Marker-Based Cloning of the Region Containing the UhAvr1 Avirulence Gene from the Basidiomycete Barley Pathogen Ustilago hordei

Genetics

Volumn 166, Issue 1, 2004, Pages 99-111

  Linning, R ^a   Lin, D ^d,f   Lee, N ^d   Abdennadher, M ^e,g   Gaudet, D ^a,b   Thomas, P ^a,c   Mills, D ^e   Kronstad, J W ^d   Bakkeren, G ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b LETHBRIDGE RESEARCH CENTRE   (Canada)

^c Cereal Research Centre   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e OREGON STATE UNIVERSITY   (United States)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g Monsanto Europe Africa   (Tunisia)

Author keywords

[No Author keywords available]

Indexed keywords

CONTIG; DNA; GENE PRODUCT; PROTEIN UHAVR1; UNCLASSIFIED DRUG;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; AVIRULENCE GENE; BACTERIAL ARTIFICIAL CHROMOSOME; BARLEY; BASIDIOMYCETES; BULKED SEGREGANT ANALYSIS; CONFORMATION; COSMID; COSMID CLONE; CULTIVAR; DNA LIBRARY; ECOLOGICAL SPECIALIZATION; GENE; GENE CONSTRUCT; GENE LOCATION; GENETIC ANALYSIS; GENETIC MARKER; HOST PATHOGEN INTERACTION; HYBRIDIZATION; MARKER BASED CLONING; MOLECULAR CLONING; NONHUMAN; PATHOLOGICAL ANATOMY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RACE; RANDOM AMPLIFIED POLYMORPHIC DNA; SEQUENCE ANALYSIS; UHAVR1 GENE; USTILAGO; USTILAGO HORDEI;

BASE SEQUENCE; CLONING, MOLECULAR; DNA, FUNGAL; GENE LIBRARY; GENES, FUNGAL; HORDEUM; LINKAGE (GENETICS); MULTIGENE FAMILY; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; RESTRICTION MAPPING; USTILAGO; VIRULENCE;

BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; FUNGI; HORDEUM VULGARE SUBSP. VULGARE; MYXOGASTRIA; USTILAGO HORDEI;

EID: 1642325154     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.166.1.99     Document Type: Article

References (80)

1. ARNAU, J., A. P. HOUSEGO and R. P. OLIVER, 1994 The use of RAPD markers in the genetic analysis of the plant pathogenic fungus Cladosporium fulvum. Curr. Genet. 25: 438-444.
2. ATTARD, A., L. GOUT, M. GOURGUES, M. L. KUHN, J. SCHMIT et al., 2002 Analysis of molecular markers genetically linked to the Leptosphaeria maculans avirulence gene AvrLm1 in field populations indicates a highly conserved event leading to virulence on Rlm1 genotypes. Mol. Plant-Microbe Interact. 15: 672-682.
3. AXTELL, M.J., and B.J. STASKAWICZ, 2003 Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
4. BACKLUND, J. E., and L. J. SZABO, 1993 Physical characteristics of the genome of the phytopathogenic fungus Puccinia graminis. Curr. Genet. 24: 89-93.
5. BAKKEREN, G., and J. W. KRONSTAD, 1993 Conservation of the b mating-type gene complex among bipolar and tetrapolar smut fungi. Plant Cell 5: 123-136.
6. BAKKEREN, G., B. GIBBARD, A. YEE, E. FROELIGER, S. LEONG et al., 1992 The a and b loci of Ustilago maydis hybridize with DNA sequences from other smut fungi. Mol. Plant-Microbe Interact. 5: 347-355.
7. BAKKEREN, G., J. W. KRONSTAD and C. A. LEVESQUE, 2000 Comparison of AFLP fingerprints and ITS sequences as phylogenetic markers in Ustilaginomycetes. Mycologia 92: 510-521.
8. COLLMER, A., 1998 Determinants of pathogenicity and avirulence in plant pathogenic bacteria. Curr. Opin. Plant Biol. 1: 329-335.
9. DANGL, J. L., and J. D. JONES, 2001 Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
10. DE WIT, P. J., 1992 Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annu. Rev. Phytopathol. 30: 391-418.
11. DIOH, W., D. THARREAU, J. L. NOTTEGHEM, M. ORBACH and M. H. LEBRUN, 2000 Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol. Plant-Microbe Interact. 13: 217-227.
12. DUTTA, S. K., 1974 Repeated DNA sequences in fungi. Nucleic Acids Res. 1: 1411-1419.
13. EBBA, T., and C. PERSON, 1975 Genetic control of virulence in Ustilago hordei. IV. Duplicate genes for virulence and genetic and environmental modification of a gene-for-gene relationship. Can. J. Genet. Cytol. 17: 631-636.
14. FARMAN, M. L., and S. A. LEONG, 1998 Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: discrepancy between the physical and genetic maps. Genetics 150: 1049-1058.
15. FARMAN, M. L., Y. ETO, T. NAKAO, Y. TOSA, H. NAKAYASHIKI et al., 2002 Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol. Plant-Microbe Interact. 15: 6-16.
16. FLOR, H. H., 1942 Inheritance of pathogenicity in Melampsora lini. Phytopathology 32: 653-669.
17. FLOR, H. H., 1971 Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9: 275-296.
18. FRIJTERS, A. C. J., Z. ZHANG, M. VAN DAMME, G. L. WANG, P. C. RONALD et al., 1997 Construction of a bacterial artificial chromosome library containing large EcoRI and HindIII genomic fragments of lettuce. Theor. Appl. Genet. 94: 390-399.
19. GIJZEN, M., H. FORSTER, M. D. COFFEY and B. TYLER, 1996 Cosegregation of Avr4 and Avr6 in Phytophthora sojae. Can. J. Bot. 74: 800-802.
20. HAMMOND KOSACK, K. E., and J. D. G. JONES, 1996 Resistance gene-dependent plant defense responses. Plant Cell 8: 1773-1791.
21. HEATH, M. C., 2000 Hypersensitive response-related death. Plant Mol. Biol. 44: 321-334.
22. HOLLIDAY, R., 1974 Ustilago maydis, pp. 575-595 in Handbook of Genetics, Vol. I, edited by R. C. KING. Plenum, New York.
23. HOLT, B. F., 3RD, D. MACKEY and J. L. DANOL, 2000 Recognition of pathogens by plants. Curr. Biol. 10: R5-R7.
24. HOLT, B. F., D. A. HUBERT and J. L. DANGL, 2003 Resistance gene signaling in plants-complex similarities to animal innate immunity. Curr. Opin. Immunol. 15: 20-25.
25. HU, G. G., R. LINNING and G. BAKKEREN, 2002 Sporidial mating and infection process of the smut fungus, Ustilago hordei, in susceptible barley. Can. J. Bot. 80: 1103-1114.
26. Hu, G. G., R. LINNING and G. BAKKEREN, 2003 Ultrastructural comparison of a compatible and incompatible interaction triggered by the presence of an avirulence gene during early infection of the smut fungus, Ustilago hordei, in barley. Physiol. Mol. Plant Pathol. 62: 155-166.
27. JI, C., J. SMITH-BECKER and N. T. KEEN, 1998 Genetics of plant-pathogen interactions. Curr. Opin. Biotechnol. 9: 202-207.
28. JIA, Y., S. A. MCADAMS, G. T. BRYAN, H. P. HERSHEY and B. VALENT, 2000 Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19: 4004-4014.
29. JOOSTEN, M. H., T. J. COZIJNSEN and P. J. DE WIT, 1994 Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367: 384-386.
30. KAMOUN, S., P. VAN WEST, V. G. VLEESHOUWERS, K. E. DE GROOT and F. GOVERS, 1998 Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INFI. Plant Cell 10: 1413-1425.
31. KEEN, N. T., 1990 Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24: 447-463.
32. KEEN, N., S. L. MIDLAND, C. BOYD, I. YUCEL, T. TSURUSHIMA et al., 1994 Syringolide elicitors specified by avirulence gene D alleles in Pseudomonas syringae, pp. 41-48 in Advances in Molecular Genetics of Plant Microbe Interactions, Vol. 3, edited by M. J. DANIELS, J. A. DOWNIE and A. E. OSBOURN. Kluwer Academic Publishers, Dordrecht, The Netherlands.
33. KNOGGE, W., 1996 Molecular basis of specificity in host/fungus interactions. Eur. J. Plant Pathol. 102: 807-816.
34. KNOGGE, W., 1998 Fungal pathogenicity. Curr. Opin. Plant Biol. 1: 324-328.
35. KNOGGE, W., 2002 Avirulence determinants and elicitors, pp. 289-310 in The Mycota, Vol. XI: Agricultural Applications, edited by F. KEMPKEN. Springer-Verlag, Berlin.
36. KORCH, C., 1987 Cross index for improving cloning selectivity by partially filling in 5′-extensions of DNA produced by type II restriction endonucleases. Nucleic Acids Res. 15: 3199-3220.
37. KRONSTAD, J. W., and S. A. LEONG, 1989 Isolation of two alleles of the b locus of Ustilago maydis. Proc. Natl. Acad. Sci. USA 86: 978-982.
38. LAM, E., N. KATO and M. LAWTON, 2001 Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848-853.
39. LAUGE, R., and P.J. DE WIT, 1998 Fungal avirulence genes: structure and possible functions. Fungal Genet. Biol. 24: 285-297.
40. LAUGE, R., M. H. JOOSTEN, G. F. J. M. VAN DEN ACKERVEKEN, H. W. J. V. D. BROEK and P. J. DE WIT, 1997 The in planta-produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors. Mol. Plant-Microbe Interact. 10: 725-734.
41. LAUGE, R., P. H. GOODWIN, P. J. DE WIT and M. H. JOOSTEN, 2000 Specific HR-associated recognition of secreted proteins from Cladosporium fulvum occurs in both host and non-host plants. Plant J. 23: 735-745.
42. LEE, N., G. BAKKEREN, K. WONG, J. E. SHERWOOD and J. W. KRONSTAD, 1999 The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc. Natl. Acad. Sci. USA 96: 15026-15031.
43. MACGREGOR, T., M. BHATTACHARYYA, B. TYLER, R. BHAT, A. F. SCHMITTHENNER et al., 2002 Genetic and physical mapping of Avr1a in Phytophthora sojae. Genetics 160: 949-959.
44. MACKEY, D., Y. BELKHADIR, J. M. ALONSO, J. R. ECKER and J. L. DANGL, 2003 Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
45. MENZIES, J. G., G. BAKKEREN, F. MATHESON, J. D. PROCUNIER and S. WOODS, 2003 Use of inter-simple sequence repeats and amplified fragment length polymorphisms to analyze genetic relationships among small grain-infecting species of Ustilago. Phytopathology 93: 167-175.
46. MENZIES, J. G., G. HAMILTON and F. MATHESON, 1996 Cereal smut survey, 1995. Can. Plant Dis. Surv. 76: 76.
47. MICHELMORE, R. W., I. PARAN and R. V. KESSELI, 1991 Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. USA 88: 9828-9832.
48. OORT, A. J. P., 1944 Onderzoekingen over stuifbrand 11. Overgevoeligheid van tarwe voor stuifbrand, Ustilago tritici. [Hypersensitiveness of wheat to loose smut.] Tijdschrift over plantenziekten 50: 73-106.
49. ORBACH, M. J., L. FARRALL, J. A. SWEIGARD, F. G. CHUMLEY and B. VALENT, 2000 A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12: 2019-2032.
50. PARAN, I., and R. W. MICHELMORE, 1993 Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor. Appl. Genet. 85: 985-993.
51. PEDERSEN, C., S. W. RASMUSSEN and H. GIESE, 2002 A genetic map of Blumeria graminis based on functional genes, avirulence genes, and molecular markers. Fungal Genet. Biol. 35: 235-246.
52. RANDALL, T. A., and H. S. JUDELSON, 1999 Construction of a bacterial artificial chromosome library of Phytophthora infestans and transformation of clones into P. infestans. Fungal Genet. Biol. 28: 160-170.
53. REHMANY, A. P., L. J. GRENVILLE, N. D. GUNN, R. L. ALLEN, Z. PANIWNVK et al., 2003 A genetic interval and physical contig spanning the Peronospora parasitica (At) avirulence gene locus ATR1Nd. Fungal Genet. Biol. 38: 33-42.
54. ROHE, M., A. GIERLICH, H. HERMANN, M. HAHN, B. SCHMIDT et al., 1995 The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J. 14: 4168-4177.
55. SAMBROOK, J., E. F. FRITSCH and T. MANIATIS, 1989 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. SHIZUYA, H., B. BIRREN, U. J. KIM, V. MANCINO, T. SLEPAK et al., 1992 Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc. Natl. Acad. Sci. USA 89: 8794-8797.
57. SIDHU, G., and C. PERSON, 1972 Genetic control of virulence in Ustilago hordei. II. Identification of genes for host resistance and demonstration of gene-for-gene relations. Can. J. Genet. Cytol. 14: 209-213.
58. STASKAWICZ, B. J., F. M. AUSUBEL, B. J. BAKER, J. G. ELLIS and J. D. JONES, 1995 Molecular genetics of plant disease resistance. Science 268: 661-667.
59. STASKAWICZ, B. J., M. B. MUDGETT, J. L. DANGL and J. E. GALAN, 2001 Common and contrasting themes of plant and animal diseases. Science 292: 2285-2289.
60. SWEIGARD J. A., A. M. CARROLL, S. KANG, L. FARRALL, F. G. CHUMLEY et al., 1995 Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7: 1221-1233.
61. TAPKE, V. F., 1945 New physiologic races of Ustilago hordei. Phytopathology 35: 970-976.
62. THOMAS, P. L., 1976 Interaction of virulence genes in Ustilago hordei. Can. J. Genet. Cytol. 18: 141-149.
63. THOMAS, P. L., 1989 Barley smuts in the Prairie Provinces of Canada, 1983-1988. Can. J. Plant Pathol. 11: 133-136.
64. THOMAS, P. L., W. K. KIM and N. K. HOWES, 1987 Independent inheritance of genes governing virulence and the production of a polypeptide in Ustilago hordei. J. Phytopathol. 120: 69-74.
65. ULLRICH, R. C., K. A. DROMS, J. D. DOYON and C. A. SPECHT, 1980 Characterization of DNA from the Basidiomycete Schizophyllum commune. Exp. Mycol. 4: 123-134.
66. VAN DEN ACKERVEKEN, G., and U. BONAS, 1997 Bacterial avirulence proteins as triggers of plant disease resistance. Trends Microbiol. 5: 394-398.
67. VAN DEN ACKERVEKEN, G. F., J. A. L. VAN KAN, M. H. JOOSTEN, J. M. MUISERS, H. M. VERBAKEL et al., 1993 Characterization of two putative pathogenicity genes of the fungal tomato pathogen Cladosporium fulvum. Mol. Plant-Microbe Interact. 6: 210-215.
68. VAN DER BIEZEN, E. A., and J. D. JONES, 1998 Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23: 454-456.
69. VAN DER HOORN, R. A., P. J. DE WIT and M. H. JOOSTEN, 2002 Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7: 67-71.
70. VAN DER LEE, T., A. TESTA, J. VAN'T KLOOSTER, G. VAN DEN BERGVELTHUIS and F. GOVERS, 2001 Chromosomal deletion in isolates of Phytophthora infestans correlates with virulence on R3, R10, and R11 potato lines. Mol. Plant-Microbe Interact. 14: 1444-1452.
71. VAN KAN, J. A. L., G. F. VAN DEN ACKERVEKEN and P. J. DE WIT, 1991 Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol. Plant-Microbe Interact. 4: 52-59.
72. VAN'T SLOT, K. A. E., and W. KNOGGE, 2002 A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Crit. Rev. Plant Sci. 21: 229-271.
73. VOS, P., R. HOGERS, M. BLEEKER, M. REIJANS, T. VAN DE LEE et al., 1995 AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23: 4407-4414.
74. WANG, J., D. W. HOLDEN and S. A. LEONG, 1988 Gene transfer system for the phytopathogenic fungus Ustilago maydis. Proc. Natl. Acad. Sci. USA 85: 865-869.
75. WHISSON, S. C., T. VAN DE LEE, G. J. BRYAN, R. WAUGH, F. GOVERS et al., 2001 Physical mapping across an avirulence locus of Phytophthora infestans using a highly representative, large-insert bacterial artificial chromosome library. Mol. Genet. Genomics 266: 289-295.
76. WHITE, F. F., B. YANG and L. B. JOHNSON, 2000 Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3: 291-298.
77. WILLIAMS, J. G., A. R. KUBELIK, K. J. LIVAK, J. A. RAFALSKI and S. V. TINGEY, 1990 DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 18: 6531-6535.
78. WING, R. A., H. B. ZHANG and S. D. TANKSLEY, 1994 Map-based cloning in crop plants. Tomato as a model system. I. Genetic and physical mapping of jointless. Mol. Gen. Genet. 242: 681-688.
79. WOLPERT, T. J., L. D. DUNKLE and L. M. CIUFFETTI, 2002 Host-selective toxins and avirulence determinants: What's in a name? Annu. Rev. Phytopathol. 40: 251-285.
80. ZAMBINO, P. J., A. R. KUBELIK and L. J. SZABO, 2000 Gene action and linkage of avirulence genes to DNA markers in the rust fungus Puccinia graminis. Phytopathology 90: 819-826.