GENETICS OF RAPE (BRASSI CA NAPUS L.) RESISTANCE TO BLACKLEG
Abstract
About the Author
E. A. VoluevichBelarus
D. Sc. (Biol.), Associate Professor, Chief scientific employee
References
1. Friedt, W., Snowdon, R., Ordon, F. and Ahlemeyer, J. (2007), “Plant breeding: assessment of genetic diversity in crop plants and its exploitation in breeding”, Progress in Botany, vol. 168, pp. 151–178.
2. Mendes-Pereira, E., Balesdent, M. H., Brun H. and Rouxel, T. (2003), “Molecular phylogeny of the Leptosphaeria maculans – L. biglobosa species complex”, Mycological Research, vol. 107, pp. 1287–1304, doi:10.1017/S0953756203008554.
3. Gudelj, I., Fitt, B. D. L. and van den Bosch, F. (2004), “Evolution of sibling fungal pathogens in relation to host specialization”, Phytopathology, vol. 94, pp. 789–795, doi: 10.1094/PHYTO.2004.94.7.789.
4. West, J. S., Kharband, P. D., Barbetti, M. J. and Fitt, B. D. L. (2001), “Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe”, Plant Pathology, vol. 50, pp. 10–27, doi: 10.1046/j.1365-3059.2001.00546.x.
5. Rouxel, T. and Balesdent, M. H. (2005), “The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era”, Molecular Plant Pathology, vol. 6, pp. 225–241. doi: 10.1111/j.1364-3703.2005.00282.x.
6. Williams, R. H. and Fitt, B. D. (1994), “Variation in host range, systemic infection and epidemiology of Leptosphaeria maculans”, Plant Pathology, vol. 43, pp. 269–277, doi: 10.1111/j.1365-3059.1994.tb02685.x.
7. Williams, R. H. and Fitt, B. D. L. (1999), “Differentiating A and B groups of Leptosphaeria maculans, causal agent of stem canker (blackleg) of oilseed rape”, Plant Pathology, vol. 48, pp. 161–175.
8. Shoemaker, R. A. and Brun, H. (2001), “The teleomorph of the weakly aggressive segregate of Leptosphaeria maculans”, Canadian Journal of Botany, vol. 79, pp. 412–419, doi: 10.1139/b01-019.
9. West, J. S., Balesdent, M. H., Rouxel, T., Narcy, J. P., Huang, Y. J., Roux, J., Steed, J. M., Fitt, B. D. L. and Schmit,
10. J. (2002a), “Colonisation of winter oilseed rape tissues by A/Tox+ and B/Tox0 Leptosphaeria maculans (phoma stem canker) in France and England”, Plant Pathology, vol. 51, pp. 311–321.
11. Jędryczka, M., Lewartowska, E. and Frencel, I. (1994), “Properties of Phoma lingam (Tode ex Fr.) Desm. isolates from Poland. I. Pathogenicity characterization”, Phytopathologia Polonica, vol. 7, pp. 71–79.
12. Karolewski, Z., Kosiada, T., Hylak-Nowosad, B. and Nowacka, K. (2002), “Changes in population structure of Leptosphaeria maculans in Poland”, Phytopathologia Polonica, vol. 25, pp. 27–34.
13. Jędryczka, M., Burzyński, A., Brachaczek, A., Langwiński, W., Chwalisz, L. and Kaczmarek, J. (2014), “Loop-mediated isothermal amplification (LAMP) is a speedy molecular tool to study Leptosphaeria spp. populations in air and plant samples”, Healthy plant – healthy people: 11th conf. of the European foundation for plant pathology, Krakόw , PL, 8–13 September 2014, p. 137.
14. Szlávik, S. Z., Jedryczka, M., Kiss, I., Lewartowska, E. and Nagy, G. (2003), “Population structure and pathogenicity grouping of L. maculans isolates from Hungary”, Blackleg News, pp. 3–4.
15. Brazauskienė, I., Piliponytė, A., Petraitienė, E. and Brazauskas, G. (2011), “Diversity of Leptosphaeria maculans / L. biglobosa species complex and epidemiology of phoma stem canker on oilseed rape in Lithuania”, Journal of Plant Pathology, vol. 93, no. 3, pp. 577–585.
16. Fitt, B. D. L., Brun, H., Barbetti, M. J. and Rimmer, S. R. (2006), “World-wide importance of Phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus)”, European Journal of Plant Pathology, vol. 114, no. 1, pp. 3–15, doi: 10.1007/s10658-005-2233-5.
17. Fernando, W. G. D., Zhang, X. and Amarasinghe, C. C. (2016), “Detection of Leptosphaeria maculans and Lepto- sphaeria biglobosa causing blackleg disease in canola from canadian canola seed lots and dockage”, Plants, vol. 5, no. 1, pp. 1–11, doi: 10.3390/plants5010012.
18. Hao, L., Song, P., Huangfu, H. and Li, Z. (2015), “Genetic diversity and differentiation of Leptosphaeria biglobosa on oilseed rape in China”, Phytoparasitica, vol. 43, issue 2, pp. 253–263, doi: 10.1007/s12600-014-0439-9.
19. Huang, Y. J., Fitt, B. D. L., Jedryczka, M., Dakowska, S., West, J. S., Gladders, P., Steed, J. M. and Li, Z.Q. (2005), “Patterns of ascospore release in relation to phoma stem canker epidemiology in England (Leptosphaeria maculans) and Poland (L. biglobosa)”, European Journal of Plant Pathology, vol. 111, pp. 263–277, doi: 10.1007/s10658-004-4421-0.
20. Hadrami, El. A., Fernando, W. G. D. and Daayf, F. (2010), “Variations in relative humidity modulate Leptosphaeria spp. pathogenicity and interfere with canola mechanisms of defence”, European Journal of Plant Pathology, vol. 126, pp. 187–202, doi: 10.1007/s10658-009-9532-1.
21. Hammond, K. E., Lewis, B. G. and Musa, T. M. (1985), “A systemic pathway in the infection of oilseed rape plants by Leptosphaeria maculans”, Plant Pathology, vol. 34, no. 4, pp. 557–565.
22. Williams, P. H. (1992), “Biology of Leptosphaeria maculans”, Canadian Journal of Plant Pathology, vol. 14, pp. 30–35.
23. Hall, R. (1992), “Epidemiology of blackleg of oilseed rape”, Can. J. Plant Pathology, vol. 14, pp. 46–55, doi: 10.3390/ plants5030031.
24. Keri, M. (1999), “Genetic studies of host-pathogen interaction between Brassica napus and Leptosphaeria maculans”, Ph. D. Thesis, University of Manitoba, Winnipeg, CA.
25. Stachowiak, A., Olechnowicz, J., Jedryczka, M. Rouxel, T., Balesdent, M.-H., Happstadius, I., Gladders, P., Latunde-Dada, A. and Evans, N. (2006), “Frequency of avirulence alleles in field populations of Leptosphaeria maculans in Europe”, European Journal of Plant Pathology, vol. 114, pp. 67–75, doi: 10.1007/s10658-005-2931-z.
26. Gladders, P. and Musa, T. M. (1980), “Observations on the epidemiology of Leptosphaeria maculans stem canker in winter oilseed rape”, Plant Pathology, vol. 29, pp. 28–37.
27. Gugel, R. K. and Petrie, G. A. (1992), History, occurrence, impact, and control of blackleg of rapeseed, Canadian Journal of Plant Pathology, vol. 14, pp. 36–45.
28. Zhang, X., White, R. P., Jedryczka, M., Lange, R. M., Li, Z. Q., Huang, Y.-J., Hall, A. M. and Fitt, B. D. L. (2014), “Potential spread of Leptosphaeria maculans (phoma stem canker) on oilseed rape crops in China”, Healthy plant – healthy people: 11th conf. of the European foundation for plant pathology, Krakόw, PL, 8–13 September 2014, p. 135.
29. Fernando, W. G. D., Chen, Y. and Ghanbarnia, K., “Breeding for blackleg resistance: the biology and epidemiology”, Advances in Botanical Research, 2007, vol. 45, pp. 271–311.
30. Salam, M. U., Fitt, B. D. L., Aubertot, J. N., Diggle, A. J., Huang, Y. J., Barbetti, M. J., Gladders, P., Jędryczka, M., Khangura, R. K., Wratten, N., Fernando, W. G. D., Penaud, A., Pinochet, X. and Sivasithamparam, K. (2007), “Two weather-based models for predicting the onset of seasonal release of ascospores of Leptosphaeria maculans or L. biglobosa”, Plant Pathology, vol. 56, pp. 412–423, doi: 10.1111/j.1365-3059.2006.01551.x.
31. Biddulph, J. E., Fitt, B. D. L., Leech, P. K., Welham, S. J. and Gladders, P. (999), “Effects of temperature and wetness duration on infection of oilseed rape leaves by ascospores of Leptosphaeria maculans (stem canker)”, European Journal of Plant Pathology, vol. 105, pp. 769–781, doi: 10.1023/A:1008727530088.
32. Badawy, H. M. A., Kakau, J. and Hoppe, H. H. (1992), “Temperature and aging of host tissue affect the interactions between different oilseed rape cultivars and pathotype groups of Leptosphaeria maculans”, Journal of Phytopathology, vol. 134, pp. 255–263.
33. Petrie, G. A. (1994), “Effects of temperature and moisture on the number, size and septation of ascospores produced by Leptosphaeria maculans (blackleg) on rapeseed stubble”, Canadian Plant Diease Survey, vol. 74, pp. 141–151.
34. Guo, X. W. and Fernando, W. G. D. (2005), “Seasonal and diurnal patterns of spore dispersal by Leptosphaeria mac-ulans from canola stubble in relation to environmental conditions”, Plant Disease, vol. 89, pp. 97–104.
35. Petrie, G. A. (1995), “Long-term survival and sporulation of Leptosphaeria maculans (blackleg) on naturally-infected rapeseed/canola stubble in Saskatchewan”, Canadian Plant Disease Survey, vol. 75, pp. 23–34.
36. West, J. S., Biddulph, J. E., Fitt, B. D. L. and Gladders, P. (1999), “Epidemiology of Leptosphaeria maculans in relation to forecasting stem canker severity on winter oilseed rape in the UK”, Annals of Applied Biology, vol. 135, pp. 535–546.
37. Marcroft, S. J., Van de Wouw, A. P., Salsibury, P. A., Pottere, T. D. and Howlett, B. J. (2012), “Effect of rotation of canola (Brassica napus) cultivars with different compliments of blackleg resistance genes on disease severity”, Plant Pathology, vol. 61, pp. 934–944, doi: 10.1111/j.1365-3059.2011.02580.x.
38. Delourme, R., Brun, H., Ermel, M., Lucas, M. O., Vallee, P., Domin, C., Walton, G., Li, H., Sivasithamparam, K. and Barbetti, M. J. (2008), “Expression of resistance to Leptosphaeria maculans in Brassica napus double haploid lines in France and Australia is influenced by location”, Annals of Applied Biology, vol. 153, pp. 259–269, doi: 10.1111/j.1744-7348.2008.00258.x.
39. Li, H., Barbetti, M. J. and Sivasithamparam, K. (2005), “Hazard from reliance on cruciferous hosts as source of major gene-based resistance for managing blackleg (Leptosphaeria maculans) disease”, Field Crops Research, vol. 91, pp. 185–198.
40. Howlett, B. J. (2004), “Current knowledge of the interaction between Brassica napus and Leptosphaeria maculans”, Canadian Journal of Plant Pathology, vol. 26, pp. 245–252.
41. Lamey, H. A. and Hershman, D. E. (1993), “Blackleg canola (Brassica napus) caused by Leptosphaeria maculans in North Dakota”, Plant Disease, vol. 77, p. 1263. doi: 10.1094/PD-77-1263B.
42. Wang, J., Kaur, S., Cogan, N. O. I., Dobrowolski, M. P., Salisbury, P. A., Burton, W. A., Baillie, R., Hand, M., Hopkins, C., Forster, J. W., Smith, K. F. and Spangenberg, G. (2009), “Assessment of genetic diversity in Australian canola (Brassica napus L.) cultivars using SSR markers”, Crop and Pasture Science, vol. 60, pp. 1193–1201.
43. Kaur, S., Cogan, N. O. I., Ye, G., Baillie, R. C., Hand, M. L., Ling, A. E., Mcgearey, A. K., Kaur, J., Hopkins, C. J., Todorovic, M., Mountford, H., Edwards, D., Batley, J., Burton, W., Salisbury, P., Gororo, N., Marcroft, S., Kearney, G., Smith, K. F., Forster, J. W. and Spangenberg, G. C. (2009), “Genetic map construction and QTL mapping of resistance to blackleg (Leptosphaeria maculans) disease in Australian canola (Brassica napus L.) cultivars”, Theoretical and Applied Genetics, vol. 120, no. 1, pp. 71–83, doi: 10.1007/s00122-009-1160-9.
44. Tollenaere, R., Hayward, A., Dalton-Morgan, J., Campbell, E., Lee, J. R. M., Lorenc, M. T., Manoli, S., Stiller, J., Raman, R., Raman, H., Edwards, D. and Batley, J. (2012), “Identification and characterization of candidate Rlm4 blackleg resistance genes in Brassica napus using next generation sequencing”, Plant Biotechnology Journal, vol. 10, no. 6, pp. 709–715, doi: 10.1111/j.1467-7652.2012.00716.x.
45. Sprague, S. J., Marcroft, S. J., Hayden, H. L. and Howlett, B. J. (2006), “Major gene resistance to blackleg in Brassica napus overcome within three years of commercial production in southeastern Australia”, Plant Pathology, vol. 59, pp. 190– 198, doi: 10.1094/PD-90-0190.
46. Tilmor: vash klyuch k vyraschivaniyu rapsa (Tilmor: your key to the cultivation of rape), Available at: http://tv.sb.by/ kolonka-eksperta/article/tilmor-vash-klyuch-k-vyrashchivaniyu-rapsa.html/ (Accessed 30 August 2016).
47. Rouxel, T., Grandaubert, J., Hane, J. K., Hoede, C., van de Wouw, A. P., Couloux, A., Dominguez, V., Anthouard, V., Bally, P., Bourras, S., Cozijnsen, A. J., Ciuffetti, L. M., Degrave, A., Dilmaghani, A., Duret, L., Fudal, I., Goodwin, S. B., Gout, L., Glaser, N., Linglin, J., Kema, G. H. J., Lapalu, N., Lawrence, C. B., May, K., Meyer, M., Ollivier, B., Poulain, J., Schoch, C. L., Simon, A., Spatafora, J.W., Stachowiak, A., Turgeon, B. G., Tyler, B. M., Vincent, D., Weissenbach, J., Amselem, J., Quesneville, H., Oliver, R. P., Wincker, P., Balesdent, M.-H. and Howlett, B. J. (2011), “Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations”, Nature Communications, vol. 2, no. 202, pp. 1–10, doi: 10.1038/ncomms1189.
48. Hayward, A., McLanders, J., Campbell, E., Edwards, D. and Batley, J. (2012), “Genomic advances will herald new insights into the Brassica: Leptosphaeria maculans pathosystem”, Plant Biology, vol. 14, suppl. 1, pp. 1–10, doi:10.1111/ j.1438-8677.2011.00481.x.
49. Gout, L., Kuhn, M. L., Vincenot, L., Bernard-Samain, S., Cattolico, L., Barbetti, M., Moreno-Rico, O., Balesdent, M. H. and Rouxel, T. (2007), “Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans”, Environmental Microbilogy, vol. 9, pp. 2978–2992, doi: 10.1111/j.1462-2920.2007.01408.x.
50. Fudal, I., Ross, S., Brun, H., Besnard, A. L., Ermel, M., Kuhn, M. L., Balesdent, M. H. and Rouxel, T. (2009), “Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans”, MPMI, vol. 22, pp. 932–941, doi: 10.1094/MPMI-22-8-0932.
51. Parlange, F., Daverdin, G., Fudal, I., Kuhn, M.-L., Balesdent, M.-H., Blaise, F., Grezes-Besset, B. and Rouxel, T. (2009), “Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change”, Molecular Microbiology, vol. 71, pp. 851–863, doi: 10.1111/j.1365-2958.2008.06547.x.
52. Farman, M. L. (2007), “Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it”, FEMS Microbiology Letters, vol. 273, pp. 125–132, doi: 10.1111/j.1574-6968.2007.00812.x.
53. Plissonneau, C., Daverdin, G., Ollivier, B., Blaise, F., Degrave, A., Fudal, I., Rouxel, T. and Balesdent, M.-H. (2016), “A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans”, New Phytologist, vol. 209, pp. 1613–1624, doi: 10.1111/nph.13736.
54. Fudal, I., Ross, S., Gout, L., Blaise, F., Kuhn, M. L., Eckert, M. R., Cattolico, L., Bernard-Samain, S., Balesdent, M. H. and Rouxel, T. (2007), “Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6”, MPMI, vol. 20, pp. 459–470.
55. Balesdent, M. H., Attard, A., Kühn, M. L. and Rouxel, T. (2002), “New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans”, Phytopathology, vol. 92, pp. 1122–1133.
56. Balesdent, M. H., Barbetti, M.J., Li, H., Sivasithamparam, K., Gout, L. and Rouxel, T. (2005), “Analysis of Lepto- sphaeria maculans race structure in a worldwide collection of isolates”, Phytopathology, vol. 95, pp. 1061–1071, doi: 10.1094/ PHYTO-95-1061.
57. Ghanbarnia, K., Lydiate, J. L., Rimmer, S. R., Li, G., Kutcher, H. R., Larkan, N. J., McVetty, P. B. E. and Fernando, W. G. D. (2012), “Genetic mapping of the Leptosphaeria maculans avirulance gene corresponding to the LepR1 resistance gene of Brassica napus”, Theoretical and Applied Genetics, vol. 124, pp. 505–513, doi: 10.1007/s00122-011-1724-3.
58. Gout, L., Fudal, I., Kuhn, M.-L., Blaise, F., Eckert, M., Cattolico, L., Balesdent, M.-H. and Rouxel, T. (2006), “Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans”, Molecular Microbiology, vol. 60, pp. 67–80, doi:10.1111/j.1365-2958.2006.05076.x.
59. Ghanbarnia, K., Fudal, I., Larkan, N. J., Links, M. G., Balesdent, M.-H., Profotova, B., Fernando, W. G. D., Rouxel, T. and Borhan, M. H. (2015), “Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2 using an intraspecific comparative genomics approach”, Molecular Plant Pathology, vol. 16, no. 7, pp. 699–709, doi: 10.1111/mpp.12228.
60. Balesdent, M.-H., Fudal, I., Ollivier, B., Bally, P., Grandaubert, J., Eber, F., Chèvre, A.-M., Leflon, M. and Rouxel, T. (2013), “The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa”, New Phytologist, vol. 198, pp. 887–898, doi: 10.1111/nph.12178.
61. Van de Wouw, A. P., Lowe, R. G. T., Elliott, C. E., Dubois, D. J. and Howlett, B. J. (2014а), “An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars”, Molecular Plant Pathology, vol. 15, pp. 523–530.
62. Balesdent, M. H., Louvard, K., Pinochet, X. and Rouxel, T. A. (2006), “A large-scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France”, European Journal of Plant Pathology, vol. 114, pp. 53–65, doi: 10.1007/ s10658-005-2104-0.
63. Mitrousia, G. K., Huang, Y.-J. and Fitt, B. D. L. (2014), “Phoma stem canker on oilseed rape cultivars with the resistance gene Rlm7 in the UK”, Healthy plant – healthy people: 11th conf. of the European foundation for plant pathology, Krakόw, PL, 8–13 September 2014, p. 128.
64. Peng, G., Fernando, D., Yu, F., Zhang, X., Lange, R. and Kutcher, H. R. (2014), “Managing blackleg of canola in western Canada – “new” strategies against an old disease”, Healthy plant – healthy people: 11th conf. of the European foundation for plant pathology, Krakόw, PL, 8–13 September 2014, p. 132.
65. Zhang, X., Peng, G., Kutcher, H. R., Balesdent, M.-H., Delourme, R. and Fernando, W. G. D. (2015), “Breakdown of Rlm3 resistance in the Brassica napus–Leptosphaeria maculans pathosystem in western Canada”, European Journal of Plant Pathology, vol. 145, no. 3, pp. 1–16, doi: 10.1007/s10658-015-0819-0.
66. Winter, M., Klӧppel, C., Fajemisin, F. and Koopmann, B. (2014), Leptosphaeria maculans in winter oilseed rape: distribution of different races in Germany and efficacy of monogenic resistance genes”, Healthy plant – healthy people: 11th conf. of the European foundation for plant pathology, Krakόw, PL, 8–13 September 2014, p. 133.
67. Ferreira, M. E., Williams, P. H. and Osborn, T. C. (1995), “Mapping of a locus controlling resistance to Albugo candida in Brassica napus using molecular markers”, Phytopathology, vol. 85, pp. 218–220.
68. Ansan-Melayah, D., Balesdent, M. H., Delourme, R., Pilet, M. L., Tanguy, X., Renard, M. and Rouxel, T. (1998), “Genes for race-specific resistance against blackleg disease in Brassica napus L.”, Plant Breeding, vol. 117, pp. P. 373–378, doi: 10.1111/j.1439-0523.1998.tb01956.x.
69. Pilet, M. L., Delourme, R., Foisset, N. and Renard, M. (1998), “Identification of QTL involved in field resistance to light leaf spot (Pyrenopeziza brassicae) and blackleg resistance (Leptosphaeria maculans) in winter rapeseed (Brassica na-pus L.)”, Theoretical and Applied Genetics, vol. 97, pp. 398–406.
70. Delourme, R., Chèvre, A. M., Brun, H., Rouxel, T., Balesdent, M. H., Dias, J. S., Salisbury, P., Renard, M. and Rim- mer, S. R. (2006), “Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus)”, European Journal of Plant Pathology, vol. 114, pp. 41–52, doi: 10.1007/s10658-005-2108-9.
71. Rimmer, S. R. and van den Berg, C. G. J. (1992), “Resistance of oilseed Brassica spp. to blackleg caused by Leptosphaeria maculans”, Canadian Journal of Plant Pathology, vol. 14, pp. 56–66.
72. Zhu, J. S., Struss, D. and Robbelen, G. (1993), “Studies on resistance to Phoma lingam in Brassica napus – Brassica nigra addition lines”, Plant Breeding, vol. 111, pp. 192–197, doi: 10.1111/j.1439-0523.1993.tb00629.x.
73. Ananga, A. O., Cebert, E., Soliman, K., Kantety, R., Pacumbaba, R. P. and Konan, K. (2006), “RAPD markers associated with resistance to blackleg disease in Brassica species”, African Journal of Biotechnology, vol. 5, pp. 2041–2048, doi: 10.5897/AJB06.594.
74. Leflon, M., Brun, H., Eber, F., Delourme, R., Lucas, M. O., Vallée, P., Ermel, M., Balesdent, M. H. and Chèvre, A. M. (2007), “Detection, introgression and localization of genes conferring specific resistance to Leptosphaeria maculans from Brassica rapa into B. napus”, Theoretical and Applied Genetics, vol. 115, pp. 897–906, doi: 10.1007/s00122-007-0616-z.
75. Delourme, R., Pilet-Nayel, M. L., Archipiano, M., Horvais, R., Tanguy, X., Rouxel, T., Brun, H., Renard, M. and Balesdent, M. H. (2004), “A cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus”, Phytopathology, vol. 94, pp. 578–583, doi: 10.1094/PHYTO.2004.94.6.578.
76. Brun, H., Chèvre, A. M., Fitt, B. D., Powers, S., Besnard, A.-L., Ermel, M., Huteau, V., Marquer, B., Eber, F., Renard, M. and Andrivon, D. (2010), “Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria mac-ulans in Brassica napus”, New Phytologist, vol. 185, pp. 285–299, doi: 10.1111/j.1469-8137.2009.03049.x.
77. Raman, R., Taylor, B., Lindbeck, K., Coombes, N., Barbulescu, D., Salisbure, P. and Raman, H. (2012), “Molecular mapping and validation of Rlm1 gene for resistance to Leptosphaeria maculans in canola (Brassica napus L.)”, Crop and Pasture Science, vol. 63, pp. 1007–1017, doi: 10.1071/CP12255.
78. Wang, Z. (2013), “Development of high-throughput molecular markers for blackleg (Leptosphaeria maculans) resistance genes in Brassica napus for gene stacking”, Universal Journal of Plant Science, vol. 1, pp. 118–124, doi: 10.13189/ ujps.2013.010402.
79. Rouxel, T., Penaud, A., Pinochet, X., Brun, H., Gout, L., Delourme, R., Schmit, J. and Balesdent, M.-H. (2003), “A ten-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape”, European Journal of Plant Pathology, vol. 109, pp. 871–881.
80. Larkan, N. J., Lydiate, D. J., Parkin, I. A. P., Nelson, M. N., Epp, D. J., Cowling, W. A., Rimmer, S. R. and Borhan, M. H. (2013), “The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1”, New Phytologist, vol. 197, pp. 595–605, doi: 10.1111/nph.12043.
81. Larkan, N. J., Lydiate, D. J., Yu. F., Rimmer, S. R. and Borhan, M. H. (2014), “Co-localisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10”, BMC Plant Biology, vol. 14, no. 387, pp. 1–9, doi: 10.1186/ s12870-014-0387-z.
82. Balesdent, M. H., Attard, A., Ansan-Melayah, D., Delourme, R., Renard, M. and Rouxel, T. (2001), “Genetic control and host range of avirulence toward Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans”, Phyto- pathology, vol. 91, pp. 70–76, doi: 10.1094/PHYTO.2001.91.1.70.
83. Raman. R., Taylor, B., Marcroft, S., Stiller, J., Eckermann, P., Coombes, N., Rehman, A., Lindbeck, K., Luckett, D., Wratten, N., Batley, J., Edwards, D., Wang, X. and Raman, H. (2012b), “Molecular mapping of qualitative and quantitative loci for resistance to Leptosphaeria maculans causing blackleg disease in canola (Brassica napus L.)”, Theoretical and Applied Genetics, vol. 125, pp. 405–418, doi: 10.1007/s00122-012-1842-6.
84. Chèvre, A. M., Barret, P., Eber, F., Dupuy, P., Brun, H., Tanguy, X. and Renard, M. (1997), “Selection of stable Bras- sica napus – B. juncea recombinant lines resistant to blackleg (Leptosphaeria maculans). 1. Identification of molecular markers, chromosomal and genomic origin of the introgression”, Theoretical and Applied Genetics, vol. 95, pp. 1104–1111.
85. Chèvre, A. M., Brun, H., Eber, F., Letanneur, J.-C., Vallee, P., Ermel, M., Glais, I., Li, H., Sivasithamparam, K. and Barbetti, M. J. (2008), “Stabilization of resistance to Leptosphaeria maculans in Brassica napus – B. juncea recombinant lines and its introgression into spring type Brassica napus”, Plant Disease, vol. 92, pp. 1208–1214, doi:10.1094/PDIS-92-8-1208.
86. Chèvre, A. M., Eber, F., This, P., Barret P., Tanguy, X., Brun, H., Delseny, M. and Renard, M. (1996), “Characterization of Brassica nigra chromosomes and of blackleg resistance in B. napus – B. nigra addition lines”, Plant Breeding, vol. 115, pp. 113–118, doi: 10.1111/j.1439-0523.1996.tb00884.x.
87. Yu, F., Lydiate, D. J. and Rimmer, S. R. (2005), “Identification of two novel genes for blackleg resistance in Brassica napus, Theoretical and Applied Genetics”, vol. 110, pp. 969–979, doi: 10.1007/s00122-004-1919-y.
88. Yu, F., Lydiate, D. J. and Rimmer, S. R. (2008), “Identification and mapping of a third blackleg resistance locus in Brassica napus derived from B. rapa subsp. sylvestris”, Genome, vol. 51, pp. 64–72, doi: 10.1139/G07-103.
89. Rimmer, S. R. (2006), “Resistance genes to Leptosphaeria maculans in Brassica napus”, Canadian Journal of Plant Pathology, vol. 28, pp. 288–297.
90. Yu, F., Gugel, R., Kutcher, H., Peng, G. and Rimmer, S. R. (2013), “Identification and mapping of a novel blackleg resistance locus LepR4 in the progenies from Brassica napus × B. rapa subsp. sylvestris”, Theoretical and Applied Genetics, vol. 126, no. 2. pp. 307–315, doi: 10.1007/s00122-012-1919-2.
91. Saal, B., Brun, H., Glais, I. and Struss, D. (2004), “Identification of a Brassica juncea-derived recessive gene conferring resistance to Leptosphaeria maculans in oilseed rape”, Plant Breeding, vol. 123, pp. 505–511.
92. Saal, B. and Struss, D. (2005), “RGA- and RAPD-derived SCAR markers for a Brassica B-genome introgression conferring resistance to blackleg in oilseed rape”, Theoretical and Applied Genetics, vol. 111, pp. 281–290, doi: 10.1007/s00122-005-2022-8.
93. Dion, Y., Gugel, R. K., Rakow, G. F. W., Séguin-Swartz, G. and Landry, B. S. (1995), “RFLP mapping of resistance to the blackleg disease [causal agent, Leptosphaeria maculans (Desm) Ces et de Not] in canola (Brassica napus L.)”, Theoretical and Applied Genetics, vol. 91, P. 1190–1194, doi: 10.1007/BF00220928.
94. Zhu, B. and Rimmer, S. R. (2003), “Inheritance of resistance to Leptosphaeria maculans in two accessions of Brassica napus”, Canadian Journal of Plant Pathology, vol. 25, pp. 98–103, doi: 10.1080/07060660309507054.
95. Mayerhofer, R., Bansal, V. K., Thiagarajah, M. R., Stringam, G. R. and Good, A. G. (1997), “Molecular mapping of resistance to Leptosphaeria maculans in Australian cultivars of Brassica napus”, Genome, vol. 40, pp. 294–301.
96. Ferreira, M. E., Rimmer, S. R., Williams, P. H. and Osborn, T. C. (1995), “Mapping loci controlling Brassica napus resistance to Leptosphaeria maculans under different screening conditions”, Phytopathology, vol. 85, no. 2, pp. 213–217.
97. Rouxel, T., Willner, E., Coudard, L. and Balesdent, M.-H. (2003), “Screening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions”, Euphytica, vol. 133, pp. 219–231.
98. Wretblad, S., Bohman, S. and Dixelius, C. (2003), “Overexpression of a Brassica nigra cDNA gives enhanced resistance to Leptosphaeria maculans in B. napus”, MPMI, vol. 16, pp. 477–484, doi: 10.1094/MPMI.2003.16.6.477.
99. Dixelius, C. (1999), “Inheritance of the resistance to Leptosphaeria maculans of Brassica nigra and B. juncea in near-isogenic lines of B. napus”, Plant Breeding, vol. 118, pp. 151–156.
100. Ansan-Melayah, D., Rouxel, T., Bertrandy, J., Letarnec, B., Mendes-Pereira, E. and Balesdent, M.-H. (1997), “Field efficiency of Brassica napus specific resistance correlates with Leptosphaeria maculans population structure”, European Journal of Plant Pathology, vol. 103, pp. 835–841, doi:10.1023/A:1008605829110.
101. Pilet, M. L., Duplan, G., Archipiano, M., Barret, P., Baron, C., Horvais, R., Tanguy, X., Lucas, M., Renard, M. and Delourme, R. (2001), “Stability of QTL for field resistance to blackleg across two genetic backgrounds in oilseed rape”, Crop Science, vol. 41, pp. 197–205.
102. Flor, H. H. (1956), “The complementary genetic systems in flax and flax rust”, Advances in Genetics, vol. 8, no. 1, pp. 29–54, doi: 10.1371/journal.pbio.0030203.
103. Jones, J. D. G. and Dangl, J. L. (2006), The plant immune system, Nature, vol. 444, no. 16, pp. 323–329, doi: 10.1038/ nature05286.
104. Poland, J. A., Balint-Kurti, P. J., Wisser, R. J., Pratt, R. C. and Nelson, R. J. (2008), “Shades of gray: the world of quantitative disease resistance”, Trends in Plant Science, vol. 14, no. 1, pp. 21–29, doi: 10.1016/j.tplants.2008.10.006.
105. Salisbury, P. A., Ballinger, D. J., Wratten, N., Plummer, K. M. and Howlett, B. J. (1995), “Blackleg disease on oilseed Brassica in Australia”, Australian Journal of Experimental Agriculture, vol. 35, pp. 665–672.
106. Khangura, R. K. and Barbetti, M. J. (2001), “Prevalence of blackleg (Leptosphaeria maculans) on canola (Brassica napus) in Western Australia”, Australian Journal of Experimental Agriculture, vol. 41, pp. 71–40, doi: 10.1071/EA00068.
107. Marcroft, S. J., Sprague, S. J., Pymer, S. J., Salisbury, P. A. and Howlett, B. J. (2003), “Factors affecting production of inoculum of the blackleg fungus Leptosphaeria maculans in south-eastern Australia”, Australian Journal of Experimental Agriculture, vol. 43, pp. 1231–1236.
108. Marcroft, S. J., Sprague, S. J., Salisbury, P. A. and Howlett, B. J. (2004), “Potential for using host-resistance to reduce production of pseudothecia and ascospores of Leptosphaeria maculans, the blackleg pathogen of Brassica napus”, Plant Pathology, vol. 53, pp. 468–474, doi: 10.1111/j.1365-3059.2004.01050.x.
109. Pilet, M. L., Delourme, R., Foisset, N. and Renard, M. (1998), “Identification of loci contributing to quantitative field resistance to blackleg disease, causal agent Leptosphaeria maculans (Desm.) ces. et De Not., in winter rapeseed (Brassica napus L.)”, Theoretical and Applied Genetics, vol. 96, pp. 23–30.
110. Brun, H., Huteau, V., Ermel, M., Eber, F., Chevre, A. M. and Renard, M. (2004), “Field behaviour of oilseed rape genotypes carrying major resistance genes exposed to different Leptosphaeria maculans populations”, International Organisation for Biological Control Bulletin, vol. 27, pp. 95–100.
111. Light, K. A., Gororo, N. N. and Salisbury, P. A. (2011), “Usefulness of winter canola (Brassica napus) race-specific resistance genes against blackleg (causal agent Leptosphaeria maculans) in southern Australian growing conditions”, Crop and Pasture Sciense, vol. 62, pp. 162–168, doi: 10.1071/CP10187.
112. Huang, Y. J., Jestin, C., Welham, S. J., King, G. J., Manzanares-Dauleux, M. J., Fitt, B. D. L. and Delourm, R. (2016), “Identification of environmentally stable QTL for resistance against Leptosphaeria maculans in oilseed rape (Brassica na-pus)”, Theoretical and Applied Genetics, vol. 129, no. 1, pp. 169–180, doi: 10.1007/s00122-015-2620-z.
113. Raman, H., Raman, R., Taylor, B., Lindbeck, K., Coombes, N., Eckermann, P., Batley, J., Edwards, D., Price, A., Rehman, A., Marcroft, S., Luckett, D., Hossain, S. and Salisbury, P. (2011), “Blackleg resistance in rapeseed: phenotypic screen, molecular markers and genome wide linkage and association mapping”, 17th Australian Research Assembly on Brassicas (ARAB), Wagga Wagga, AU, 15–17 August, pp. 61–64.
114. Jestin, C., Lodé, M., Vallée, P., Domin, C., Falentin, C., Horvais, R., Coedel, S., Manzanares-Dauleux, M. J. and Delourme, R. (2011), “Association mapping of quantitative resistance for Leptosphaeria maculans in oilseed rape (Brassica napus L.)”, Molecular Breeding, vol. 27, pp. 271–287, doi: 10.1007/s11032-010-9429-x.
115. Brun, H., Levivier, S., Eber, F., Renard, M. and Chèvre, A. M. (1997), “Electrophoretic analysis of natural populations of Leptosphaeria maculans directly from leaf lesions”, Plant Pathology, vol. 46, pp. 147–154, doi: 10.1046/j.1365-3059.1997. d01-209.x.
116. Somda, I., Renard, M. and Brun, H. (1998), “Seedling and adult plant reactions of Brassica napus – B. juncea recombinant lines towards A- and B-group isolates of Leptosphaeria maculans”, Annals of Applied Biology, vol. 132, pp. 187–196, doi: 10.1111/j.1744-7348.1998.tb05196.x.
117. Plissonneau, C., Rouxel, T., Daverdin, G. Meur, L. L., Soulard, T., Cugnire, L. and Balesdent, M.-H. (2014), “Evolution of the frequency of the AvrLm7 allele of Leptosphaeria maculans in France under selection pressure: a 15-years survey”, Healthy plant – healthy people: 11th conf. of the European foundation for plant pathology, Krakόw, PL, 8–13 Sep- tember 2014, p. 129.
118. Chalhoub, B., Denoeud, F., Liu, S., Parkin, I. A. P., Tang, H., Wang, X., Chiquet, J., Belcram, H., Tong, C., Samans, B., Corréa, M., Silva, C. D., Just, J., Falentin, C., Koh, C. S., Clainche, I. L., Bernard, M., Bento, P., Noel, B., Labadie, K., Alberti, A., Charles, M., Arnaud, D., Guo, H., Daviaud, C., Alamery, S., Jabbari, K., Zhao, M., Edger, P. P., Chelaifa, H., Tack, D., Lassalle, G., Mestiri, I., Schnel, N., Paslier, M.-C. L., Fan, G., Renault, V., Bayer, P. E., Golicz, A. A., Manoli, S., Lee, T.-H., Thi, V. H. D., Chalabi, S., Hu, Q., Fan, C., Tollenaere, R., Lu, Y., Battail, C., Shen, J., Sidebottom, C. H. D., Wang, X., Canaguier, A., Chauveau, A., Bérard, A., Deniot, G., Guan, M., Liu, Z., Sun, F., Lim, Y. P., Lyons, E., Town, C. D., Bancroft, I., Wang, X., Meng, J., Ma, J., Pires, J. C., King, G. J., Brunel, D., Delourme, R., Renard, M., Aury, J.-M., Adams, K. L., Batley, J., Snowdon, R. J., Tost, J., Edwards, D., Zhou, Y., Hua, W., Sharpe, A. G., Paterson, A. H., Guan, C. and Wincker, P. (2014), “Early allopolyploid evolution in the post – Neolithic Brassica napus oilseed genome”, Science, vol. 345, pp. 950–953.