Abstract
Near-isogenic isolates of Leptosphaeria maculans differing at the AvrLm4 avirulence locus (AvrLm4 or avrLm4) were produced in vitro. Methods for inoculation of leaves of oilseed rape with ascospores or conidia were compared. The ‘ascospore shower’ inoculation was the most efficient method for use when inoculum is limited (e.g. ascospores produced in vitro). It was used in controlled environments to compare fitness of AvrLm4 and avrLm4 isolates at 5, 10, 15, 20 or 25 °C on leaves of oilseed rape cultivars Eurol and Darmor lacking the resistance gene Rlm4, which corresponds to AvrLm4. At all temperatures tested, AvrLm4 ascospores produced more lesions than avrLm4 ascospores. The diameters of lesions produced by AvrLm4 ascospores were greater than those of lesions produced by avrLm4 ascospores. At 15–20 °C, more lesions initiated by AvrLm4 ascospores produced pycnidia than did lesions initiated by avrLm4 ascospores. However, there were no differences between AvrLm4 and avrLm4 isolates in incubation period (from inoculation to appearance of lesions) or rate of mycelial growth in leaves from lesions towards the stems. In field experiments with winter oilseed rape cultivars lacking Rlm4, the frequency of AvrLm4 isolates increased from 5.7% at the phoma leaf lesion stage (autumn) to 20.5% at the stem canker stage (summer) during 2002/2003 and from 7.9 to 11.5% during 2003/2004 growing seasons. Results of controlled environment and field experiments indicate that avrLm4 isolates have a fitness cost compared to AvrLm4 isolates.
Similar content being viewed by others
Abbreviations
- AFLP:
-
amplified fragment length polymorphism
- BC:
-
back-cross
- cv:
-
cultivar
- GS:
-
growth stage
- NI:
-
near isogenic
References
A Attard L Gout M Gourgues ML Kuhn J Schmit S Laroche D Ansan-Melayah A Billault L Cattolico MH Balesdent T Rouxel (2002) ArticleTitleAnalysis 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 Occurrence Handle12118883 Occurrence Handle1:CAS:528:DC%2BD38Xlt1Wku7w%3D Occurrence Handle10.1094/MPMI.2002.15.7.672
D Ansan-Melayah MH Balesdent R Delourme ML Pilet X Tanguy M Renard T Rouxel (1998) ArticleTitleGenes for race-specific resistance against blackleg disease in Brassica napus L Plant Breeding 117 373–378 Occurrence Handle10.1111/j.1439-0523.1998.tb01956.x
MH Balesdent A Attard D Ansan-Melayah R Delourme M Renard T Rouxel (2001) ArticleTitleGenetic control and host range of avirulence towards Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans Phytopathology 91 70–76 Occurrence Handle18944280 Occurrence Handle1:STN:280:DC%2BD1cjjslOhsA%3D%3D
MH Balesdent A Attard ML Kühn T Rouxel (2002) ArticleTitleNew avirulence genes in the phytopathologenic fungus Leptosphaeria maculans Phytopathology 92 1122–1133 Occurrence Handle1:CAS:528:DC%2BD38XotlGitrg%3D Occurrence Handle18944223
MH Balesdent K Louvard X Pinochet T Rouxel (2006) ArticleTitleA large-scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France European Journal of Plant Pathology 114 53–65 Occurrence Handle10.1007/s10658-005-2104-0
JE Biddulph BDL Fitt PK Leech SJ Welham P Gladders (1999) ArticleTitleEffects of temperature and wetness duration on infection of oilseed rape leaves by ascospores of Leptosphaeria maculans (stem canker) European Journal of Plant Pathology 105 769–781 Occurrence Handle10.1023/A:1008727530088
H Brun S Levivier D Ruer I Somda AM Chèvre M Renard (2000) ArticleTitleA field method for evaluating the potential duability of new resistance sources: application to the Leptosphaeria maculans/Brassica napus pathosystem Phytopathology 90 961–966 Occurrence Handle18944519 Occurrence Handle1:STN:280:DC%2BD1cjjslyitA%3D%3D
H Brun D Ruer S Levivier I Somda AM Chèvre M Renard (2001) ArticleTitlePresence in Leptosphaeria maculans populations of isolates virulent on resistance introgressed into Brassica napus from the B. nigra B genome Plant Pathology 50 69–74 Occurrence Handle10.1046/j.1365-3059.2001.00535.x
AJ Cozijnsen BJ Howlett (2003) ArticleTitleCharacterisation of the mating-type locus of the plant pathogenic ascomycete Leptosphaeria maculans Current Genetics 43 351–357 Occurrence Handle10.1007/s00294-003-0391-6 Occurrence Handle12679880 Occurrence Handle1:CAS:528:DC%2BD3sXltFCntLk%3D
JF Crow (1986) Basic Concepts in Population, Quantitative Evolutionary Genetics Academic New York 273
R Delourme ML Pilet-Nayel M Archipiano R Horvais X Tanguy T Rouxel H Brun M Renard MH Balesdent (2004) ArticleTitleA cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus Phytopathology 94 578–583 Occurrence Handle1:CAS:528:DC%2BD2cXltFynurs%3D Occurrence Handle18943482
R Delourme A-M Chèvre H Brun T Rouxel MH Balesdent JS Dias PA Salisbury M Renard SR Rimmer (2006) ArticleTitleMajor gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus) European Journal of Plant Pathology 114 41–52 Occurrence Handle10.1007/s10658-005-2108-9
ML Farman SA Leong (1998) ArticleTitleChromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: discrepancy between the physical and genetic maps Genetics 150 1049–1058 Occurrence Handle9799257 Occurrence Handle1:CAS:528:DyaK1cXnsFCnt7Y%3D
BDL Fitt H Brun MJ Barbetti SR Rimmer (2006) ArticleTitleWorld-wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus) European Journal of Plant Pathology 114 3–15 Occurrence Handle10.1007/s10658-005-2233-5
C Gall MH Balesdent P Robin T Rouxel (1994) ArticleTitleTetrad analysis of acid phosphatase, soluble protein patterns and mating type in Leptosphaeria maculans Phytopathology 84 1299–1305 Occurrence Handle1:CAS:528:DyaK2MXis1yjsb0%3D
P Gladders TM Musa (1980) ArticleTitleObservations on the epidemiology of Leptosphaeria maculans stem canker in winter oilseed rape Plant Pathology 29 28–37
YJ Huang C Toscano-Underwood BDL Fitt AD Todd JS West B Koopmann MH Balesdent (2001) ArticleTitleEffects 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
YJ Huang C Toscano-Underwood BDL Fitt XJ Hu AM Hall (2003) ArticleTitleEffects of temperature on ascospore germination and penetration of oilseed rape (Brassica napus) leaves by A-group or B-group Leptosphaeria maculans (phoma stem canker) Plant Pathology 52 245–255 Occurrence Handle10.1046/j.1365-3059.2003.00813.x
YJ Huang BDL Fitt M Jedryczka S Dakowska JS West P Gladders JM Steed ZQ Li (2005) ArticleTitlePatterns 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 Occurrence Handle10.1007/s10658-004-4421-0
ML Kuhn L Gout BJ Howlett D Melayah M Meyer MH Balesdent T Rouxel (2006) ArticleTitleGenetic linkage maps and genomic organization in Leptosphaeria maculans European Journal of Plant Pathology 114 17–31 Occurrence Handle10.1007/s10658-005-3168-6 Occurrence Handle1:CAS:528:DC%2BD2MXhtlSjtLbM
JE Leach CM Vera Cruz J Bai H Leung (2001) ArticleTitlePathogen fitness penalty as a predictor of durability of disease resistance genes Annual Review of Phytopathology 39 187–224 Occurrence Handle10.1146/annurev.phyto.39.1.187 Occurrence Handle11701864 Occurrence Handle1:CAS:528:DC%2BD3MXmvVygs7s%3D
H Li K Sivasithamparam MJ Barbetti (2003) ArticleTitleBreakdown of a Brassica rapa subsp. sylvestris single dominant blackleg resistance gene in B. napus rapeseed by Leptosphaeria maculans field isolates in Australia Plant Disease 87 752
A Mengistu RS Rimmer PH Williams (1993) ArticleTitleProtocols for in vitro sporulation, ascospore release, sexual mating, and fertility in crosses of Leptosphaeria maculans Plant Disease 77 538–540 Occurrence Handle10.1094/PD-77-0538
M Meyer F Blaise E Rémy L Zhou C Tourneur JP Narcy T Rouxel MH Balesdent (2004) ArticleTitleAgrobacterium tumefaciens-mediated transformation of Leptosphaeriamaculans International Organisation for Biological Control Bulletin 27 179–192
RW Payne PW Lane PGN Digby SA Harding PK Leech GW Morgan AD Todd R Thompson G Tunnicliffe Wilson SJ Welham RP White (1993) Genstat 5 Release 3 Reference Manual Clarendon Press Oxford, UK
S Pietravalle S Lemarié F Bosch Particlevan den (2005) ArticleTitleDurability of resistance and cost of virulence European Journal of Plant Pathology 114 107–116 Occurrence Handle10.1007/s10658-005-3479-7
A Pringle JW Taylor (2002) ArticleTitleThe fitness of filamentous fungi Trends in Microbiology 10 475–481 Occurrence Handle10.1016/S0966-842X(02)02447-2
T Rouxel A Penaud X Pinochet H Brun L Gout R Delourme J Schmit MH Balesdent (2003a) ArticleTitleA 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 Occurrence Handle10.1023/A:1026189225466 Occurrence Handle1:CAS:528:DC%2BD3sXotV2jsbg%3D
T Rouxel E Willner L Coudard MH Balesdent (2003b) ArticleTitleScreening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions Euphytica 133 219–231 Occurrence Handle10.1023/A:1025597622490 Occurrence Handle1:CAS:528:DC%2BD3sXmvVaisbg%3D
SJ Sprague MH Balesdent H Brun HL Hayden SJ Marcroft X Pinochet T Rouxel BJ Howlett (2006) ArticleTitleMajor gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia European Journal of Plant Pathology 114 33–40 Occurrence Handle10.1007/s10658-005-3683-5
A Stachowiak J Olechnowicz M Jedryczka T Rouxel MH Balesdent I Happstadius P Gladders A Latunde-Dada N Evans (2006) ArticleTitleFrequency of avirulence alleles in field populations of Leptosphaeria maculans in Europe European Journal of Plant Pathology 114 67–75 Occurrence Handle10.1007/s10658-005-2931-z
R Sylvester-Bradley RJ Makepeace (1985) ArticleTitleRevision of a code for stages of development in oilseed rape (Brassica napus L.) Aspects of Applied Biology: Field trials methods and data handling 10 395–400
C Toscano-Underwood JS West BDL Fitt AD Todd M Jedryczka (2001) ArticleTitleDevelopment of phoma lesions on oilseed rape leaves inoculated with ascospores of A-group or B-group Leptosphaeria maculans (stem canker) at different temperatures and wetness durations Plant Pathology 50 28–41 Occurrence Handle10.1046/j.1365-3059.2001.00526.x
CM Vera Cruz J Bai I Oña H Leung RJ Nelson T-W Mew JE Leach (2000) ArticleTitlePredicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation Proceedings of the National Academy of Sciences of the USA 97 13500–13505 Occurrence Handle10.1073/pnas.250271997 Occurrence Handle11095723 Occurrence Handle1:STN:280:DC%2BD3M%2FosFCruw%3D%3D
JS West JE Biddulph BDL Fitt P Gladders (1999) ArticleTitleEpidemiology of Leptosphaeria maculans in relation to forecasting stem canker severity on winter oilseed rape in the UK Annals of Applied Biology 135 535–546 Occurrence Handle10.1111/j.1744-7348.1999.tb00885.x
JS West PD Kharbanda MJ Barbetti BDL Fitt (2001) ArticleTitleEpidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe Plant Pathology 50 10–27 Occurrence Handle10.1046/j.1365-3059.2001.00546.x
JS West MH Balesdent T Rouxel JP Narcy YJ Huang J Roux JM Steed BDL Fitt J Schmit (2002) ArticleTitleColonisation of winter oilseed rape tissues by A/Tox+ and B/Tox0 Leptosphaeria maculans (phoma stem canker) in France and England Plant Pathology 51 311–21 Occurrence Handle10.1046/j.1365-3059.2002.00689.x
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Huang, Y.J., Li, Z.Q., Evans, N. et al. Fitness Cost Associated with Loss of the AvrLm4 Avirulence Function in Leptosphaeria maculans (Phoma Stem Canker of Oilseed Rape). Eur J Plant Pathol 114, 77–89 (2006). https://doi.org/10.1007/s10658-005-2643-4
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10658-005-2643-4