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Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape)

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Abstract

To investigate whether the reported fitness cost of virulence at the AvrLm4 locus in Leptosphaeria maculans is common to other loci, near-isogenic (NI) isolates differing at AvrLm1 locus were produced in vitro. Fitness of virulent (avrLm1) or avirulent (AvrLm1) isolates on Brassica napus without the corresponding R (resistance) gene Rlm1 was investigated in controlled environment (CE) and field experiments. Results indicate that there is a measurable fitness cost for avrLm1 compared to AvrLm1 isolates in terms of number of lesions, size of lesions, distance grown through leaf tissue towards the petiole in CE experiments and systemic growth from leaf lesions to stems in field experiments. There were differences in fitness cost between the AvrLm1 and AvrLm4 loci. There was a cultivar effect on fitness cost of virulence at the AvrLm1 locus but not at the AvrLm4 locus. In CE experiments, the optimal temperature for leaf infection was greater for AvrLm4 isolates than for AvrLm1 isolates. Field experiment results suggest that on the same host AvrLm4 isolates are more fit than AvrLm1 isolates in warmer seasons. The fitness cost at the AvrLm4 locus was generally greater than at the AvrLm1 locus, suggesting that the corresponding R gene Rlm4 may be more suitable than Rlm1 for redeployment in commercial cultivars after an interval of a few years.

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References

  • Attard, A., Gout, L., Gourgues, M., 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. Molecular Plant-Microbe Interactions, 15, 672–682.

    Article  CAS  PubMed  Google Scholar 

  • Bent, A. F., & Mackey, D. (2007). Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology, 45, 399–436.

    Article  CAS  PubMed  Google Scholar 

  • Balesdent, M. H., Attard, A., Kuhn, M. L., & Rouxel, T. (2002). New avirulence genes in the phytopathologenic fungus Leptosphaeria maculans. Phytopathology, 92, 1122–1133.

    Article  CAS  PubMed  Google Scholar 

  • Balesdent, M. H., Louvard, K., Pinochet, X., & Rouxel, T. (2006). A large-scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France. European Journal of Plant Pathology, 114, 53–65.

    Article  Google Scholar 

  • Delourme, R., Chèvre, A.-M., Brun, H., et al. (2006). Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). European Journal of Plant Pathology, 114, 41–52.

    Article  Google Scholar 

  • Evans, N., Baierl, A., Semenov, M. A., Gladders, P., & Fitt, B. D. L. (2008). Range and severity of a plant disease increased by global warming. Journal of the Royal Society Interface, 5, 525–531.

    Article  Google Scholar 

  • Fitt, B. D. L., Brun, H., Barbetti, M. J., & 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, 114, 3–15.

    Article  Google Scholar 

  • Fitt, B. D. L., Hu, B. C., Li, Z. Q., et al. (2008). Strategies to prevent spread of Leptosphaeria maculans (phoma stem canker) onto oilseed rape crops in China; costs and benefits. Plant Pathology, 57, 652–664.

    Article  Google Scholar 

  • Fudal, I., Ross, S., Gout, L., et al. (2007). Heterochromatin-like regions as encological niches for avirulence gene in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Molecular Plant-Microbe Interactions, 20, 459–470.

    Article  CAS  PubMed  Google Scholar 

  • Fudal, I., Ross, S., Brun, H., Besnard, A.L., Ermel, M., Kuhn, M.L., Balesdent, M.H., & Rouxel, T. (2009). Repeat-Induced Point mutation (RIP) as an alternative mechanism of evolution towards virulence in Leptosphaeria maculans. Molecular Plant-Microbe Interactions, 22, 932–941.

  • Gout, L., Fudal, I., Kuhn, M. L., et al. (2006). Lost in the middle of nowhere: the AvrLm1 avirulence gene of the dothideomycete Leptosphaeria maculans. Molecular Biology, 60, 67–80.

    CAS  Google Scholar 

  • Gout, L., Kuhn, M. L., Vincenot, L., et al. (2007). Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environmental Microbiology, 9, 2978–2992.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Y. J., Toscano-Underwood, C., Fitt, B. D. L., et al. (2001). Effects of temperature on germination and hyphal growth from ascospores of A-group and B-group Leptosphaeria maculans (phoma stem canker of oilseed rape). Annals of Applied Biology, 139, 193–207.

    Article  Google Scholar 

  • Huang, Y. J., Fitt, B. D. L., Jedryczka, M., et al. (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, 111, 263–277.

    Article  Google Scholar 

  • Huang, Y. J., Evans, E., Li, Z. Q., et al. (2006a). Temperature and leaf wetness duration affect phenotypic expression of Rlm6-mediated resistance to Leptosphaeria maculans in Brassica napus. New Phytologist, 170, 129–141.

    Article  Google Scholar 

  • Huang, Y. J., Li, Z. Q., Evans, N., Rouxel, T., Fitt, B. D. L., & Balesdent, M. H. (2006b). Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). European Journal of Plant Pathology, 114, 77–89.

    Article  Google Scholar 

  • Huang, Y. J., Pirie, E. J., Evans, N., Delourme, R., King, G. J., & Fitt, B. D. L. (2009). Quantitative resistance to symptomless growth of Leptosphaeria maculans (phoma stem canker) in Brassica napus (oilseed rape). Plant Pathology, 58, 314–323.

    Article  Google Scholar 

  • Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 44, 323–329.

    Article  Google Scholar 

  • Leach, J. E., Vera Cruz, C. M., Bai, J., & Leung, H. (2001). Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annual Review of Phytopathology, 39, 187–224.

    Article  CAS  PubMed  Google Scholar 

  • Parlange, F., Daverdin, G., Fudal, I., et al. (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, 71, 851–863.

    Article  CAS  PubMed  Google Scholar 

  • Payne, R. W., Harding, S. A., Murray, D. A., et al. (2007). The guide to GenStat release 10, part 2: statistics. Oxford: VSN International. 1096 pages.

    Google Scholar 

  • Pietravalle, S., Lemarié, S., & van den Bosch, F. (2006). Durability of resistance and cost of virulence. European Journal of Plant Pathology, 114, 107–116.

    Article  Google Scholar 

  • Pringle, A., & Taylor, J. W. (2002). The fitness of filamentous fungi. Trends in Microbiology, 10, 475–481.

    Article  Google Scholar 

  • Rouxel, T., Penaud, A., Pinochet, X., et al. (2003). 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.

    Article  CAS  Google Scholar 

  • Sprague, S. J., Balesdent, M. H., Brun, H., et al. (2006). Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence population of Leptosphaeria maculans in France and Australia. European Journal of Plant Pathology, 114, 33–40.

    Article  Google Scholar 

  • Stachowiak, A., Olechnowicz, J., Jedryczka, M., et al. (2006). Frequency of avirulence alleles in field populations of Leptosphaeria maculans in Europe. European Journal of Plant Pathology, 114, 67–75.

    Article  Google Scholar 

  • Stergiopoulos, I., De Kock, M. J. D., Lindhout, P., & De Wit, P. J. G. M. (2007). Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions, 20, 1271–1283.

    Article  CAS  PubMed  Google Scholar 

  • Van de Wouw, A. P., Marcroft, S. J., Barbetti, M. J., et al. (2009). Dual control of avirulence in Leptosphaeria maculans towards a Brassica napus cultivar with ‘sylvestris-derived’ resistance suggests involvement of two resistance genes. Plant Pathology, 58, 305–313.

    Article  Google Scholar 

  • West, J. S., Kharbanda, P. D., Barbetti, M. J., & Fitt, B. D. L. (2001). Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathology, 50, 10–27.

    Article  Google Scholar 

  • West, J. S., Balesdent, M. H., Rouxel, T., et al. (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.

    Article  Google Scholar 

  • Yu, F. Q., Lydiate, D. J., & Rimmer, S. R. (2008). Identification and mapping of a third blackleg resistance locus in Brassica napus derived from B. rapa subsp. sylvestris. Genome, 51, 64–72.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the European Union (SECURE, QLK5-CT-2002-01813), CETIOM, the UK Biotechnology and Biological Sciences Research Council (BBSRC, IPA project, BB/E001610/1), the Department for Environment, Food and Rural Affairs (Defra), the Chadacre Agricultural Trust, the British Council and the Royal Society for supporting the work. We thank Alan Todd and Rodger White for statistical analyses of the data, Michel Renard for supplying seed of Darmor and Eurol, M. Chabirand for technical assistance, C. Montagnier for field experiment management at Versailles and J. N. Aubertot for weather data. We thank John Lucas for critical reading of the manuscript.

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  1. Zi-Qin Li

    Present address: Plant Protection Institute, Inner Mongolia Academy of Agricultural Sciences, Huhhot, 010031, China

Authors and Affiliations

  1. Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK

    Yong-Ju Huang, Zi-Qin Li, Neal Evans & Bruce D. L. Fitt

  2. INRA-UMR1290, BIOGER-CPP, Versailles Cedex, 78026, France

    Marie-Hélène Balesdent & Thierry Rouxel

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  1. Yong-Ju Huang
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  2. Marie-Hélène Balesdent
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  3. Zi-Qin Li
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  4. Neal Evans
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  5. Thierry Rouxel
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  6. Bruce D. L. Fitt
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Correspondence to Yong-Ju Huang.

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Huang, YJ., Balesdent, MH., Li, ZQ. et al. Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur J Plant Pathol 126, 279–291 (2010). https://doi.org/10.1007/s10658-009-9539-7

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  • DOI: https://doi.org/10.1007/s10658-009-9539-7

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