Revision of the nomenclature of the differential host-pathogen interactions of venturia inaequalis and malus

Annual Review of Phytopathology

Volumn 49, Issue , 2011, Pages 391-413

  Bus, Vincent G M ^a   Rikkerink, Erik H A ^a   Caffier, Valérie ^b   Durel, Charles Eric ^b   Plummer, Kim M ^c  

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

^b CEMAGREF   (France)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Apple scab; Avirulence gene; Gene for gene relationship; Race isolate; Resistance gene

Indexed keywords

ASCOMYCETES; DISEASE RESISTANCE; FUNGAL GENE; GENETIC VARIABILITY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MALUS; MICROBIOLOGY; PATHOGENICITY; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; REVIEW;

ASCOMYCOTA; DISEASE RESISTANCE; GENES, FUNGAL; GENES, PLANT; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; MALUS; PHENOTYPE; PLANT DISEASES; PLANT IMMUNITY;

MALUS; MALUS X DOMESTICA; VENTURIA INAEQUALIS;

EID: 80051768939     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-072910-095339     Document Type: Review

References (153)

1. Aldwinckle H S, Gustafson H L, Lamb RC. 1976. Early determination of genotypes for apple scab resistance by forced flowering of test cross progenies. Euphytica 25:185-191
2. Bagga H S, Boone DM. 1968. Genes in Venturia inaequalis controlling pathogenicity to crabapples. Phytopathology 58:1176-1182
3. Bagga H S, BooneDM. 1968. Inheritance of resistance to Venturia inaequalis in crabapples. Phytopathology 58:1183-1187
4. Barbara D J, Roberts A L, Xu XM. 2008. Virulence characteristics of apple scab (Venturia inaequalis) isolates from monoculture and mixed orchards. Plant Pathol. 57:552-561 (Pubitemid 351691940)
5. Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, et al. 2004. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. USA 101:886-890 (Pubitemid 38121053)
6. Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signalling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7:391-399 (Pubitemid 38871612)
7. Benaouf G, Parisi L. 2000. Genetics of host-pathogen relationships between Venturia inaequalis races 6 and 7 and Malus species. Phytopathology 90:236-242 (Pubitemid 30124734)
8. Bengtsson M, Lindhard H, Grauslund J. 2000. Occurrence of races of Venturia inaequalis in apple scab race screening orchard in Denmark. IOBC/WPRS Bull. 23(12):225-229
9. Black W, Mastenbroek C, MillsW R, PetersonLC. 1953.A proposal for an international nomenclature of races of Phytophthora infestans and genes controlling immunity in Solanum demissum derivatives. Euphytica 2:173-179
10. Blaise P, Gessler C. 1994. Cultivar mixtures in apple orchards as a mean to control apple scaB Norweg. J. Agric. Sci. 17:105-112
11. Bolar J P, Norelli J L, Wong K W, Hayes C K, Harman G E, Aldwinckle HS. 2000. Expression of endochitinase from Trichoderma harzianum in transgenic apple increases resistance to apple scab and reduces vigor. Phytopathology 90:72-77. (Pubitemid 30028269)
12. Boone DM. 1971. Genetics of Venturia inaequalis. Annu. Rev. Phytopathol. 9:297-318.
13. Boone D M, Keitt GW. 1957. Venturia inaequalis (Cke.) Wint. XII. Genes controlling pathogenicity of wild-type lines. Phytopathology 47:403-9.
14. Boudichevskaia A, Flachowsky H, Peil A, Fischer C, Dunemann F. 2006. Development of a multiallelic SCAR marker for the scab resistance gene Vr1/Vh4/Vx from R12740-7A apple and its utility for molecular breeding. Tree Genet. Genomes 2:186-195 (Pubitemid 44327011)
15. Bowen J K, Mesarich C H, Bus VG M, Beresford R M, Plummer K M, Templeton MD. 2011. Venturia inaequalis: the causal agent of apple scab. Mol. Plant Pathol. 12:105-122
16. Bowen J K, Mesarich C H, Rees-George J, Cui W, Fitzgerald A, et al. 2009. Candidate effector gene identification in the ascomycete fungal phytopathogen Venturia inaequalis by expressed sequence tag analysis. Mol. Plant Pathol. 10:431-448
17. Broggini GA L, Bus VG M, Parrivicini G, Kumar S, Groenwold R, Gessler C. 2011. Genetic mapping of 14 avirulence genes in an EU-B04 1639 progeny of Venturia inaequalis. Fungal Genet. Biol. 48:166-176
18. Broggini GA L, Le Cam B, Parisi L, Wu C, Zhang H B, et al. 2007. Construction of a contig of BAC clones spanning the region of the apple scab avirulence gene AvrVg. Fungal Genet. Biol. 44:44-51. (Pubitemid 44960065)
19. Brun H, Chevre A M, Fitt BD L, Powers S, Besnard A L, et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185:285-299
20. BusVGM. 2006. Differential host-pathogen interactions of Venturia inaequalis and Malus. PhD thesis. Univ. Auckland, New Zealand. 158 pp.
21. Bus VG M, Bassett HC M, Bowatte D, Chagne D, Ranatunga C A, et al. 2010. Genome mapping of an apple scab, a powdery mildew and a woolly apple aphid resistance gene from open-pollinated mildew immune selection. Tree Genet. Genomes 6:477-487
22. Bus VG M, Laurens FN D, van deWeg W E, Rusholme R L, Rikkerink EH A, et al. 2005. 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. 166:1035-1049 (Pubitemid 40717699)
23. Bus V, Plummer K, Rikkerink E, Luby J. 2000. Evaluation of the pathogenicity of two scab isolates derived from the Vf-resistant apple cultivar 'Baujade'. IOBC wprs Bull. 23(12):231-237
24. Bus V, Ranatunga C, Gardiner S, Bassett H, Rikkerink E. 2000. Marker assisted selection for pest and disease resistance in the New Zealand apple breeding programme. Acta Hortic. 538:541-547
25. Bus V, Rikkerink E, Aldwinckle H S, Caffier V, Durel C E, et al. 2009. A proposal for the nomenclature of Venturia inaequalis races. Acta Hortic. 814:739-746
26. Bus VG M, Rikkerink EH A, van de Weg W E, Rusholme R L, Gardiner S E, et al. 2005. 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. 15:103-116 (Pubitemid 40374288)
27. Caffier V, Didelot F, Pumo B, Causeur D, Durel C E, Parisi L. 2010. Aggressiveness of eight Venturia inaequalis isolates virulent and avirulent to the major resistance gene Rvi6 on a non-Rvi6 apple cultivar. Plant Pathol. 59:1072-1080
28. Calenge F, Faure A, Goerre M, Gebhardt C, van deWeg W E, et al. 2004. 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 94:370-79 (Pubitemid 38398399)
29. Celton J-M, Christoffels A, Sargent D J, Xu X, Rees DJG. 2010. Genome-wide SNP identification by high-throughput sequencing and selective mapping allows sequence assembly positioning using a framework genetic linkage map. BMC Biol. 8:155.
30. Cheng F S, Weeden N F, Brown S K, Aldwinckle H S, Gardiner S E, Bus VG. 1998. Development of a DNA marker for Vm, a gene conferring resistance to apple scab. Genome 41:208-214 (Pubitemid 28370082)
31. Chevalier M, Lespinasse Y, Renaudin S. 1991. A microscopic study of the different classes of symptoms coded by the Vf gene in apple for resistance to scab (Venturia inaequalis). Plant Pathol. 40:249-256
32. Chevalier M, Parisi L. 2000. Expression of Golden Delicious resistance to race 7 of Venturia inaequalis. IOBC wprs Bull. 23(12):239-244
33. Dayton D F, Williams EB. 1968. Independent genes in Malus for resistance to Venturia inaequalis. Proc. Am. Soc. Hortic. Sci. 92:89-94.
34. Dayton D F, Williams EB. 1970. Additional allelic genes in Malus for scab resistance of two reaction types. Proc. Am. Soc. Hortic. Sci. 95:735-736
35. Dayton D F, Shay J R, Hough LF. 1953. Apple scab resistance from R12740-7A, a Russian apple. Proc. Am. Soc. Hortic. Sci. 62:334-340
36. Didelot F, Brun L, Parisi L. 2007. Effects of cultivar mixtures on scab control in apple orchards. Plant Pathol. 56:1014-1022 (Pubitemid 350076019)
37. Dodds P N, Lawrence G J, Ellis JG. 2001. Six amino acid changes confined to the leucine-rich repeat B-strand/B-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163-178 (Pubitemid 32177041)
38. Dunemann F, Egerer J. 2010. A major resistance gene from Russian apple 'Antonovka' conferring field immunity against apple scab is closely linked to the Vf locus. Tree Genet. Genomes 6:627-633
39. Durel C E, Freslon V, Denance C, Laurens F, Lespinasse Y, et al. 2006. Genetic localisation of new major and minor pest and disease resistance factors in the apple genome. 3rd Int. Rosaceae Genomics Conf., 19-22 March 2006, Napier, New Zealand, p. 5 (Abstr.).
40. Durel C E, Parisi L, Laurens F, van de WegW E, Liebhard R, Jourjon MF. 2003. Genetic dissection of partial resistance to race 6 of Venturia inaequalis in apple. Genome 46:224-234 (Pubitemid 36610676)
41. Durel C E, van deWeg E, Venisse J S, Parisi L. 2000. Localisation of a major gene for scab resistance on the European genetic map of the Prima x Fiesta cross. IOBC wprs Bull. 23(12):245-248
42. Erdin N, Tartarini S, Broggini GA L, Gennari F, Sansavini S, et al. 2006. Mapping of the apple scabresistance gene Vb. Genome 49:1238-1245
43. Fitzgerald A, Mudge A M, Gleave A P, Plummer KM. 2003. Agrobacterium and PEG-mediated transformation of the phytopathogen Venturia inaequalis. Mycol. Res. 7:803-810 (Pubitemid 37029466)
44. Fitzgerald A, van Kan JA L, Plummer KM. 2004. Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet. Biol. 41:963-971 (Pubitemid 39165641)
45. Flor HH. 1971. Current status of the gene-for-gene concept. Ann. Rev. Phytopathol. 9:275-296
46. Galli P, Broggini GA L, Gessler C, Patocchi A. 2010. Phenotypic characterization of the Rvi15 (Vr2) apple scab resistance. J. Plant Pathol. 92:219-226
47. Galli P, Broggini GA L, Kellerhals M, Gessler C, Patocchi A. 2010. High-resolution genetic map of the Rvi15 (Vr2) apple scab resistance locus. Mol. Breed. 26:561-572
48. Galli P, Patocchi A, Broggini GA L, Gessler C. 2010. The Rvi15 (Vr2) apple scab resistance locus contains three TIR-NBS-LRR genes. Mol. Plant-Microbe Interact. 23:608-617
49. Gao Z, van de Weg W. 2006. The Vf gene for scab resistance in apple is linked to sub-lethal genes. Euphytica 151:123-133
50. Gardiner S E, Bassett HC M, Noiton DA M, Bus V G, Hofstee M E, et al. 1996. A detailed linkage map around an apple scab resistance gene demonstrates that two disease resistance classes both carry the Vf gene. Theor. Appl. Genet. 93:485-493 (Pubitemid 26351046)
51. Gessler C, Patocchi A, Sansavini S, Tartarini S, Gianfranceschi L. 2006. Venturia inaequalis resistance in apple. Crit. Rev. Plant Sci. 25:473-503. (Pubitemid 46015979)
52. Gilissen LJW J, Bolhaar STH P, Matos C I, Rouwendal GJ A, Boone M J, et al. 2005. Silencing the major apple allergen Mal d 1 by using the RNA interference approach. J. Allergy Clin. Immunol. 115:364-369 (Pubitemid 40215104)
53. Gladieux P, Caffier V, Le Cam B. 2010. Host-specific differentiation among populations of Venturia inaequalis causing scab on apple, pyrcantha and loquat. Fungal Genet. Biol. 47:511-522
54. 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.
55. Gladieux P, Zhang X G, Roldan-Ruiz I, Caffier V, Leroy T, et al. 2010. Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Mol. Ecol. 19:658-674
56. Guerin F, Franck P, Loiseau A, Devaux M, Le Cam B. 2004. Isolation of 21 new polymorphic microsatellite loci in the phytopathogenic fungus Venturia inaequalis. Mol. Ecol. Notes 4:268-270 (Pubitemid 38689005)
57. Guerin F, Gladieux P, Le Cam B. 2007. Origin and colonization history of newly virulent strains of the phytopathogenic fungus Venturia inaequalis. Fungal Genet. Biol. 44:284-292 (Pubitemid 46343704)
58. Gygax M, Gianfranceschi L, Liebhard R, Kellerhals M, Gessler C, Patocchi A. 2004. Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor. Appl.Genet. 109:1702-9. (Pubitemid 40024936)
59. Hemmat M, Brown S K, Aldwinckle H S, Mehlenbacher S A, Weeden NF. 2003. Identification and mapping of markers for resistance to apple scab from 'Antonovka' and 'Hansen's baccata #2'. Acta Hortic. 622:153-161
60. Hemmat M, Brown S K, Weeden NF. 2002. Tagging and mapping scab resistance genes from R12740-7A apple. J. Am. Soc. Hortic. Sci. 127:365-370 (Pubitemid 34294478)
61. Hemmat M, Weeden N F, Brown SK. 2003. Mapping and evaluation of Malus x domestica microsatellites in apple and pear. J. Am. Soc. Hortic. Sci. 128:515-520 (Pubitemid 36684893)
62. Hernandez CD. 1990. La tavelure du pommier Venturia inaequalis (Cke.) Wint.: etude du pouvoir pathog̀ene des races 1 et 5 et essai de lutte raisonnee. PhD thesis. Univ. Nantes, France. 163 pp.
63. Hernandez CF D, Parisi L, Lespinasse Y. 1994. Heredabilidad de la resistencia del hibrido de manzano X 2045 a Venturia inaequalis (Cke.) Wint. Rev. Mexic. Fitopatol. 12:27-29.
64. Hough LF. 1944. A survey of the scab resistance of the foliage on seedlings in selected apple progenies. Proc. Am. Soc. Hortic. Sci. 44:260-272
65. Hough L F, Shay J R, Dayton DF. 1953. Apple scab resistance from Malus floribunda Sieb. Proc. Am. Soc. Hortic. Sci. 62:341-347
66. Huang L, Brooks S, Li W, Fellers J, Nelson J C, Gill B. 2009. Evolution of new disease specificity at a simple resistance locus in a crop-weed complex: reconstitution of the Lr21 gene in wheat. Genetics 182:595-602.
67. Hulbert S H, Webb C A, Smith S M, Sun Q. 2001. Resistance gene complexes: evolution and utilization. Ann. Rev. Phytopathol. 39:285-312. (Pubitemid 32965187)
68. James D J, Passey A J, Barbara D J, BevanMJ. 1989. Genetic transformation of apple (Malus pumila Mill.) using disarmed Ti-binary vector. Plant Cell Rep. 7:658-661
69. Jefferson RM. 1970. History, Progeny, and Location of Crabapples of Documented Authentic Origin. Washington, DC: U.S. Dep. Agric. 107 pp.
70. Jones JD G, Dangl JF. 2006. The plant immune system. Nature 444:323-329 (Pubitemid 44764102)
71. JoostenMHA J, Cozijnsen T J, deWit PJGM. 1994. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367:384-386 (Pubitemid 24062348)
72. Julien J B, Spangelo LPS. 1957. Physiological races of Venturia inaequalis. Can. J. Plant Sci. 37:102-7.
73. Juniper B E, Watkins R, Harris SA. 1999. The origin of the apple. Acta Hortic. 484:27-33.
74. Keitt G W, Palmiter DH. 1938. Heterothallism and variability in Venturia inaequalis. Am. J. Bot. 25:338-45.
75. Kellerhals M, Fouillet A, Lespinasse Y. 1993. Effect of the scab inoculum and the susceptible parent on the resistance to apple scab (Venturia inaequalis) in the progenies of crosses to the scab resistant cv 'Florina'. Agronomie 13:631-636 (Pubitemid 2027746)
76. Korban S S, Chen H. 1992. Apple. In Biotechnology of Perennial Fruit Crops, ed. FA Hammerschlag, RE Litz, pp. 203-27. Wallingford, UK: CABI.
77. Korban S S, Skirvin RM. 1984. Nomenclature of the cultivated apple. HortScience 19:177-180
78. Kucheryava N, Bowen J K, Sutherland P W, Conolly J J, Mesarich C H, et al. 2008. Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane. Fungal Genet. Biol. 45:1329-1339
79. Lamb R C, Hamilton JM. 1969. Environmental and genetic factors influencing the expression of resistance to scab (Venturia inaequalis Cke. Wint.) in apple progenies. J. Am. Soc. Hortic. Sci. 94:554-557
80. Laurens F, Chevalier M, Dolega E, Gennari F, Goerre M, et al. 2004. Local European cultivars as sources of durable scab resistance in apple. Acta Hortic. 663:115-121
81. Le Cam B, Parisi L, Arene L. 2002. Evidence of two formae speciales in Venturia inaequalis, responsible for apple and pyracantha scab. Phytopathology 92:314-320 (Pubitemid 34212836)
82. Leach J E, Vera Cruz C M, Bai J, Leung H. 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Ann. Rev. Phytopathol. 39:187-224. (Pubitemid 32965184)
83. Lespinasse Y. 1989. Breeding pome fruits with stable resistance to diseases. 3. Genes, resistance mechanisms, present work and prospects. IOBC wprs Bull. 12(6):100-115
84. Lespinasse Y. 1994. Apple scab resistance and durability. New races and strategies for the future. In Progress in Temperate Fruit Breeding, ed. H Schmidt, M Kellerhals, pp. 105-106. Dordrecht, The Netherlands: Kluwer Acad. Publ.
85. Lespinasse Y, Olivier J M, Godicheau M. 1979. E tudes enterprises dans le cadre de la resistance à la tavelure du pommier. Proc. Tree Fruit Breed. Symp. Eucarpia Fruit Sect. Angers, pp. 97-110. Angers: INRA.
86. Liebhard R, Gianfranceschi L, Koller B, Ryder C D, Tarchini R, et al. 2002. Development and characterisation of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol. Breed. 10:217-241 (Pubitemid 35326063)
87. Liebhard R, Koller B, Patocchi A, Kellerhals M, Pfammatter W, et al. 2003. Mapping quantitative field resistance against apple scab in a 'Fiesta' x 'Discovery' progeny. Phytopathology 93:493-501. (Pubitemid 36352454)
88. Luby J, Forsline P, Aldwinckle H, Bus V, Geibel M. 2001. Silk road apples: collection, evaluation, and utilization of Malus sieversii from Central Asia. HortScience 36:225-231 (Pubitemid 32333395)
89. Mabberley D J, Jarvis C E, Juniper BE. 2001. The name of the apple. Telopea 9:421-430
90. MacHardy WE. 1996. Apple Scab: Biology, Epidemiology, and Management. St. Paul, MN: APS Press. 545 pp.
91. Maliepaard C, Alston F H, van Arkel G, Brown L M, Chevreau E, et al. 1998. Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor. Appl. Genet. 97:60-73. (Pubitemid 28371665)
92. Malnoy M, Boresjza-Wysocka E E, Norelli J L, Flaishman M A, Gidoni D, AldwinckleHS. 2010. Genetic transformation of apple (Malus x domestica) without use of a selectable marker gene. Tree Genet. Genomes 6:423-433
93. Malnoy M, Xu M, Borejsza-Wysocka E, Korban S S, Aldwinckle HS. 2008. Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol. Plant-Microbe Interact. 21:448-458 (Pubitemid 351521755)
94. Manganaris A G, Alston F H, Weeden N F, Aldwinckle H S, Gustafson H L, Brown SK. 1994. Isozyme locus Pgm-1 is tightly linked to a gene (Vf) for scab resistance in apple. J. Am. Soc.Hortic. Sci. 119:1286-1288
95. Maor R, Shirasu K. 2005. The arms race continues: battle strategies between plants and fungal pathogens. Curr. Opin. Microbiol. 8:399-404. (Pubitemid 41024940)
96. Mattison H, Nybom H. 2005. Application ofDNA markers for detection of scab resistant apple cultivars and selections. Int. J. Hortic. Sci. 11(3):59-63.
97. McCrory S A, Shay JR. 1951. Apple scab resistance survey of South Dakota apple varieties and breeding stocks. Plant Dis. Rep. 35:433-434
98. Meinke D, Koornneef M. 1997. Community standards for Arabidopsis genetics. Plant J. 12:247-253 (Pubitemid 27389615)
99. Mundt CC. 1990. Probability of mutation to multiple virulence and durability of resistance gene pyramids. Phytopathology 80:221-223
100. N'Diaye A, van de Weg W E, Kodde L P, Koller B, Dunemann F, et al. 2008. Construction of an integrated consensus map of the apple genome based on four mapping populations. Tree Genet. Genom. 4:727-743
101. Olivier J M, Lespinasse Y. 1982. Resistance du pommier ̀a la tavelure Venturia inaequalis (Cke.) Wint.: sources de resistance, comportement du parasite, programme de selection. Cryptogamie, Mycologie 3:361-75.
102. Palloix A, Ayme V, Moury B. 2009. Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol. 183:190-199
103. Paris R, Cova V, Pagliarani G, Tartarini S, Komjanc M, Sansavini S. 2009. Expression profiling in HcrVf2-transformed apple plants in response to Venturia inaequalis. Tree Genet. Genom. 5:81-91.
104. Parisi L, Fouillet V, Schouten H J, Groenwold R, Laurens F, et al. 2004. Variability of the pathogenicity of Venturia inaequalis in Europe. Acta Hortic. 663:107-113
105. Parisi L, Lespinasse Y. 1996. Pathogenicity of Venturia inaequalis strains of race 6 on apple clones (Malus sp.). Plant Dis. 80:1179-1183
106. Parisi L, Lespinasse Y, Guillaumes J, Kruger J. 1993. A new race of Venturia inaequalis virulent to apples with resistance due to Vf gene. Phytopathology 83:533-537
107. Patocchi A, Bigler, B, Koller B, Kellerhals M, Gessler C. 2004. Vr2: a new apple scab resistance gene. Theor. Appl. Genet. 109:1087-1092 (Pubitemid 39348251)
108. Patocchi A, Frei A, Frey J E, Kellerhals M. 2009. Towards improvement of marker assisted selection of apple scab resistant cultivars: Venturia inaequalis virulence surveys and standardization of molecular marker alleles associated with resistance genes. Mol. Breed. 24:337-347
109. Patocchi A, Walser M, Tartarini S, Broggini GA L, Gennari F, et al. 2005. Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48:630-636 (Pubitemid 41483422)
110. Poland J A, Balint-Kurti P J, Wisser R J, Pratt R C, Nelson RJ. 2009. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 14:21-29.
111. Raabe R D, Gardner MW. 1972. Scab of pyracantha, loquat, toyon, and kageneckia. Phytopathology 62:914-916
112. Rousselle G L, Williams E B, Hough LF. 1974. Modification of the level of resistance to apple scab from the Vf gene. Proc. 19th Int. Hortic. Congress, Vol. 3, pp. 19-26. Warsaw: ISHS.
113. Sandskar B, Liljeroth E. 2005. Incidence of races of the apple scab pathogen (Venturia inaequalis) in apple growing districts in Sweden. Acta Agric. Scand. Section B Soil Plant Sci. 55:143-150 (Pubitemid 43138345)
114. Sapoukhina N, Durel C E, Le Cam B. 2009. Spatial deployment of gene-for-gene resistance governs evolution and spread of pathogen populations. Theor. Ecol. 2:229-238
115. Schmidt M. 1938. Venturia inaequalis (Cooke) aderhold. VIII. Weitere Untersuchungen zur Zuchtung schorfwiderstandsfahiger Apfelsorten. Z̈uchter 10:280-291
116. Schnabel G, Schnabel E L, Jones AL. 1999. Characterization of ribosomal DNA from Venturia inaequalis and its phylogenetic relationship to rDNAfrom other tree-fruit Venturia species. Phytopathology 89:100-8. (Pubitemid 29032022)
117. Schouten H, Krens F A, Jacobsen E. 2006. Cisgenic plants are similar to traditionally bred plants. EMBO Rep. 7:750-753
118. Servin B, Martin O C, Mezard M, Hospital F. 2004. Toward a theory ofmarker-assisted gene pyramiding. Genetics 168:513-553
119. Shay J R, Dayton D F, Hough LF. 1953. Apple scab resistance from a number of Malus species. Proc. Am. Soc. Hortic. Sci. 62:348-356
120. Shay J R, Hough LF. 1952. Evaluation of apple scab resistance in selections of Malus.Am. J. Bot. 39:288-97.
121. Shay J R, Williams EB. 1953. Physiologic specialization in Venturia inaequalis. Phytopathology 43:483-84 (Abstr.).
122. Shay J R, WilliamsEB. 1956. Identification of three physiologic races of Venturia inaequalis. Phytopathology 46:190-193
123. Shay J R, Williams E B, Janick J. 1962. Disease resistance in apple and pear. Proc. Am. Soc. Hortic. Sci. 80:97-104.
124. Sierotzki H, Gessler C. 1998. Inheritance of virulence of Venturia inaequalis toward Malus x domestica cultivars. J. Phytopathol. 146:509-514 (Pubitemid 129536277)
125. Sierotzki H, Gessler C. 1998. Genetic analysis of a cross of two Venturia inaequalis strains that differ in virulence. J. Phytopathol. 146:515-519 (Pubitemid 129536278)
126. Sierotzki H, Eggenschwiler M, Boillat O, McDermott J M, Gessler C. 1994. Detection of variation in virulence toward susceptible apple cultivars in natural populations of Venturia inaequalis. Phytopathology 84:1005-9.
127. Silfverberg-Dilworth E, Besse S, Paris R, Belfanti E, Tartarini S, et al. 2005. Identification of functional apple scab resistance gene promoters. Theor. Appl. Genet. 110:1119-1126 (Pubitemid 40607579)
128. Soriano J M, Joshi S G, vanKaauwen M, Noordijk Y, Groenwold R, et al. 2009. Identification and mapping of the novel apple scab resistance gene Vd3. Tree Genet. Genom. 5:475-482
129. Soufflet-Freslon V, Gianfranceschi L, Patocchi A, Durel CE. 2008. Inheritance studies of apple scab resistance and identification of Rvi14, a new major gene that acts together with other broad-spectrum QTL. Genome 51:657-667
130. Spangelo LP S, Julien J B, Racicot H N, Blair DS. 1956. Breeding apples for resistance to scab. Can. J. Agric. Sci. 36:329-338
131. Stukenbrock E H, McDonald BA. 2008. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46:75-100.
132. Tartarini S, Gennari F, Pratesi D, Palazetti C, Sansavini S, et al. 2004. Characterisation and genetic mapping of a major scab resistance gene from the old Italian apple cultivar 'Durello di Forl̀?'. Acta Hortic. 663:129-133
133. Tellier A, Brown JKM. 2007. Polymorphism in multilocus host-parasite coevolutionary interactions. Genetics 177:1777-1790 (Pubitemid 350277070)
134. Tenzer I, Gessler C. 1997. Subdivision and genetic structure of four populations of Venturia inaequalis in Switzerland. Eur. J. Plant Pathol. 103:565-571 (Pubitemid 27378320)
135. Tenzer I, Gessler C. 1999. Genetic diversity of Venturia inaequalis across Europe. Eur. J. Plant Pathol. 105:545-552 (Pubitemid 29506592)
136. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, et al. 2010. The genome of the domesticated apple (Malus x domestica Borkh.). Nat. Genet. 42:833-839
137. Vinatzer B A, Patocchi A, Gianfranceschi L, Tartarini S, Zhang H B, et al. 2001. Apple contains receptorlike 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. 14:508-515 (Pubitemid 32241272)
138. Vinatzer B A, Patocchi A, Tartarini S, Gianfranceschi L, Sansavini S, Gessler C. 2004. Isolation of two microsatellite markers from BAC clones of the Vf scab resistance region and molecular characterization of scab-resistant accessions in Malus germplasm. Mol. Breed. 123:1-6.
139. Volz R, Rikkerink E, Austin P, Lawrence T, De Silva N, Bus V. 2009. "Fast-breeding" in apple: a strategy to accelerate introgression of new traits into elite germplasm. Acta Hortic. 814:163-168
140. Way R D, Aldwinckle H S, Lamb R C, Rejman A, Sansavini S, et al. 1989. Apples (Malus). Acta Hortic. 290:1-62.
141. Westerink N, Joosten MHA J, de Wit PJGM. 2004. Fungal (a)virulence factors at the crossroads of disease susceptibility and resistance. In Fungal Disease Resistance in Plants, ed. ZK Punja, pp. 93-137. New York, NY: Haworth Press.
142. Williams E B, Brown AG. 1968. A new physiologic race of Venturia inaequalis, incitant of apple scab. Plant Dis. Rep. 52:799-801.
143. Williams E B, Dayton DF. 1968. Four additional sources of the Vf locus for Malus scab resistance. Proc. Am. Soc. Hortic. Sci. 92:95-98.
144. Williams E B, Dayton D F, Shay JR. 1966. Allelic genes in Malus for resistance to Venturia inaequalis. Proc. Am. Soc. Hortic. Sci. 88:52-56.
145. Williams E B, Kuc J. 1969. Resistance in Malus to Venturia inaequalis. Ann. Rev. Phytopathol. 7:223-246
146. Williams E B, Shay JR. 1957. The relationship of genes for pathogenicity and certain other characters in Venturia inaequalis (Cke.) Wint. Genetics 42:704-711
147. Win J, Greenwood D R, Plummer KM. 2003. Characterisation of a protein from Venturia inaequalis that induces necrosis in Malus carrying the Vm resistance gene. Physiol. Mol. Plant Pathol. 62:193-202. (Pubitemid 37089966)
148. Win J, Morgan W, Bos J, Krasileva K V, Cano L M, et al. 2007. Adaptive evolution has targeted the C-terminal domain of RXLR effectors of plant pathogenic oomycetes. Plant Cell 19:2349-2369 (Pubitemid 47583830)
149. Xu M, Korban SS. 2002.Acluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 162:1995-2006. (Pubitemid 36114679)
150. Xu X M, Roberts T, Barbara D J, Harvey N G, Gao L, Sargent DJ. 2009. A genetic linkage map of Venturia inaequalis, the causal agent of apple scab. BMC Res. Notes 2:163.
151. Xu X M, Yang J R, Thakur V, Roberts A, Barbara DJ. 2008. Population variation of apple scab (Venturia inaequalis) isolates from Asia and Europe. Plant Disease 92:247-252
152. Yao J L, Cohen D, Atkinson R, Richardson K, Morris B. 1995. Regeneration of transgenic plants from the commercial apple cultivar Royal Gala. Plant Cell Rep. 14:407-412
153. Zini E. 2005. Construzione di una mappa di associazione della popolazione di melo 'Golden Delicious' x 'Freedom' e caratterizzazione del gene di resistenza Va a ticchiolatura. PhD thesis, Univ. Bologna, Italy. 126 pp.