens and Plants at theBiotrophic InterfaceMihwa Yi and Barbara Valent � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 587

Errata

An online log of corrections to Annual Review of Phytopathology articles may be found athttp://phyto.annualreviews.org/

Contents vii

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Annual Review of Phytopathology Volume 51 Issue 1 2013 [Doi 10.1146%2Fannurev-Phyto-082712-102239] Venturi, Vittorio; Fuqua, Clay -- Chemical Signaling Between Plants and Plant-Pathogenic

Documents

agrobacterium plant

plant phenoliccompounds

plant physiology

host plant

plant pathogens

plant andbacteria

land plants

plant hostvia lowmolecular