Abstract
The previous chapters have discussed how phytopathogenic bacteria can sense and respond to conditions present in a variety of microenvironments: soil, water, plant cell surfaces, and intracellular spaces. The switch from epiphyte to pathogen is apparently accompanied by fundamental reprogramming of gene activity and attendant function, as evidenced by induction of hrp genes and subsequent production of various virulence and pathogenicity factors, some of which are hostspecific, some not. This reprogramming switch between epiphytic and pathogenic growth strategies, “the pathogenic cusp” (DANGL 1994), is the point at which not only the potential pathogen but also the host first sense and respond to each other. A successful plant defense response should be based on surveillance and interdiction before the pathogen has a chance to establish production of the armory of factors which determine successful colonization of that host. It is incumbent on each potential plant host, then, to evolve mechanisms to recognize some factor, preferably one produced at this pathogenic cusp, and to base resistance strategies on early recognition. Thus, an evolutionary tug-of-war is begun: plants evolve to “recognize” a particular isolate of a particular pathogen; variants arise in the pathogen population which are no longer recognized; variants arise in the host population which recognize the new pathogen variant, and the familiar game is afoot. This scenario has apparently given rise to systems of plantpathogen interactions explained genetically by the now well established “gene-for-gene” hypothesis (reviewed in CRUTE 1985; DANGL 1992; ELLINGBOE 1981; FLOR 1971; GABRIEL and ROLFE 1990; KEEN 1990; KEEN and STASKAWICZ 1988) . During plantmicrobe interactions of this sort, the products, either direct or indirect, of pathogen avirulence (avr) genes trigger a successful host resistance reaction through the action of the product of a particular host resistance (R) gene. These interactions are thus allele-specific: each partner is defined only by the simultaneous presence of the other. The complexity of resistance loci defined genetically is astounding and the paucity of knowledge regarding their structure and function is beginning to be resolved, as evidenced by the recent cloning of the first plant resistance gene of this class (MARTIN et al. 1993) . In contrast, a plethora of avirulence genes from pseudomonads and xanthomonads have been cloned, as discussed in the remainder of this review.
Preview
Unable to display preview. Download preview PDF.
References
Barta TM, Kinscherf TG, Willis DK (1992) Regulation of tabtoxin production by the lemA gene of Pseudomonas syringae. J Bacteriol 174: 3011–3020
Bavage AD, Vivian A, Atherton GT, Taylor JD, Malik AN (1991) Molecular genetics of Psudomonas syringae isolates pathovars: plasmid involvement in cultivar-specific incompatibility. J Gen Microbiol 137: 2231–2239
Bonas U, Stall RE, Staskawicz BJ (1989) Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv vesicatoria. Mol Gen Genet 218: 127–136
Bonas U, Conrad-Struach J, Balbo I (1993) Resistance in tomato to Xanthomonas campestris pv. vesicatoria is determined by alleles of the pepper-specific avirulence gene avrBs3. Mol Gen Genet 238: 261–269
Boucher CA, Barberis PA, Arlat M (1988) Acridine orange selects for deletions of hrp genes in all races of Pseudomonas solanacearum. Mol Plant Microbe Interact 1: 282–288
Brown I, Mansfield JW, Irlam I, Conrads-Strauch J, Bonas U (1993) Ultrastructure of interactions between xanthomonas camepstris pv. vesicatoria and pepper, including immunocytochemical localization of extracellular polysaccharides and the AvrBs3 protein. Mol Plant Microbe Interact 6: 376–386
Canteros B, Minisavage G, Bonas U, Pring D, Stall RE (1992) A gene from Xanthomonas campestris pv. vesicatoria that determines avirulence in tomato is related to avrBs3. Mol Plant Microbe Interact 4: 628–632
Carney BF, Denny TP (1990) A cloned avirulence gene from Pseudomonas solanacearum determines incompatibility on Nicotiana tabacum at the host species level. J Bacteriol 172: 4836–4843
Crute I (1985) The genetic bases of relationships between microbial parasites and their hosts. In: Fraser R (ed) Mechanisms of resistance to plant diseases. Kluwer Academic, Boston, pp 80–142
Dangl JL (1992) The major histocompatibility complex a la carte: are there analogies to plant disease resistance genes on the menu? Plant J 2: 3–11
Dangl JL (1993a) Applications of Arabidopsis thaliana to outstanding issues in plant-pathogen interactions. Int Rev Cytol 144: 53–83
Dangl JL (1993b) The emergence of Arabidopsis thaliana as a model for plant-pathogen interactions. Adv Plant Pathol 10: 127–155
Dangl JL (1994) Genes involved in bacterial pathogenesis of plants. In: Singh US (ed) Advanced methods in plant pathology. Elsevier, Oxford (in press)
Dangl JL, Ritter C, Gibbon MJ, Wood JR, Mur LA J, Goss S, Mansfield JW, Taylor JD, Vivian A (1992) Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell 4: 1359–1369
De Feyter R, Gabriel DW (1991) At least six avirulence genes are clustered on a 90-kilobase plasmid in Xanthomonas campestris pv. malvacearum. Mol Plant Microbe Interact 4: 423–432
De Feyter R, Yang Y, Gabriel DW (1993) Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvavearum avr genes. Mol Plant Microbe Interact 6: 225–237
Debener T, Lehnackers H, Arnold M, Dangl JL (1991) Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate, Plant J 1: 289–302
Ellingboe AH (1981) Changing concepts in host-pathogen genetics. Annu Rev Phytopathol 19: 125–143
Faucher C, Camut S, Denarie J, Truchet G (1989) The nodH and nodQ host range genes of Rhizobium meliloti behave as avirulence gene in R. Leguminosarium and determine changes in the production of plant-specific extracellular signals. Mol Plant Microbe Interact 2: 291–300
Felley R, Rahme LG, Mindrinos MN, Frederick RD, Pisi A, Panapoulos NJ (1991) Genes and signals controlling the Pseudomonas syringae pv. phaseolicola-plant interaction. In: Hennecke H, Verma DPS (ed) Advances in molecular genetics of plant-microbe inter-actions. Kluwer Academic, Dordrecht, pp 45–52
Fillingham AJ, Wood J, Bevan JR, Crute IR, Mansfield JW, Taylor JD, Vivian A (1992) Avirulence genes from Pseudomonas syringae pathovars phaseolicola and pisi confer specificity towards both host and non-host species. Physiol Mol Plant Pathol 40: 1–15
Flor H (1956) The complementary genie systems in flax and flax rust. Adv Genet 8: 29–54
Flor H (1971) Current status of the gene-for-gene concept, Annu Rev Phytopathol 9: 275–296
Gabriel DW, Rolfe B (1990) Working models of specific recognition in plant-microbe interactions, Annu Rev Phytopathol 28: 365–3910
Heath MC (1991) The role of gene-for-gene interactions in the determination of host-species specificity. Phytopathology 81: 127–130
Herbers K, Conrads-Strauch J, Bonas U (1992) Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356: 172–174
Heu S, Hutcheson SW (1993) Nucleotide sequence and properties of the hrmA locus associated with the Pseudomonas syringae pv. syringae 61 hrp cluster. Mol Plant Microbe Interact 5: 553–564
Hopkins CM, White FF, Choi S-H, Guo A, Leach JE (1993) Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 5: 451–459
Hrabak EM, Willis DK (1992) The lemA gene required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators. J Bacteriol 174: 3011–3020
Hrabak EM, Willis DK 1993 ) Involvement of the lemA gene in production of syringomycin and protease by Pseudomonas syringae pv. syringae. Mol Plant-Microbe Interact 6: 368–375
Huang H-C, Hutcheson SW, Collmer A (1991) Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of genes encoding exported or membrane-spanning hrp proteins. Mol Plant Microbe Interact 4: 469–476
Huynh TV, Dahlbeck D, Staskawicz BJ (1989) Bacterial blight of soybean: regulation of pathogen gene determining host cultivar specificity. Science 245: 1374–1377
Innes RW, Bent AF, Kunkel BN, Bisgrove SR, Staskawicz BJ (1993a) Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J Bacteriol 175: 4859–4869
Innes RW, Bisgrove SR, Smith NM, Bent AF, Staskawicz BJ, Liu Y-C (1993b) Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant J 4: 813–820
Jenner C, Hitchin E, Mansfield JW, Walters K, Betteridge P, Teverson D, Taylor JD (1991) Gene-for-gene interactions between Pseudomonas syringae pv. phaseolicola and phaseolus. Mol Plant Microbe Interact 4: 553–562
Kearney B, Staskawicz BJ (1990) Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346: 385–386
Kearney B, Ronald PC, Dahlbeck D, Staskawicz BJ (1988) Molecular basis for evasion of plant host defence in bacterial spot disease of pepper. Nature 332: 541–543
Keen NT (1982) Specific recognition in gene-for-gene host-parasite systems, Adv Plant Pathol 2: 35–82
Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions, Annu Rev Genet 24: 447–463
Keen NT, Buzzell Rl (1991) New resistance genes in soybean against Pseudomonas syringae pv. glycinea: evidence that one of them interacts with a bacterial elicitor. Theor Appl Genet 81: 133–138
Keen NT, Staskawicz BJ (1988) Host range determinants in plant pathogens and symbionts. Annu Rev Microbiol 42: 421–440
Keen NT, Tamaki S, Kobayashi D, Gerhold D, Stayton M, Shen H, Gold S, Lorang J, Thordal-Christenson H, Dahlbeck D, Staskawicz BJ (1990) Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. Mol Plant Microbe Interact 3: 112–121
Kingsley MT, Gabriel DW, Marlow GC, Roberts PD (1993) The opsX locus of Xanthomonas campestris affects host range and the bioaynthesis of lipopolysaccharide and extra-cellular polysaccharide. J Bacteriol 175: 5839–5850
Knoop V, Staskawicz BJ, Bonas U (1991) Expression of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria is not under the control of hrp genes and is independent of plant factors. J Bacteriol 173: 7142–7150
Kobayashi DY, Tamaki SJ, Keen NT (1989) Cloned avirulence gene from the tomato pathogen Pseudomonas syringae pv. tomato cultivar specificity on soybean. Proc Natl Acad Sci USA 86: 157–161
Kobayashi DA, Tamaki SJ, Keen NT (1990a) Molecular characterization of avirulence gene D from Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 3: 94–102
Kobayashi DY, Tamaki SJ, Trollinger DJ, Gold S, Keen NT (1990b) A gene from Pseudomonas syringae pv. glycinea with homology to avirulence gene D from P.s pv. tomato but devoid of the avirulence phenotype. Mol Plant Microbe Intract 3: 103–111
Lorang JM, Keen NT (1994) Characterization of Psedomonas syringae pv. tomato avrE: a hrp-linked locus. Mol Plant Microbe Interact 7 (in press)
Lorang JM, Shen H, Kobayashi D, Keen NT (1994) The role of Pseudomonas syringae pv tomato avirulence genes in virulence and host range. Mol Plant Microbe Interact 7 (in press)
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432–1436
Midland SL, Keen NT, Sims JJ, Midland MM, Stayton MM, Burton V, Graham KJ, Clardy J (1993) The structures of Syringolides 1 and 2, noval C-Glcosidic elicitors from Pseudomonas syringae pv. tomato. J Org Chem 58: 2940–2945
Minisavage GV, Dahlbeck D, Whalen MC, Kearney B, Bonas U, Staskawicz BJ, Stall RE (1990) Gene-forgene relationships specifying disease resistance in Xanthomonas cam-pestris pv. Vesicatoriapepper interactions. Mol Plant Microbe Interact 3: 41–47
Moulton PJ, Vivian A, Hunter PJ, Taylor JD (1993) Changes in cultivar-specificity toward pea can result from transfer of plasmid RP4 and incompatibility group P1 replicons to Pseudomonas syringae pv. pisi. J Gen Microbiol 139 (in press)
Parker JE, Barber CE, Mi-jiao F, Daniels MJ (1993) Interaction of Xanthomonas campestris with Arabidopsis thaliana: characterization of a gene from X. campestris pathovar raphani which confers avirulence to most A. thaliana accessions. Mol Plant Microbe Interacts 6: 216–224
Rich JJ, Hirano SS, Willis DK (1992) Pathovar-specific requirement for the Pseudomonas syringae lemA gene in disease lesion formation. Appl Environ Microbiol 58: 1440–1446
Ritter C, Dangl JL (1994) The avrRpml gene of Pseudomonas syringae pv. maculicola is required for maximal virulence on Arabidopsis, (submitted)
Ronald PC, Staskawicz BJ (1988) The avirulence gene avrBsl from Xanthomonas campes-tris pv. vesicatoria encodes a 50-kD protein. Mol Plant Microbe Interact 1: 191–198
Ronald PC, Salmerón JM, Carland FM, Staskawicz BJ (1992) The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J Bacteriol 174: 1604–1611
Salmerón JM, Staskawicz BJ (1993) Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato. Mol Gen Genet 239: 6–16
Shen H, Keen NT (1993) Characterization of the promoter of avirulence gene D from Pseudomonas syringae pv. tomato. J Bacteriol 175: 5916–5924
Shintaku MH, Kluepfel DA, Yacoub A, Patil SS (1989) Cloning and partial characterization of an avirulence gene from race 1 of Pseudomonas syringae pv. phaseolicola. Physiol Mol Plant Pathol 35: 313–322
Smith MJ, Mazzola EP, Sims JJ, Midland SL, Keen NT, Burton V, Stayton MM (1993) The syringolides: bacterial C-glycosyl lipids that trigger plant disease resistance. Tetrahedron Lett 34: 223–226
Staskawicz BJ, Napoli C (1987) Molecular characterization and nucleic acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv. glycinea. J Bacteriol 169: 572–578
Staskawicz BJ, Dahlbeck D, Keen N (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc Natl Acad Sci USA 81: 6024–6028
Staskawicz BJ, Dahlbeck D, Keen NT, Napoli C (1987) Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J Bacteriol 169: 5789–5794
Swanson J, Kearney B, Dahlbeck D, Staskawicz BJ (1988) Cloned avirulence gene of Xanthomonas campestris pv. vesicatoria complements spontaneous race-change mutants. Mol Plant Microbe Interact 1: 5–9
Swarup S, De Feyter R, Brlansky RH, Gabriel DW (1991) A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of X. campestris to elicit canker-like lesions on citrus. Phytopathology 802–809
Swarup S, Yang Y, Kingsley MT, Gabriel DW (1992) An Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on nonhosts. Mol Plant Microbe Interact 5: 204–213
Tamaki S, Dahlbeck D, Staskawicz BJ, Keen NT (1988) Characterization and expression of two avirulence genes cloned from Pseudomonas syringae pv. glycinea. J Bacteriol 170: 4846–4854
Tamaki SJ, Kobayashi DY, Keen NT (1991) Sequence domains requried for the activity of avirulence genes avrB and avrC from Pseudomonas syringae pv. glycinea. J Bacteriol 173: 301–307
Tosa Y (1989) Evidence on wheat for gene-for-gene relationships between formae speciales of Erysiphe graminis and genera of gramineous plants.Genome 32: 918–924
Valent B, Farrau L, Chumley FG (1990) Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127: 87–101
Vivian A, Mansfield J (1993) A proposal for a uniform genetic nomenclature for avirulence genes in phytopathogenic Pseudomonads. Mol Plant-Microbe Interact 6: 9–11
Vivian A, Atherton GT, Bevan JR, Crute IR, Mur LAJ, Taylor JD (1989) Isolation and characterization of cloned DNA conferring specific avirulence in Pseudononas syringae pv. pisito pea (Pisum sativum) cultivars, which possess the resistance allele R2. Physiol Mol Plant Pathol 34: 335–344
Whalen MC, Stall RE, Staskawicz BJ (1988) Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc Natl Acad Sci USA 85: 6743–6747
Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both arabidopsis and soybean. Plant Cell 3: 49–59
Whalen MC, Wang JF, Carland FM, Heiskell MF, Dahlbeck D, Minisavage G. Jones JB, Scott JW, Stall RE, Staskawicz BJ (1993) Avirulence gene avrRxv from Xanthomonas campestris pv. Vesicatoria specifies resistance on tomato line Hawaii 7998. Mol Plant Microbe Interact 5: 616–627
Willis DK, Hrabak EM, Rich JJ, Barta TM, Lindow SE, Panapoulos NJ (1990) Isolation and characterization of a Pseudomonas syringae pv. syringae mutant deficient in lesion formation on bean. Mol Plant Microbe Interact 3: 149–156
Wood JR, Vivian A, Jenner C, Mansfield JW, Taylor JD (1994) Isolation and partial characterization of a plasmid-borne avirulence gene from Pseudomonas syringae pv. phaseolicola associated with nonhost recognition. Mol Plant Microbe Interact (in press)
Xiao, Y, Heu S, Yi J, Lu Y, Hutcheson SW (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol 176: 1025–1036
Yucel I, Keen NT (1994a) Amino acid residues required for the activity of avr alleles. Mol Plant Microbe Interact 7: 140–147
Yucel I, Boyd C, Debnam Q, Keen NT (1994a) Two different classes of avrD alleles occur in pathovars of Pseudomonas syringae. Mol Plant Microbe Interact 7: 131–139
Yucel I, Keen NT (1994b) New avirulence region from Pseudomonas syringae pv. phaseolicola closely linked to avrD confers cultivar specificity on soybean. Mol Plant Microbe Interact 7 (in press)
Yucel I, Midland SL, Sims JJ, Keen NT (1994b) Class I and II avrD alleles direct the production of different products in Gram negative bacteria. Mol Plant Microbe Interact 7: 148–150
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1994 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Dangl, J.L. (1994). The Enigmatic Avirulence Genes of Phytopathogenic Bacteria. In: Dangl, J.L. (eds) Bacterial Pathogenesis of Plants and Animals. Current Topics in Microbiology and Immunology, vol 192. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-78624-2_5
Download citation
DOI: https://doi.org/10.1007/978-3-642-78624-2_5
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-78626-6
Online ISBN: 978-3-642-78624-2
eBook Packages: Springer Book Archive