Abstract
Leptosphaeria maculans, the cause of stem canker of oilseed rape (OSR), exhibits gene-for-gene interactions with its host plant. The race structure of L. maculans was assessed on the basis of the analysis of 1011 isolates collected in France between 1990 and 2000, with regards to three AVR genes, AvrLm1, AvrLm2 and AvrLm4. The effect of selection pressure, due to large-scale cropping of Rlm1 cultivars, on the evolution of races of the fungus was also evaluated. The results revealed a scarcity or complete absence of isolates harbouring AvrLm2, whereas isolates harbouring AvrLm4 were present at a variable level, that was as high as 17.2–31.2% depending on the sample year and location. When obtained from rlm1 cultivars, isolates harbouring AvrLm1 always represented more than 83% of the populations until the 1997–1998 growing season. As a consequence, the Rlm1 cultivars had been highly efficient at controlling the disease and were grown on an estimated 43.7% of the total French acreage in OSR in 1998–1999. However, the increased commercial success of Rlm1 cultivars was paralleled by a decrease in the proportion of isolates harbouring AvrLm1 in 1997–1998 and 1998–1999. This resulted in less than 13% of isolates harbouring AvrLm1 in populations being collected from rlm1 cultivars in 1999 and 2000, and contributed to the loss of efficiency of the Rlm1 resistance in the field. The present study is an illustration of one round of a `boom and bust' cycle that occurred for a pathosystem where it has never been reported before. These data and the high evolutionary potential of L. maculans are fully supportive of one pathogen species with a high risk of breaking down resistance genes in OSR and suggest that the development of integrated strategies aiming at maximising the durability of novel resistance is now a priority for this pathosystem.
Similar content being viewed by others
References
Ansan-Melayah D, Balesdent M-H, Buée M and Rouxel T (1995) Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans. Phytopathology 85: 1525-1529
Ansan-Melayah D, Rouxel T, Bertrandy J, Letarnec B, Mendes-Pereira E and Balesdent M-H (1997) Field effi-ciency of Brassica napus specific resistance correlates with Leptosphaeria maculans population structure. European Journal of Plant Pathology 103: 835-841
Ansan-Melayah D, Balesdent M-H, Delourme R, Pilet ML, Tanguy X, Renard M and Rouxel T (1998) Genes for racespecific resistance against blackleg disease in Brassica napus L. Plant Breeding 117: 373-378
Attard A, Gourgues M, Gout L, Schmit J, Roux J, Narcy JP, Balesdent MH and Rouxel T (2001) Molecular characterisation and polymorphism of MinLm1, a minisatellite from the phytopathogenic ascomycete Leptosphaeria maculans. Current Genetics 40: 54-64
Attard A, Gout L, Gourgues M, Khün ML, Schmit J, Laroche S, Ansan-Melayah D, Billault A, Cattolico L, Balesdent MH and Rouxel T (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. Molecular Plant-Microbe Interactions 15: 672-682
Badawy HMA, Hoppe HH and Koch E (1991) Differential reactions between the genus Brassica and aggressive single spore isolates of Leptosphaeria maculans. Journal of Phytopathology 131: 109-119
Balesdent M-H, Gall C, Robin P and Rouxel T (1992) Intraspecific variation in soluble mycelial protein and esterase patterns of Leptosphaeria maculans French isolates. Mycological Research 96: 677-684
Balesdent M-H, Jedryczka M, Jain L, Mendes-Pereira E, Bertrandy J and Rouxel T (1998) Conidia as a substrate for internal transcribed spacer-based PCR identification of members of the Leptosphaeria maculans species complex. Phytopathology 88: 1210-1217
Balesdent MH, 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. Phytopathology 91: 70-76
Balesdent M-H, Attard A, Kühn ML and Rouxel T (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92: 1122-1133
Brun H, Levivier S, Somda I, Ruer D, Renard M and Chèvre AM (2000) A field method for evaluating the potential durability of new resistance sources: Application to the Leptosphaeria maculans-Brassica napus pathosystem. Phytopathology 90: 961-966
CETIOM (1997) Colza d'hiver. Le contexte économique, les techniques culturales, les debouchés. Edition CETIOM, Paris, France
CETIOM (1998) Colza d'hiver. Les techniques culturales, le contexte économique. Edition CETIOM, Paris, France
CETIOM (1999) Colza d'hiver. Les techniques culturales, le contexte économique. Edition CETIOM, Paris, France
CETIOM (2001) Colza d'hiver. Les techniques culturales, le contexte économique. Edition CETIOM, Paris, France
Gall C, Balesdent MH, Robin P and Rouxel T (1994) Tetrad analysis of acid phosphatase, soluble protein patterns, and mating type in Leptosphaeria maculans. Phytopathology 84: 1299-1305
Hall R (1992) Epidemiology of blackleg of oilseed rape. Canadian Journal of Plant Pathology 14: 46-55
Kuswinanti T, Sock J and Hoppe HH (1995) Variation in virulence of aggressive isolates of Leptosphaeria maculans based on cotyledon reactions on an extended differential set. In: Proc 9th Int Rapeseed Congress (pp 1248-1250) 4-7 July 1995, Cambridge, GB
McDonald BA and Linde C (2002a) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124: 163-180
McDonald BA and Linde C (2002b) Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 40: 349-379
Mengistu A, Rimmer SR, Koch E and Williams PH (1991) Pathogenicity grouping of isolates of Leptosphaeria maculans on Brassica napus cultivars and their disease reaction profiles on rapid-cycling brassicas. Plant Disease 75: 1279-1282
Pilet ML (1999) Analyse génétique de la résistance du colza à la nécrose du collet et à la cylindrosporiose à l'aide des marqueurs moléculaires. Ph.D. Thesis, Institut National Agronomique Paris-Grignon, 182 pp
Purwantara A, Barrins JM, Cozijnsen AJ, Ades PK and Howle BJ (2000) Genetic diversity of isolates of the Leptosphaeria maculans species complex from Australia, Europe and North America using amplified fragment length polymorphism analysis. Mycological Research 104: 772-781
Rouxel T, Gall C and Balesdent MH (1994) Du polymorphisme au complexe d'espèces: Combien d'agents pathogènes sont impliqués dans la nécrose du collet du colza? Agronomie 14: 413-432
Shoemaker RA and Brun H (2001) The teleomorph of the weakly aggressive segregate of Leptosphaeria maculans. Canadian Journal of Botany 79: 412-419
Somda I, Renard M and Brun H (1996) Morphology, pathogenicity and isozyme variation amongst French isolates of Leptosphaeria maculans recovered from Brassica juncea cv. Picra. Plant Pathology 45: 1090-1098
Volke B (1999) Leptosphaeria maculans, der Erreger der Wurzelhals-und Stengelfäule an Raps: Verbreitung verschiedener Pathogenitätsgruppen in Europa, Quantifizierung des Befalls und Schadwirkung im Freiland. Ph.D. Thesis, University of Göttingen, Germany, 116 pp
West JS, Kharbanda PD, Barbetti MJ and Fitt BDL (2001) Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathology 50: 10-27
West JS, Balesdent M-H, Rouxel T, Narcy JP, Huang Y-J, Roux J, Steed JM, Fitt BDL and Schmit J (2002) Colonisation of winter oilseed rape tissues by A/Tox+ and B/Tox0 Leptosphaeria maculans (phoma stem canker) in France and England. Plant Pathology 51: 311-321
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rouxel, T., Penaud, A., Pinochet, X. et al. A 10-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 109, 871–881 (2003). https://doi.org/10.1023/A:1026189225466
Issue Date:
DOI: https://doi.org/10.1023/A:1026189225466