A report of The Keystone Symposium on Plant Innate Immunity, Keystone, USA, 10-15 February 2008

Robatzek, Silke

Saijo, Yusuke

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Silke Robatzek

Yusuke Saijo

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Plant immunity from A to Z

Robatzek, S.

Saijo, Y.

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Genome Biology 2008, 9:304Meeting reportPlant immunity from A to ZSilke Robatzek and Yusuke SaijoAddress: Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Cologne, Germany.Correspondence: Silke Robatzek. Email: robatzek@mpiz-koeln.mpg.dePublished: 9 April 2008Genome Biology 2008, 9:304 (doi:10.1186/gb-2008-9-4-304)The electronic version of this article is the complete one and can befound online at http://genomebiology.com/2008/9/4/304© 2008 BioMed Central Ltd A report of The Keystone Symposium on Plant InnateImmunity, Keystone, USA, 10-15 February 2008.Plants resist potential microbial infections by deploying awide range of innate defenses. More than 150 plant scientistsassembled recently at a Keystone Conference in Colorado todiscuss the latest advances in plant innate immunity. Manynovel and exciting findings were presented in the spirit ofthe meeting. This report highlights some key presentations.In the keynote address, Brian Staskawicz (University ofCalifornia, Berkeley, USA) illustrated major advances overthe past half century and recent paradigm shifts (Figure 1),and encouraged his audience to integrate their studies onpathogen effector functions, the in planta targets andmolecular bases of resistance towards the development ofdurable disease resistance in the field.PAMP-triggered immunityPathogen-associated molecular patterns (PAMPs) are con-served microbial structures that are perceived through hostreceptors and induce a plethora of plant defense responsestriggering immunity. In Arabidopsis, the best-characterizedPAMPs are the bacterial proteins flagellin (flg22) andtranslation elongation factor Tu (elf18), which are recog-nized by the plant receptor kinases FLS2 and EFR, respec-tively, both of which use the receptor kinase BAK1 as a co-factor. Despite its importance in plant defense, little isknown about the molecular basis of PAMP signaling and thecomponents required for PAMP-triggered immunity. CyrilZipfel (Sainsbury Laboratory, Norwich, UK) reported theisolation of more than 100 elf18-insensitive (elfin)Arabidopsis mutants that are not due to mutations in theEFR gene. The mutant elfin27-6 appeared to be unique inbeing affected in both elf18 and flg22 signaling and themutated gene responsible turned out to be BAK1. Zipfel alsoidentified elfin1 as SDF2 (stromal-derived factor 2). Sdf2mutants are specifically impaired in responses to elf18 andare highly susceptible to bacterial infection. He providedevidence that SDF2 localizes to the endoplasmic reticulum(ER) and noted that three other ELFIN genes encode proteinswith known roles in protein quality control in the ER.Paul Schulze-Lefert (Max-Planck-Institute for Plant BreedingResearch, Cologne, Germany) described the isolation of‘priority for sweet life’ (psl) mutants that exhibitderepression of sucrose-induced flavonoid accumulation (astress response) in the presence of elf18. Cloning of theresponsible genes revealed components of the ER proteinquality control system: PSL1 encodes a member of thecalreticulin family involved in the ER chaperone system andPSL2 codes for an UDP-glucose glycoprotein glucosyl-transferase that functions as a folding sensor in the ER. Bothpresentations pointed to the significance of the ER proteinfolding system during EFR-mediated PAMP-triggeredimmunity. It remains to be shown whether EFR itself is theclient of the ER quality control system.Pathogen effector moleculesOver the past few years the virulence-promoting function ofpathogen effectors and their host targets has become acenter of attention. Effectors appear to be modular proteins,an adaptation to the everlasting evolutionary arms racebetween plant and pathogen. Gregory Martin (BoyceThompson Institute for Plant Research, Ithaca, USA) hasdefined the roles of different modules in the bacterialeffector AvrPtoB from Pseudomonas syringae pv tomatoDC3000 (Figure 1). The amino terminus (amino acids 1-307)of AvrPtoB interacts with the tomato Pto kinase, whichtriggers resistance via recognition of the resistance (R)protein Prf. This region of AvrPtoB is also important for thevirulence function of the protein, and Martin reported that itassociates with the LysM-receptor kinase Bti9, a potentialvirulence target. A longer amino-terminal fragment (1-387)interacts with the tomato Fen kinase, which mediates Prfresistance in the absence of Pto. The carboxyl terminus ofAvrPtoB shares structural homology with eukaryotic E3ubiquitin ligases and ubiquitinates Fen, but not Pto. Martindiscussed the means by which Pto resists the AvrPtoB E3ligase activity and hypothesized that Pto actively inhibitsubiquitination (by phosphorylation of the ligase) or passivelyresists it (due to a lack of key lysine residues). He identifiedwild tomato accessions in which AvrPtoB-triggeredresistance occurs independently of Pto, and thus Fen alsoappears resistant to AvrPtoB-mediated degradation in theseplants, possibly due to the substitution of key lysineresidues.Martin also noted that both Pto and Fen phosphorylateAvrPtoB, but at different residues. In line with this, JohnRathjen (Sainsbury Laboratory, Norwich, UK) reported thatin Nicotiana benthamiana Pto phosphorylates AvrPtoB inthe E3 ligase domain and that the Pto kinase activity isrequired for preventing AvrPtoB-mediated ubiquitination ofPto. In regard to the virulence function of AvrPtoB, Rathjenreported that AvrPtoB associates with the Arabidopsiskinase chitin elicitor receptor kinase 1 (CERK1), anotherreceptor that activates plant defenses. Thorsten Nürnberger(University of Tübingen, Germany) described work done incollaboration with Jen Sheen (Harvard Medical School,Boston, USA) showing that AvrPto and AvrPtoB bothinteract with FLS2 and BAK1 and inhibit flg22-triggeredFLS2/BAK1 complex formation. AvrPtoB thus has multiplefunctions and, as it can suppress both PAMP-triggeredimmunity and effector-triggered immunity, it provides cluesto trace how plant-microbe coevolution has shaped thevirulence strategy of a pathogen.Regine Kahmann (Max-Planck-Institute for TerrestrialMicrobiology, Marburg, Germany) presented a genomicapproach to identifying effectors of the smut fungus Ustilagomaydis. Genome sequencing of U. maydis has revealedabout 550 proteins that are predicted to be secreted.Comparison of the genomes of U. maydis and Sporisoriumreilianum, a close relative that, unlike U. maydis, does nottrigger tumor formation during infections, uncovered a highdegree of sequence conservation and synteny, whereas genesin previously defined pathogenicity clusters were only poorlyconserved. The deletion of one poorly conserved patho-genicity cluster resulted in loss of pathogenesis in U. maydis,but S. reilianum retained full virulence. The deletion mutantsof U. maydis proliferated inside the plant but failed to elicithttp://genomebiology.com/2008/9/4/304 Genome Biology 2008, Volume 9, Issue 4, Article 304 Robatzek and Saijo 304.2Genome Biology 2008, 9:304Figure 1Classic and current views of plant-microbe interactions. (a) The ‘gene-for-gene’ model proposed by HH Flor in 1946 is illustrated by the interaction ofP. syringae AvrPtoB and tomato Pto, which is guarded by the resistance (R) gene Prf. A plant cultivar expressing a given R gene is resistant to a pathogenstrain delivering a cognate avirulence (Avr) gene. This host-pathogen incompatibility is typically accompanied by the hypersensitive response (HR). Ifeither component of the Avr/R gene pair is missing, the plant-microbe interaction becomes compatible and disease occurs. (b) The ‘zigzag’ modelproposed by Jonathan Jones and Jeffery Dangl in 2006. The perception of PAMPs (for example, flg22) by a cognate pattern recognition receptor (forexample, FLS2) mediates PAMP-triggered immunity (PTI). Pathogens secrete effectors (for example, AvrPtoB N-ter) that suppress PAMP signaling andPAMP-triggered immunity, and thus confer disease in the absence of R protein activation. In resistant tomato plants, Prf recognizes AvrPtoB N-ter viaFen and induces a reinforcement of defense termed effector-triggered immunity (ETI). To counteract this, P. syringae has acquired a new function forAvrPtoB by the addition of a carboxy-terminal E3 ligase domain that targets Fen for degradation. In turn, tomato plants have evolved Pto that resistsAvrPtoB-mediated degradation and triggers strong ETI involving the HR. Compared with the gene-for-gene relationship, this model integrates the multi-layered/stacked plant immune responses of different amplitudes and highlights the constant evolutionary adaptation in plant-microbe interactions.Components of plant immunity are shown in green, pathogen-derived molecules are depicted in red.HRDiseaseImmunityDefense amplitude  Evolution of plant-microbe interactionsflg22AvrPtoBN-terFenAvrPtoBPtoFLS2PTI ETI ETI(b)Plant cultivarPathogen strainPto ptoAvrPtoBavrPtoBHRincompatibleDiseasecompatibleDiseasecompatibleDiseasecompatible(a)tumors, and so Kahmann suggested that this cluster might beresponsible for U. maydis tumor formation. This studyemphasizes the power of comparative genomics combinedwith mutant analysis for the identification of effectorsresponsible for different stages of the infection process.The oomycetes include some serious plant pathogens, suchas Phytophthora infestans, the cause of potato blight. Inthese pathogens, as in bacteria, genome sequencing is apowerful tool for identifying the effector inventory. JimBeynon (Warwick University, UK) reported the genomesequencing of the oomycete Hyaloperonospora parasitica,and predicted the presence of about 200 so-called RxLReffectors (named after a shared RxLR amino acid motif).Sophien Kamoun (Sainsbury Laboratory, Norwich, UK)presented a genome-wide catalogue of oomycete effectors.He focused on the Phytophthora CRINKLER family ofeffectors, which trigger cell death in plants and compriseabout 200 members carrying an LxLFLAK motif. JeanGreenberg (University of Chicago, USA) formulated aninteresting question: why do pathogens encode so manyeffectors, for example, the 30-40 effectors in P. syringae?She proposed that pathogens require different sets ofeffectors in different infection phases, such as epiphyticgrowth and growth inside the plant.Networks in defense and hormone signaling, growthcontrol and diseaseCorné Pieterse (Utrecht University, The Netherlands)described the antagonism between salicylic acid (SA) andjasmonic acid (JA) signaling pathways in diverse plant-microbe interactions. He has observed the suppression ofJA-induced expression of the defensin gene PDF1.2 in A.thaliana upon application of SA during infection with thefungus Alternaria or with a combined H. parasiticainfection and infestation by caterpillars of the cabbage whitebutterfly (Pieris rapae). He found that this effect is longlasting, and is conserved in different A. thaliana accessions.Interestingly, the SA-mediated repression of JA signaling isabolished by the loss of non-expressor of PR-1 (NPR1) orglutathione biosynthesis; the NPR1-dependence is, however,rescued by ethylene. Gene-expression profiling revealed that30% of JA-responsive genes and 20% of SA-responsivegenes are under the antagonistic control by the otherhormone. Pieterse proposed that regulation of the SA/JAcross-talk occurs at the transcriptional level.Jane Glazebrook (University of Minnesota, Minneapolis-StPaul, USA) described work with Fumi Katagiri on the use ofDNA miniarrays to study the gene-expression profiles ofpathogen-responsive genes in a large number of knowndefense and signaling mutants of Arabidopsis uponchallenge with P. syringae DC3000 AvrRpt2. Systems-biology principles were applied to the data to determinepositive and negative interactions among components ofplant immunity. The analysis indicated that SA signaling ispart of PAMP signaling, and also revealed a calmodulin-binding protein as a node in the network of SA and PAMPsignaling. Mutations in the gene encoding this proteinenhanced disease susceptibility and reduced PAMP-inducedaccumulation of SA.We were reminded by Jonathan Jones (Sainsbury Labora-tory, Norwich, UK) that many plant pathogens produce planthormones, such as auxin or gibberellic acid. He reportedthat auxin promotes pathogen propagation and compro-mises PAMP-induced expression of PR-1, a well knownmarker gene for the SA pathway of defense responses. Jonestested whether the auxin effect occurs through JA signalingantagonizing responses to SA, and found that virulence ofthe disarmed P. syringae DC3000 COR- strain, which isdeficient in the synthesis of the JA mimic coronatin, waspartially restored in mutant plants with elevated auxinlevels. In addition, he reported that DELLA proteins, whichare negative regulators of gibberellic acid signaling, arestabilized in response to PAMP treatment, and repressdefense against P. syringae. Accumulation of DELLAproteins leads to repression of SA signaling but activation ofJA signaling. Jones concluded that plant hormone pathwaysinfluence each other strongly, and thus the modulation of asingle hormone pathway can greatly affect plant defenses.Resistance protein functionPlant resistance (R) proteins monitor the actions of isolate-specific pathogen effectors, and can trigger programmed celldeath, a defense reaction known as the hypersensitiveresponse (HR). One prominent class of R proteins comprisesthe so-called nucleotide-binding site leucine-rich repeat(NB-LRR) proteins, which carry either a coiled coil (CC)domain or a Toll-interleukin receptor (TIR)-like domain attheir amino termini. Frank Takken (University ofAmsterdam, The Netherlands) updated the model of themechanism of NB-LRR protein activation. He described thecoexpression in N. benthamiana of the CC-NB-ARCdomains and TAP-tagged LRR domains derived from thetomato NB-LRR protein Mi-1, which conferred full activityas detected by HR, supporting the model of NB-LRR proteinactivation by intramolecular interactions. Takken pointedout the role of the MHD motif in the NB-ARC domain foractivation. Substitution of the conserved aspartate (D)residue in this motif caused autoactivation of four NB-LRRproteins tested, whereas replacement of the histidine (H)conferred either autoactivation or loss of function. Thegeneralization of this updated model will require furtherstudies, however. Takken also reported that the LRR domaininteracts with the chaperones Hsp90 and PP5.Kirsten Bomblies (Max-Planck-Institute for DevelopmentalBiology, Tübingen, Germany) described temperature-sensitive hybrid necrosis that occurs in crosses of normallyhttp://genomebiology.com/2008/9/4/304 Genome Biology 2008, Volume 9, Issue 4, Article 304 Robatzek and Saijo 304.3Genome Biology 2008, 9:304healthy A. thaliana accessions. She first focused on the Uk-1/Uk-3 hybrid, in which pathogen-responsive genes areexpressed constitutively, and which show cell deathreminiscent of an HR. The Uk-1/Uk-3 incompatibility wasmapped to two semi-dominant loci: DM1 in Uk-3 and DM2in UK-1. Bomblies observed a complex variation at the DM1locus, which carries two TIR-NB-LRR genes in the referencesequence, but only a single TIR-NB-LRR gene in Uk-3. ThisNB-LRR was shown to cause constitutive defense activation.Although the responsible gene at the DM2 locus is stillunknown, it should be noted that DM2 was mapped toanother complex NB-LRR cluster carrying two RPP1homologs. A further survey for a potential involvement of Rgenes in other hybrid necroses revealed that RPW8 seems toplay a role in the Mrk-0/KZ10 hybrid. R genes have beenproposed to be costly for plant growth, and the risk ofnecrosis could cause constraints on their evolution.Bomblies also referred to the Est-1 accession, in which anallele of ACD6 (a positive regulator of defense) causes HR-like lesions. Thus, the risk of necrosis caused by auto-activation of cell-death inducers in plant immunity might insome situations present a barrier to gene flow.Although the plant HR has been seen as the ultimaterestriction of pathogen propagation ever since HH Flor firstdescribed gene-for-gene resistance in the 1940s, little isknown about how HR cell death is initiated and regulated.Jeffery Dangl (University of North Carolina, Chapel Hill,USA) reviewed the LSD1-mediated control of cell deathadjacent to infection sites. LSD1 (for lesion simulatingdisease resistance 1) is a plant-specific zinc finger proteinthat regulates the oxidative stress response that accom-panies the HR. Dangl described how a gradient of SA deter-mines a cell for death. He also found that the plant NADPHoxidase AtRbohD restricts systemic cell death in lsd1mutants, which indicates that reactive oxygen species have arole in limiting the HR. He reported that LSD1 interacts withthe zinc-finger-containing metacaspases AtMC1 and AtMC2.Mutation of AtMC1 suppresses runaway cell death in lsd1and enhances the basal level of defense. Consistent with this,AtMC1 appears to be stabilized in lsd1 mutants, andconstitutive overexpression of AtMC1 induces cell death.Whereas the metacaspase AtMC1 promotes cell death, AtMC2negatively regulates cell death via repression of AtMC1.In his concluding remarks, Dangl noted that one reason forthe successful growth of the field of plant-microbe inter-actions had been the sharing of resources and unpublishedinformation between researchers, and he hoped that thiswould continue. In this respect, this meeting was a primeexample of the further nourishment of our plant immunitystudies.AcknowledgementsMany thanks to R Panstruga for reading the manuscript.http://genomebiology.com/2008/9/4/304 Genome Biology 2008, Volume 9, Issue 4, Article 304 Robatzek and Saijo 304.4Genome Biology 2008, 9:304

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