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Science 20 December 1996:
Vol. 274. no. 5295, pp. 2063 - 2065
DOI: 10.1126/science.274.5295.2063
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Reports

Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato

Steven R. Scofield, * Christian M. Tobias, * John P. Rathjen, Jeff H. Chang, Daniel T. Lavelle, Richard W. Michelmore, Brian J. Staskawicz dagger

Transient expression of the Pseudomonas syringae avirulence gene avrPto in plant cells resulted in a Pto-dependent necrosis. The AvrPto avirulence protein was observed to interact directly with the Pto resistance protein in the yeast two-hybrid system. Mutations in the Pto and avrPto genes which reduce in vivo activity had parallel effects on association in the two-hybrid assay. These data suggest that during infection the pathogen delivers AvrPto into the plant host cell and that resistance is specified by direct interaction of Pto with AvrPto.

S. R. Scofield, J. P. Rathjen, J. H. Chang, D. T. Lavelle, NSF Center for Engineering Plants for Resistance Against Pathogens (CEPRAP), University of California, Davis, CA 95616.
C. M. Tobias, Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720.
R. W. Michelmore, NSF Center for Engineering Plants for Resistance Against Pathogens and Department of Vegetable Crops, University of California, Davis, CA 95616.
B. J. Staskawicz, NSF Center for Engineering Plants for Resistance Against Pathogens and Department of Plant and Microbial Biology, University of California, Davis, CA 94720.
*   These authors made equal contributions to this report.

dagger    To whom correspondence should be addressed. E-mail: stask{at}garnet.berkeley.edu

In plants, resistance to a variety of pathogens is determined by the action of complementary pairs of resistance (R) genes in the host and avirulence (avr) genes in the pathogen. These gene-for-gene interactions have been observed between plants and a diverse array of pathogens, including viruses, bacteria, fungi, nematodes, and insects (1). From genetic analysis it has been proposed that R genes recognize an elicitor produced directly or indirectly by the pathogen's avr gene, which leads to a resistance response in the infected plant (2).

Bacterial speck disease of tomato is caused by Pseudomonas syringae pv. tomato (Pst). In tomato, resistance to strains of Pst that contain the avr gene avrPto is conferred by the Pto gene (3). The Pto locus encodes a family of related serine-threonine kinases. Among these, Fen is active in a parallel pathway that confers sensitivity to the insecticide fenthion (4).

R and avr proteins may interact directly, thereby activating plant defenses. For the protein product of Pto, this binding would likely occur intracellularly because of its predicted cytoplasmic localization. The activity of many avr genes, including avrPto, depends on an hrp secretion pathway which is similar to the type III secretory systems of Yersinia, Shigella, and Salmonella (5). These pathogens translocate a set of virulence proteins into host cells. Therefore, we considered the possibility that the bacterial AvrPto protein moves across the plant cell wall and plasma membrane where it directly interacts with the tomato Pto protein.

Evidence indicating that AvrPto acts inside the plant cell was obtained by transiently expressing avrPto in transgenic Nicotiana benthamiana plants transformed with Pto (6) (Fig. 1). This resulted in necrosis similar to the Pto-mediated HR elicited by P. syringae expressing avrPto and indicated that AvrPto was active within the plant cell. Deletion of 30 amino acids from the COOH-terminus of AvrPto did not eliminate this activity, whereas deletion of 59 amino acids destroyed activity. Activity of the deletion derivatives in the transient expression assays correlated with biological activity in P. syringae. These results suggested that the products of the avr and R genes may interact directly.

Fig. 1. Agrobacterium tumefaciens strain A281 (sites 3 to 6) or the nontumorogenic strain C58C1 (sites 1 and 2) containing avrPto gene constructs (10) were infiltrated into leaves of a Pto transformed plant (A) or leaves of untransformed N. benthamiana (B). Expression of avrPto (sites 1 and 4), and avrPto deletions of 30 (site 6), and 59 (site 3) amino acids off the COOH-terminus was controlled by the CaMV 35S viral promoter in a binary plan transformation vector. An avrPto construct (pPtE6) lacking left and right T-DNA borders or a plant promoter (11) was also infiltrated (sites 2 and 5). Leaves were photographed 3 days after inoculation. [View Larger Version of this Image (107K GIF file)]

We employed the yeast two-hybrid system to directly test this hypothesis (7). Pto, Fen, and avrPto coding sequences were expressed as fusions to GAL4 DNA binding (BD) and transcriptional activating (AD) domains. Reciprocal combinations of BD and AD fusions were tested for beta -galactosidase reporter gene activity in yeast. Interaction was only observed when the BD::Pto and AD::AvrPto fusions were coexpressed (Fig. 2). Controls did not show any interaction. Furthermore, no interaction was detected between BD::Fen and AD::AvrPto (Figs. 2 and 3A).

Fig. 2. Yeast strain Y190 transformed with various combinations of two-hybrid plasmids were tested for beta -galactosidase activity. Plasmids encoding fusions to the GAL4 DNA binding domain are indicated by BD, whereas fusions to GAL4 transcriptional activation domain are denoted by AD. The pair of plasmids encoding BD fusions to murine p53 (BD::p53) and AD fusions to SV40 large T antigen (AD::LTA) serve as controls for the specificity of the Pto-AvrPto interaction (7). [View Larger Version of this Image (106K GIF file)]

Fig. 3. Analysis of avrPto and Pto interaction. Pto sequences are represented by open boxes, Fen sequences by filled boxes, AvrPto sequences by slashed boxes (12). Numbers and arrows indicate relative positions of amino acids in the sequence (4, 5). Single-letter amino acid codes are used to indicate mutations where relevant. (A) Interaction of AvrPto with Pto and Fen. (B) Activity of in vivo Pto mutants, pto6, pto7, and pto11 (8). (C) Activity of avrPto COOH-terminal deletions. (D) Activity of reciprocal Fen-Pto swaps. PFBglII and FPBglII. (E) Analysis of Fen-Pto fusions. The region shown corresponds to catalytic kinase subdomains VIB-IX (11). (F) Effects of amino acid substitution of invariant catalytic residues. Average beta -galactosidase activities were determined on at least three colonies from each transformation, with three replicates for each colony (13). Western blot analysis demonstrated that mutant Pto and AvrPto fusion proteins accumulate to similar levels as wild-type fusions (data not shown). [View Larger Version of this Image (24K GIF file)]

To test the biological relevance of the interaction, inactive alleles of Pto and avrPto were tested. Three inactive Pto alleles, pto6, pto7 and pto11, were previously identified through mutagenesis of resistant tomato plants (8). Sequence analysis revealed single amino acid changes in each mutant allele (Fig. 3B). The mutant Pto sequences showed no detectable interaction with AvrPto in yeast. Thus, mutant alleles that confer susceptibility to Pst also fail to interact with AvrPto in the two-hybrid system. The two deletions of AvrPto tested in the transient expression assay were examined for their ability to interact with Pto (Fig. 3C). AvrPto Delta 30C, which is biologically active, interacted with Pto, whereas Delta 59C, which had no biological activity, showed no interaction. Therefore, the binding activity of mutants of both Pto and AvrPto coincides with reduced biological function in vivo.

Because Fen is 80% identical to Pto at the amino acid level but does not interact with AvrPto, it provides a model for defining the Pto sequences responsible for specific interaction with AvrPto. Reciprocal Fen-Pto hybrid constructs demonstrated that the COOH-terminal 192 amino acids of Pto contain the residues necessary to confer binding to AvrPto (Fig. 3D). Analysis of a series of Fen-Pto gene fusions recombinant at variant residues between amino acids 167 and 239 places the residues responsible for specific binding between amino acids 190 and 213 (Fig. 3E). There are only four variant amino acids in this interval, which also corresponds to conserved kinase subdomain VIII, a region implicated in substrate binding in other kinases (9). Although the series of recombinant molecules was useful for defining a small region of Pto essential for specific interaction, the fact that the hybrid genes displayed reduced beta -galactosidase activity indicates that other residues also participate in binding.

Two invariant residues essential for kinase catalytic activity in Pto were mutated to examine the role of kinase function in the interaction with AvrPto (Fig. 3F). Neither mutant showed detectable interaction with AvrPto. These results suggest that phosphorylation activity of Pto is required for the binding of AvrPto, although it is possible that the engineered mutations may abolish binding by some other effect.

These data suggest that Pto-mediated disease resistance involves entry of AvrPto into the plant cell and interaction with the Pto kinase. The high degree of recognitional specificity that is the hallmark of gene-for-gene disease resistance systems is evident at the molecular level. Although the determinants of specificity reside in regions of Pto that correspond to conserved kinase domains involved in substrate recognition, these residues alone are insufficient for mediating interaction with AvrPto. Mutations in residues essential for ATP binding and catalytic activity also eliminate detectable binding to AvrPto. Thus, our analysis shows that alterations in different parts of Pto can eliminate the ability to interact with AvrPto.

Demonstration of direct binding between R and Avr proteins supports a receptor-ligand model for recognition in plant-pathogen interactions. Pto is unique among the cloned R genes in lacking a leucine-rich repeat (LRR) motif. LRRs are known to mediate protein-protein interactions and are found in some receptor molecules, making them logical candidates for mediating the recognition of avr molecules. Pto-mediated resistance does require an LRR protein encoded by the Prf gene, located within the Pto locus, and it is somewhat surprising that AvrPto interacts directly with Pto. Perhaps Pto and AvrPto form a complex which is then able to interact with Prf. It will be interesting to see if this system represents a unique class of resistance mechanism that utilizes a kinase as the element to determine specificity, or whether there are orthologous kinases participating in other resistance systems.

Isolation of avr genes has proven to be a more tractable biological task than cloning plant R genes. Our experiments suggest that, at least for systems involving recognition within the plant cytoplasm, it may be possible to use avr genes as bait in the yeast two-hybrid system to isolate the corresponding R genes from plant cDNA libraries.

REFERENCES AND NOTES

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  10. Transient Agrobacterium-mediated transformation was performed by pressure infiltration of leaves with Agrobacterium at a density of 1 to 2 × 109 cfu/ml. The full-length and delted AvrPto constructs were cloned into the pBIN19 derivative pMD1. Positive clones were introduced into Agrobacterium via electroporation.
  11. P. C. Ronald, J. M. Salmeron, F. C. Carland, B. J. Staskawicz, J. Bacteriol. 174, 1604 (1992) [Medline].
  12. Mutations were introduced to the Pto gene sequence by recombinant polymerase chain reaction with the use of cloned Pto and Fen templates (D.T.L., J.P.R. and J.H.C., unpublished data). Recombinant PCR products were cloned into the yeast two-hybrid vector pAS2-1 (Clontech) and sequenced before testing. Wild-type and mutant avrPto genes were cloned into a pACT2 (Clontech).
  13. J. H. Miller, Experiments in Molecular Genetics (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1972).
  14. We thank D. O. Lavelle, J. Gardner, and J. Luke for DNA sequencing and G. Oldroyd, M. B. Mudgett, S. Barker, V. Szabo, and L. Doyle for comments on the manuscript. Supported by NSF Cooperative Agreement BIR-8920216 to CEPRAP and by CEPRAP corporate associates Calgene, Inc., Ciba Geigy Biotechnology Corporation, Sandoz Seeds, and Zeneca Seeds.

30 August 1996; accepted 22 November 1996


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J. Bacteriol. 182, 3498-3507
   Abstract »    Full Text »
The Alternative Sigma Factor RpoN Is Required for hrp Activity in Pseudomonas syringae pv. Maculicola and Acts at the Level of hrpL Transcription.
E. L. Hendrickson, P. Guevera, and F. M. Ausubel (2000)
J. Bacteriol. 182, 3508-3516
   Abstract »    Full Text »
Members of the Arabidopsis HRT/RPP8 Family of Resistance Genes Confer Resistance to Both Viral and Oomycete Pathogens.
M. B. Cooley, S. Pathirana, H.-J. Wu, P. Kachroo, and D. F. Klessig (2000)
PLANT CELL 12, 663-676
   Abstract »    Full Text »
Pti4 Is Induced by Ethylene and Salicylic Acid, and Its Product Is Phosphorylated by the Pto Kinase.
Y.-Q. Gu, C. Yang, V. K. Thara, J. Zhou, and G. B. Martin (2000)
PLANT CELL 12, 771-786
   Abstract »    Full Text »
Characterization of the Cryptogein Binding Sites on Plant Plasma Membranes.
S. Bourque, M.-N. Binet, M. Ponchet, A. Pugin, and A. Lebrun-Garcia (1999)
J. Biol. Chem. 274, 34699-34705
   Abstract »    Full Text »    PDF »
The C Terminus of AvrXa10 Can Be Replaced by the Transcriptional Activation Domain of VP16 from the Herpes Simplex Virus.
W. Zhu, B. Yang, N. Wills, L. B. Johnson, and F. F. White (1999)
PLANT CELL 11, 1665-1674
   Abstract »    Full Text »
The Avr (Effector) Proteins HrmA (HopPsyA) and AvrPto Are Secreted in Culture from Pseudomonas syringae Pathovars via the Hrp (Type III) Protein Secretion System in a Temperature- and pH-Sensitive Manner.
K. van Dijk, D. E. Fouts, A. H. Rehm, A. R. Hill, A. Collmer, and J. R. Alfano (1999)
J. Bacteriol. 181, 4790-4797
   Abstract »    Full Text »
Identification of Three Putative Signal Transduction Genes Involved in R Gene-Specified Disease Resistance in Arabidopsis.
R. F. Warren, P. M. Merritt, E. Holub, and R. W. Innes (1999)
Genetics 152, 401-412
   Abstract »    Full Text »
The Rx Gene from Potato Controls Separate Virus Resistance and Cell Death Responses.
A. Bendahmane, K. Kanyuka, and D. C. Baulcombe (1999)
PLANT CELL 11, 781-792
   Abstract »    Full Text »
Isolation of Ethylene-Insensitive Soybean Mutants That Are Altered in Pathogen Susceptibility and Gene-for-Gene Disease Resistance.
T. Hoffman, J. S. Schmidt, X. Zheng, and A. F. Bent (1999)
Plant Physiology 119, 935-950
   Abstract »    Full Text »
Pathogen-Induced Elicitin Production in Transgenic Tobacco Generates a Hypersensitive Response and Nonspecific Disease Resistance.
H. Keller, N. Pamboukdjian, M. Ponchet, A. Poupet, R. Delon, J.-L. Verrier, D. Roby, and P. Ricci (1999)
PLANT CELL 11, 223-236
   Abstract »    Full Text »
Rapid Avr 9- and Cf-9 –Dependent Activation of MAP Kinases in Tobacco Cell Cultures and Leaves: Convergence of Resistance Gene, Elicitor, Wound, and Salicylate Responses.
T. Romeis, P. Piedras, S. Zhang, D. F. Klessig, H. Hirt, and J. D. G. Jones (1999)
PLANT CELL 11, 273-288
   Abstract »    Full Text »
Overexpression of P to Activates Defense Responses and Confers Broad Resistance.
X. Tang, M. Xie, Y. J. Kim, J. Zhou, D. F. Klessig, and G. B. Martin (1999)
PLANT CELL 11, 15-30
   Abstract »    Full Text »
The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response.
D. C. Boyes, J. Nam, and J. L. Dangl (1998)
PNAS 95, 15849-15854
   Abstract »    Full Text »    PDF »
Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process.
R. W. Michelmore and B. C. Meyers (1998)
Genome Res. 8, 1113-1130
   Abstract »    Full Text »
Three Genes of the Arabidopsis RPP1 Complex Resistance Locus Recognize Distinct Peronospora parasitica Avirulence Determinants.
M. A. Botella, J. E. Parker, L. N. Frost, P. D. Bittner-Eddy, J. L. Beynon, M. J. Daniels, E. B. Holub, and J. D. G. Jones (1998)
PLANT CELL 10, 1847-1860
   Abstract »    Full Text »    PDF »
The Tomato Cf-5 Disease Resistance Gene and Six Homologs Show Pronounced Allelic Variation in Leucine-Rich Repeat Copy Number.
M. S. Dixon, K. Hatzixanthis, D. A. Jones, K. Harrison, and J. D. G. Jones (1998)
PLANT CELL 10, 1915-1926
   Abstract »    Full Text »    PDF »
The Pseudomonas syringae pv. tomato HrpW Protein Has Domains Similar to Harpins and Pectate Lyases and Can Elicit the Plant Hypersensitive Response and Bind to Pectate.
A. O. Charkowski, J. R. Alfano, G. Preston, J. Yuan, S. Y. He, and A. Collmer (1998)
J. Bacteriol. 180, 5211-5217
   Abstract »    Full Text »
Negative Regulation of hrp Genes in Pseudomonas syringae by HrpV.
G. Preston, W.-L. Deng, H.-C. Huang, and A. Collmer (1998)
J. Bacteriol. 180, 4532-4537
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A Mutation within the Leucine-Rich Repeat Domain of the Arabidopsis Disease Resistance Gene RPS5 Partially Suppresses Multiple Bacterial and Downy Mildew Resistance Genes.
R. F. Warren, A. Henk, P. Mowery, E. Holub, and R. W. Innes (1998)
PLANT CELL 10, 1439-1452
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A cloned Erwinia chrysanthemi Hrp (type III protein secretion) system functions in Escherichia coli to deliver Pseudomonas syringae Avr signals to plant cells and to secrete Avr proteins in culture.
J. H. Ham, D. W. Bauer, D. E. Fouts, and A. Collmer (1998)
PNAS 95, 10206-10211
   Abstract »    Full Text »    PDF »
Genetically engineered broad-spectrum disease resistance in tomato.
G. E. D. Oldroyd and B. J. Staskawicz (1998)
PNAS 95, 10300-10305
   Abstract »    Full Text »    PDF »
Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis.
N. Aarts, M. Metz, E. Holub, B. J. Staskawicz, M. J. Daniels, and J. E. Parker (1998)
PNAS 95, 10306-10311
   Abstract »    Full Text »    PDF »
D-Subgenome Bias of Xcm Resistance Genes in Tetraploid Gossypium (Cotton) Suggests That Polyploid Formation Has Created Novel Avenues for Evolution.
R. J. Wright, P. M. Thaxton, K. M. El-Zik, and A. H. Paterson (1998)
Genetics 149, 1987-1996
   Abstract »    Full Text »    PDF »
The Root Knot Nematode Resistance Gene Mi from Tomato Is a Member of the Leucine Zipper, Nucleotide Binding, Leucine-Rich Repeat Family of Plant Genes.
S. B. Milligan, J. Bodeau, J. Yaghoobi, I. Kaloshian, P. Zabel, and V. M. Williamson (1998)
PLANT CELL 10, 1307-1320
   Abstract »    Full Text »
Biochemical Properties of Two Protein Kinases Involved in Disease Resistance Signaling in Tomato.
G. Sessa, M. D'Ascenzo, Y.-T. Loh, and G. B. Martin (1998)
J. Biol. Chem. 273, 15860-15865
   Abstract »    Full Text »    PDF »
Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants.
C. J. Hueck (1998)
Microbiol. Mol. Biol. Rev. 62, 379-433
   Abstract »    Full Text »    PDF »
Correlation between Binding Affinity and Necrosis-Inducing Activity of Mutant AVR9 Peptide Elicitors.
M. Kooman-Gersmann, R. Vogelsang, P. Vossen, H. W. van den Hooven, E. Mahé, G. Honée, and P. J.G.M. de Wit (1998)
Plant Physiology 117, 609-618
   Abstract »    Full Text »
Xa21D Encodes a Receptor-like Molecule with a Leucine-Rich Repeat Domain That Determines Race-Specific Recognition and Is Subject to Adaptive Evolution.
G.-L. Wang, D.-L. Ruan, W.-Y. Song, S. Sideris, L. Chen, L.-Y. Pi, S. Zhang, Z. Zhang, C. Fauquet, B. S. Gaut, et al. (1998)
PLANT CELL 10, 765-780
   Abstract »    Full Text »    PDF »
Erwinia amylovora Secretes DspE, a Pathogenicity Factor and Functional AvrE Homolog, through the Hrp (Type III Secretion) Pathway.
A. J. Bogdanove, D. W. Bauer, and S. V. Beer (1998)
J. Bacteriol. 180, 2244-2247
   Abstract »    Full Text »
Characterization of a 34-kDa soybean binding protein for the syringolide elicitors.
C. Ji, C. Boyd, D. Slaymaker, Y. Okinaka, Y. Takeuchi, S. L. Midland, J. J. Sims, E. Herman, and N. Keen (1998)
PNAS 95, 3306-3311
   Abstract »    Full Text »    PDF »
Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein.
S. D. Mills, A. Boland, M.-P. Sory, P. van der Smissen, C. Kerbourch, B. B. Finlay, and G. R. Cornelis (1997)
PNAS 94, 12638-12643
   Abstract »    Full Text »    PDF »
A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria.
W.-D. Hardt and J. E. Galan (1997)
PNAS 94, 9887-9892
   Abstract »    Full Text »    PDF »
Signal perception and transduction in plant defense responses..
Y Yang, J Shah, and D F Klessig (1997)
Genes & Dev. 11, 1621-1639
   PDF »
Signaling in Plant-Microbe Interactions.
B. Baker, P. Zambryski, B. Staskawicz, and S. P. Dinesh-Kumar (1997)
Science 276, 726-733
   Abstract »    Full Text »
Flagellin from an Incompatible Strain of Pseudomonas avenae Induces a Resistance Response in Cultured Rice Cells.
F.-S. Che, Y. Nakajima, N. Tanaka, M. Iwano, T. Yoshida, S. Takayama, I. Kadota, and A. Isogai (2000)
J. Biol. Chem. 275, 32347-32356
   Abstract »    Full Text »    PDF »
HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore invitro.
J. Lee, B. Klusener, G. Tsiamis, C. Stevens, C. Neyt, A. P. Tampakaki, N. J. Panopoulos, J. Noller, E. W. Weiler, G. R. Cornelis, et al. (2001)
PNAS 98, 289-294
   Abstract »    Full Text »    PDF »
The gene coding for the Hrp pilus structural protein is required for type III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato.
W. Wei, A. Plovanich-Jones, W.-L. Deng, Q.-L. Jin, A. Collmer, H.-C. Huang, and S. Y. He (2000)
PNAS 97, 2247-2252
   Abstract »    Full Text »    PDF »
The Cf-9 Disease Resistance Protein Is Present in an ~420-Kilodalton Heteromultimeric Membrane-Associated Complex at One Molecule per Complex.
S. Rivas, T. Romeis, and J. D. G. Jones (2002)
PLANT CELL 14, 689-702
   Abstract »    Full Text »    PDF »


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Science. ISSN 0036-8075 (print), 1095-9203 (online)