Genetic mapping of 14 avirulence genes in an EU-B04×1639 progeny of Venturia inaequalis

Fungal Genetics and Biology

Volumn 48, Issue 2, 2011, Pages 166-176

  Broggini, Giovanni A L ^a   Bus, Vincent G M ^b   Parravicini, Gabriella ^a   Kumar, Satish ^b   Groenwold, Remmelt ^c   Gessler, Cesare ^a  

^a ETH ZURICH   (Switzerland)

^b THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Apple scab; Avirulence gene; Gene for gene relationship; Genetic map; Resistance gene; Venturia inaequalis

Indexed keywords

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; APPLE SCAB; ARTICLE; AVIRULENCE GENE; AVRRVI2 GENE; AVRRVI8 GENE; AVRRVI9 GENE; AVRVDG2 GENE; AVRVH3.2 GENE; AVRVRJRD GENE; AVRVS1 GENE; AVRVSV GENE; AVRVT57 GENE; AVRVU1 GENE; AVRVU2 GENE; AVRVU4 GENE; AVRVV1 GENE; AVRVV2 GENE; EUROPE; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS; GENE; GENE CLUSTER; GENE INTERACTION; GENE MAPPING; GENETIC LINKAGE; INHERITANCE; MICROSATELLITE MARKER; NONHUMAN; PLANT FUNGUS INTERACTION; PRIORITY JOURNAL; PROGENY; VENTURIA INAEQUALIS;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ASCOMYCOTA; CHROMOSOME MAPPING; MALUS; MICROSATELLITE REPEATS; PLANT DISEASES; VIRULENCE; VIRULENCE FACTORS;

MALUS; MALUS BACCATA; MALUS MICROMALUS; MALUS X DOMESTICA; SPILOCAEA; VENTURIA INAEQUALIS;

EID: 78649920727     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.09.001     Document Type: Article

References (93)

1. Aderhold R. Die Fusicladien unserer Obstbäume I. Teil. Landwirtsch. Jahrberichte 1896, 29:875-914.
2. Aderhold R. Ein Beitrag zur Frage der Empfänglichkeit der Apfelsorten für Fusicladium dendriticum, Wallr. Fuck. und derem Beziehungen zum Wetter. Arbeiten Biol. Abt. Land- und Forstwirtschaft 1902, 2:560-566.
3. Ayliffe M.A., Dodds P.N., Lawrence G.J. Characterisation of a beta-tubulin gene from Melampsora lini and comparison of fungal beta-tubulin genes. Mycol. Res. 2001, 105:818-826.
4. Bagga H.S., Boone D.M. Genes in Venturia inaequalis controlling pathogenicity to crabapples. Phytopathology 1968, 58:1176-1182.
5. Bagga H.S., Boone D.M. Inheritance of resistance to Venturia inaequalis in crabapples. Phytopathology 1968, 58:1183-1187.
6. Barbara D.J., Roberts A.L., Xu X.M. Virulence characteristics of apple scab, Venturia inaequalis isolates from monoculture and mixed orchards. Plant Pathol. 2008, 57:552-561.
7. Belfanti E., Silfverberg-Dilworth E., Tartarini S., Patocchi A., Barbieri M., Zhu J., Vinatzer B.A., Gianfranceschi L., Gessler C., Sansavini S. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. 2004, 101:886-890.
8. Bénaouf G., Parisi L. Genetics of host-pathogen relationships between Venturia inaequalis races 6 and 7 and Malus species. Phytopathology 2000, 90:236-242.
9. Boone D.M. Genetics of Venturia inaequalis. Annu. Rev. Phytopathol. 1971, 9:297-318.
10. Boone D.M., Keitt G.W. Venturia inaequalis, Cke. Wint. VIII. Inheritance of color mutant characters. Am. J. Bot. 1956, 43:226-233.
11. Boone D.M., Keitt G.W. Venturia inaequalis, Cke. Wint. XII. Genes controlling pathogenicity of wild-type lines. Phytopathology 1957, 47:403-409.
12. Bowen J.K., Mesarich C.H., Rees-George J., Cui W., Fitzgerald A., Win J., Plummer K.M., Templeton M.D. Candidate effector gene identification in the ascomycete fungal phytopathogen Venturia inaequalis by expressed sequence tag analysis. Mol. Plant Pathol. 2009, 10:431-448.
13. Broggini G.A.L., Le Cam B., Parisi L., Wu C., Zhang H.B., Gessler C., Patocchi A. Construction of a contig of BAC clones spanning the region of the apple scab avirulence gene AvrVg. Fungal Genet. Biol. 2007, 44:44-51.
14. Broggini G.A.L., Galli P., Parravicini G., Gianfranceschi L., Gessler C., Patocchi A. HcrVf paralogs are present on linkage groups 1 and 6 of Malus. Genome 2009, 52:129-138.
15. Brun H., Chèvre A.-M., Fitt B.D.L., Powers S., Besnard A.-L., Ermel M., Huteau V., Marquer B., Eber F., Renard M., Andrivon D. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 2009, 185:285-299.
16. Bus V.G.M., Laurens F.N.D., van de Weg W.E., Rusholme R.L., Rikkerink E.H.A., Gardiner S.E., Bassett H.C.M., Kodde L.P., Plummer K.M. The Vh8 locus of a new gene-for-gene interaction between Venturia inaequalis and the wild apple Malus sieversii is closely linked to the Vh2 locus in Malus pumila R12740-7A. New Phytol. 2005, 166:1035-1049.
17. Bus V.G.M., Rikkerink E.H.A., van de Weg W.E., Rusholme R.L., Gardiner S.E., Bassett H.C.M., Kodde L.P., Parisi L., Laurens F., Meulenbroek E.J., Plummer K.M. The Vh2 and Vh4 scab resistance genes in two differential hosts derived from Russian apple R12740-7A map to the same linkage group of apple. Mol. Breed. 2005, 15:103-116.
18. Bus V., Rikkerink E., Aldwinckle H.S., Caffier V., Durel C.-E., Gardiner S., Gessler C., Groenwold R., Laurens F., Le Cam B., Luby J., Meulenbroek B., Kellerhals M., Parisi L., Patocchi A., Plummer K., Schouten H.J., Tartarini S., van de Weg E. A proposal for the nomenclature of Venturia inaequalis races. Acta Hort. 2009, 814:739-746.
19. Calenge F., Faure A., Goerre M., Gebhardt C., van de Weg W.E., Parisi L., Durel C.-E. Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 2004, 94:370-379.
20. Catanzariti A.-M., Dodds P.N., Lawrence G.J., Ayliffe M.A., Ellis J.G. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 2006, 18:243-256.
21. Chen Q.H., Wang Y.C., Zheng X.B. Genetic analysis and molecular mapping of the avirulence gene PRE1, a gene for host-species specificity in the blast fungus Magnaporthe grisea. Genome 2006, 49:873-881.
22. Chevalier M., Lespinasse Y., Renaudin S. A microscopic study of the different classes of symptoms coded by the Vf gene in apple for resistance to scab, Venturia inaequalis. Plant Pathol. 1991, 40:249-256.
23. Dangl J.L., Jones J.D.G. Plant pathogens and integrated defence responses to infection. Nature 2001, 411:826-833.
24. Day P.R., Boone D.M., Keitt G.W. Venturia inaequalis, Cke. Wint. 11. The chromosome number. Am. J. Bot. 1956, 43:835-838.
25. Dayton D.F., Williams E.B. Independent genes in Malus for resistance to Venturia inaequalis. Proc. Am. Soc. Hort. Sci. 1968, 92:89-94.
26. Dayton D.F., Shay J.R., Hough L.F. Apple scab resistance from R12740-7A, a Russian apple. Proc. Am. Soc. Hort. Sci. 1953, 62:334-340.
27. Dodds P.N., Lawrence G.J., Catanzariti A.-M., Teh T., Wang C.-I.A., Ayliffe M., Kobe B., Ellis J.G. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant cell 2004, 16:755-768.
28. Dodds P.N., Lawrence G.J., Catanzariti A.-M., Ayliffe M., Ellis J.G. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. 2006, 103:8888-8893.
29. Ellis J.G., Lawrence G.J., Luck J.E., Dodds P.N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 1999, 11:495-506.
30. Fitzgerald A.M., Mudge A.M., Gleave A.P., Plummer K.M. Agrobacterium and PEG-mediated transformation of the phytopathogen Venturia inaequalis. Mycol. Res. 2003, 107:803-810.
31. Fitzgerald A.M., Van Kan J.A.L., Plummer K.M. Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet. Biol. 2004, 41:963-971.
32. Flor H.H. The complementary genic systems in flax and flax rust. Adv. Genet. 1956, 8:29-54.
33. Flor H.H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 1971, 9:275-296.
34. Gardiner S.E., Bus V.G.M., Rusholme R.L., Chagné D., Rikkerink E.H.A. Apple. Genome Mapping and Molecular Breeding in Plants. Fruits and Nuts 2007, 1-62. Springer-Verlag, Berlin Heidelberg. C. Kole (Ed.).
35. Gessler C., Patocchi A., Sansavini S., Tartarini S., Gianfranceschi L. Venturia inaequalis resistance in apple. Crit. Rev. Plant Sci. 2006, 25:473-503.
36. Gladieux, P., Zhang, X.-G., Afoufa-Bastien, D., Valdebenito Sanhueza, R.-M., Sbaghi, M., Le Cam, B., 2008. On the origin and spread of the scab disease of apple: out of Central Asia. PLoS ONE, 3(1), e1455. doi:1410.1371/journal.pone.0001455.
37. Gladieux P., Zhang X.-G., Róldan-Ruiz I., Caffier V., Leroy T., Devaux M., Van Glabeke S., Coart E., Le Cam B. Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Mol. Ecol. 2010, 19:658-674.
38. Gladieux, P., Caffier, V., Devaux, M., Le Cam, B., in press. Host-specific differentiation among populations of Venturia inaequalis causing scab on apple, pyracantha and loquat. Fungal Genet. Biol. doi 10.1016/j.fgb.2009.12.007.
39. Guérin F., Franck P., Loiseau A., Devaux M., Le Cam B. Isolation of 21 new polymorphic microsatellite loci in the phytopathogenic fungus Venturia inaequalis. Mol. Ecol. Notes 2004, 4:268-270.
40. Hernández, C.D., 1990. La tavelure du pommier Venturia inaequalis, Cke. Wint.: étude du pouvoir pathogène des races 1 et 5 et essai de lutte raisonnée. PhD Thesis, University of Nantes, France.
41. Hernández C.F.D., Parisi L., Lespinasse Y. Heredabilidad del factor de avirulencia de una cepa de Venturia inaequalis, Cke. Wint. sobre el cultivar de manzano, Malus×domestica Borkh. Golden delicious. Rev. Mexic. Fitopat. 1994, 12:31-34.
42. Hogenhout S.A., van der Hoorn R.A.L., Terauchi R., Kamoun S. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant-Microbe Interact. 2009, 22:115-122.
43. Hulbert S., Pryor T., Hu G., Richter T., Drake J. Genetic fine structure of resistance loci. The Gene-for-Gene Relationship in Plant-Parasite Interactions 1997, 27-43. CAB International. E.B. Holub, J.J. Burdon, I.R. Crute (Eds.).
44. Johnson R. Practical breeding for durable resistance to rust diseases in self-pollinating cereals. Euphytica 1978, 27:529-540.
45. Johnson R. Classical plant breeding for durable resistance to diseases. J. Plant Pathol 2000, 82:3-7.
46. Julien J.B. Cytological studies of Venturia inaequalis. Can. J. Bot. 1958, 36:607-613.
47. Kang B.-C., Yeam I., Jahn M.Y. Genetics of plant virus resistance. Ann. Rev. Phytopathol. 2005, 43:581-621.
48. Kaye C., Milazzo J., Rozenfeld S., Lebrun M.-H., Tharreau D. The development of simple sequence repeat markers for Magnaporthe grisea and their integration into an established genetic linkage map. Fungal Genet. Biol. 2003, 40:207-214.
49. Keitt G.W., Langford M.H. Venturia inaequalis, Cke. Wint. I. A groundwork for genetic studies. Am. J. Bot. 1941, 28:805-820.
50. Keitt G.W., Langford M.H., Shay J.R. Venturia inaequalis, Cke. Wint. II. Genetic studies on pathogenicity and certain mutant characters. Am. J. Bot. 1943, 30:491-500.
51. Koch T., Kellerhals M., Gessler C. Virulence pattern of Venturia inaequalis field isolates and corresponding differential resistance in Malus×domestica. J. Phytopathol. 2000, 148:357-364.
52. Kucheryava N., Bowen J.K., Sutherland P.W., Conolly J.J., Mesarich C.H., Rikkerink E.H.A., Kemen E., Plummer K.M., Hahn M., Templeton M.D. Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane. Fungal Genet. Biol. 2008, 45:1329-1339.
53. Laurens F. Review of the current apple breeding programmes in the world: objectives for scion cultivar improvement. Acta Hort. 1999, 484:163-170.
54. Leach J.E., Cruz C.M.V., Bai J.F., Leung H. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 2001, 39:187-224.
55. Lespinasse Y. Breeding pome fruits with stable resistance to diseases. 3. Genes, resistance mechanisms, present work and prospects. IOBC wprs Bull. 1989, 12(6):100-115.
56. Liebhard R., Koller B., Gianfranceschi L., Gessler C. Creating a saturated reference map for the apple, Malus×domestica Borkh genome. Theor. Appl. Genet. 2003, 106:1497-1508.
57. Liebhard R., Koller B., Patocchi A., Kellerhals M., Pfammatter W., Jermini M., Gessler C. Mapping quantitative field resistance against apple scab in a 'Fiesta'×'Discovery' progeny. Phytopathology 2003, 93:493-501.
58. MacHardy W.E. Apple Scab Biology, Epidemiology and Management 1996, APS Press, St. Paul, Minnesota.
59. MacHardy W.E., Gadoury D.M., Gessler C. Parasitic and biological fitness of Venturia inaequalis: relationship to disease management strategies. Phytopathology 2001, 85:1036-1050.
60. Malnoy M., Xu M., Borejsza-Wysocka E., Korban S.S., Aldwinckle H.S. Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol. Plant-Microbe Interact. 2008, 21:448-458.
61. Nitta N., Farman M.L., Leaong S.A. Genome organization of Magnaporthe grisea: integration of genetic maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor. Appl. Genet. 1997, 95:20-32.
62. Palloix A., Ayme V., Moury B. Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol. 2009, 183:190-199.
63. Parisi L., Lespinasse Y. Pathogenicity of Venturia inaequalis strains of race 6 on apple clones, (Malus sp.). Plant Dis. 1996, 80:1179-1183.
64. Parisi L., Fouillet V., Schouten H.J., Groenwold R., Laurens F., Didelot F., Evans K., Fischer C., Gennari F., Kemp H., Lateur M., Patocchi A., Thissen J., Tsipouridis C. Variability of the pathogenicity of Venturia inaequalis in Europe. Acta Hort. 2004, 663:107-113.
65. Parlevliet J. Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 2002, 124:147-156.
66. Pedersen C., Rasmussen S.W., Giese H. A genetic map of Blumeria graminis based on functional genes, avirulence genes, and molecular markers. Fungal Genet. Biol. 2002, 35:235-246.
67. Pink D.A.C. Strategies using genes for non-durable disease resistance. Euphytica 2002, 124:227-236.
68. Sacristán S., García-Arenal F. The evolution of virulence and pathogenicity in plant pathogen populations. Mol. Plant Pathol. 2008, 9:369-384.
69. Schmidt M. Venturia inaequalis, Cooke. Aderhold. VIII. Weitere Untersuchungen zur Züchtung schorfwiderstandsfähiger Apfelsorten. Züchter 1938, 10:280-291.
70. Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 2000, 18:233-234.
71. Shay J.R., Hough L.F. Evaluation of apple scab resistance in selections of Malus. Am. J. Bot. 1952, 39:288-297.
72. Shay J.R., Williams E.B. Identification of three physiologic races of Venturia inaequalis. Phytopathology 1956, 46:190-193.
73. Sierotzki H., Gessler C. Genetic analysis of a cross of two Venturia inaequalis strains that differ in virulence. J. Phytopathol. 1998, 146:515-519.
74. Sierotzki H., Gessler C. Inheritance of virulence of Venturia inaequalis toward Malus×domestica cultivars. J. Phytopathol. 1998, 146:509-514.
75. Sierotzki H., Eggenschwiler M., Boillat O., Mcdermott J.M., Gessler C. Detection of variation in virulence toward susceptible apple cultivars in natural populations of Venturia inaequalis. Phytopathology 1994, 84:1005-1009.
76. Soufflet-Freslon V., Gianfranceschi L., Patocchi A., Durel C.-E. Inheritance studies of apple scab resistance and identification of Rvi14, a new major gene that acts together with other broad-spectrum QTL. Genome 2008, 51:657-667.
77. Sreewongchai T., Sriprakhon S., Wongsaprom C., Vanavichit A., Toojinda T., Tharreau D., Sirithunya P. Genetic mapping of Magnaporthe grisea avirulence gene corresponding to leaf and panicle blast resistant QTLs in Jao Hom Nin rice cultivar. J. Phytopathol. 2009, 157:338-343.
78. Stuthman D.D., Leonard K.J., Miller-Garvin J. Breeding crops for durable resistance to disease. Adv. Agron. 2007, 95:319-367.
79. Tenzer I., degli Ivanissevich S., Morgante M., Gessler C. Identification of microsatellite markers and their application to population genetics of Venturia inaequalis. Phytopathology 1999, 89:748-753.
80. van der Biezen E.A., Jones J.D.G. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 1998, 23:454-456.
81. van der Hoorn R.A.L., de Wit P.J.G.M., Joosten M.H.A.J. Balancing selection favors guarding resistance genes. Trends Plant Sci. 2002, 7:67-71.
82. van Ooijen J., Voorrips R. JoinMap® 3.0, Software for the Calculation of Genetic Linkage Maps 2001, Plant Research International, Wageningen, the Netherlands.
83. Vera Cruz C.M., Bai J., Ona I., Leung H., Nelson R.C., Mew T.W., Leach J.E. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl. Acad. Sci. 2000, 97:13500-13505.
84. Vinatzer B.A., Patocchi A., Gianfranceschi L., Tartarini S., Zhang H.B., Gessler C., Sansavini S. Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol. Plant-Microbe Interact. 2001, 14:508-515.
85. Visser T., Verhaegh J.J., de Vries D.P. Resistance to scab, Venturia inaequalis. and mildew, Podosphaera leucotricha. and fruiting properties of the offspring of the apple cultivar Antonovka. Euphytica 1974, 23:353-364.
86. Voorrips R.E. MapChart: software for the graphical presentation of linkage maps and QTLs. J. Hered. 2002, 93:77-78.
87. Wang S., Basten C.J., Zeng Z.B. Windows QTL Cartographer 2.5 2005, NCSU, Chapel Hill, NC.
88. Wang C.A., Gunčar G., Forwood J.K., Teh T., Catanzariti A.-M., Lawrence G.J., Loughlin F.E., Mackay J.P., Schirra H.J., Anderson P.A., Ellis J.G., Dodds P.N., Kobe B. Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 2007, 19:2898-2912.
89. Wiesman R. Untersuchungen über Apfel- und Birnschorfpilz Fusicladium dendriticum, Wallr. Fckl. und Fusicladium pirinum, Lib. Fckl. Landwirtsch. Jahrbuch Schweiz 1931, 35:109-156.
90. Williams E.B., Shay J.R. The relationship of genes for pathogenicity and certain other characters in Venturia inaequalis, Cke. Wint. Genet. 1957, 42:704-711.
91. Win J., Greenwood D., Plummer K. Characterisation of a protein from Venturia inaequalis that induces necrosis in Malus carrying the Vm resistance gene. Physiol. Mol. Plant Pathol. 2003, 62:193-202.
92. Xu M., Korban S.S. A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 2002, 162:1995-2006.
93. Xu X., Roberts T., Barbara D., Harvey N., Gao L., Sargent D. A genetic linkage map of Venturia inaequalis, the causal agent of apple scab. BMC Res. Notes 2009, 2:163.