Frequency and genetic variability of the avirulence gene AvrLm4-7 among Leptosphaeria maculans isolates collected in Oklahoma, USA

References

• Balesdent M-H, Attard A, Ansan-Melayah D, Delourme R, Renard M, Rouxel T. 2001. Genetic control and host range of avirulence toward Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans. Phytopathology. 91(1):70–76. doi:10.1094/PHYTO.2001.91.1.70.
   PubMed Web of Science ®Google Scholar
• Balesdent M-H, Attard A, Kühn ML, Rouxel T. 2002. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology. 92(10):1122–1133. doi:10.1094/PHYTO.2002.92.10.1122.
   Web of Science ®Google Scholar
• Balesdent M-H, Barbetti M, Li H, Sivasithamparam K, Gout L, Rouxel T. 2005. Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology. 95(9):1061–1071. doi:10.1094/PHYTO-95-1061.
   PubMed Web of Science ®Google Scholar
• Blondeau K, Blaise F, Graille M, Kale SD, Linglin J, Ollivier B, Labarde A, Lazar N, Daverdin G, Balesdent MH. 2015. Crystal structure of the effector Avrlm4–7 of Leptosphaeria maculans reveals insights into its translocation into plant cells and recognition by resistance proteins. Plant J. 83:610–624. doi:10.1111/tpj.12913.
   PubMed Web of Science ®Google Scholar
• Brun H, Chèvre AM, Fit DDL, Powers S, Besnard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard F, et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185(1):285–299. doi:10.1111/j.1469-8137.2009.03049.x
   PubMed Web of Science ®Google Scholar
• Bushong J, Lofton J, Sanders H, Stamm M. 2018. Great plains canola production handbook. Kansas State Univ Agric Exp Sta and Coop Ext Serv. MF2734 42.
   Google Scholar
• Carpezat J, Bothorel S, Daverdin G, Balesdent MH, Leflon M. 2014. Use of high resolution melting analysis to genotype the avirulence AvrLm4-7 gene of Leptosphaeria maculans, a fungal pathogen of Brassica napus. Ann Appl Biol. 164(3):430–440. doi:10.1111/aab.12112.
   Web of Science ®Google Scholar
• Daverdin G, Rouxel T, Gout L, Aubertot JN, Fudal I, Meyer M, Parlange F, Carpezat J, Balesdent M-H. 2012. Genome structure and reproductive behavior influence the evolutionary potential of a fungal phytopathogen. PLOS Pathog. 8(11):e1003020. doi:10.1371/journal.ppat.1003020.
   PubMed Web of Science ®Google Scholar
• Degrave A, Wagner M, George P, Coudard L, Pinochet X, Ermil M, Gay E, Fudal I, Moreno-Rico O, Rouxel T, et al. 2021. A new avirulence gene of Leptosphaeria maculans, AvrLm14, identifies a resistance source in American broccoli (Brassica oleracea) genotypes. Mol Plant Pathol. 22(12):1599–1612. doi:10.1111/mpp.13131
   PubMed Web of Science ®Google Scholar
• Delourme R, Chevre AM, Brun H, Rouxel T, Balesdent M-H, Dias JS, Salisbury P, Renard M, Rimmer SR. 2006. Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur J Plant Pathol. 114(1):41–52. doi:10.1007/s10658-005-2108-9.
   Web of Science ®Google Scholar
• Diaz C, Cevallos F, Damicone J. 2019. Characterization of the race structure of Leptosphaeria maculans causing blackleg of winter canola in Oklahoma and Kansas. Plant Dis. 103(9):2353–2358. doi:10.1094/PDIS-01-19-0181-RE.
   PubMed Web of Science ®Google Scholar
• Dilmaghani A, Balesdent M-H, Didier J, Wu C, Davey J, Barbetti M, Li H, Moreno‐Rico O, Phillips D, Despeghel J. 2009. The Leptosphaeria maculans–Leptosphaeria biglobosa species complex in the American continent. Plant Pathol. 58(6):1044–1058. doi:10.1111/j.1365-3059.2009.02149.x.
   Web of Science ®Google Scholar
• Dwight Z, Palais R, Wittwer CT. 2011. uMelt: prediction of high-resolution melting curves and dynamic melting profiles of PCR products in a rich web application. Bioinformatics. 27(7):1019–1020. doi:10.1093/bioinformatics/btr065.
   PubMed Web of Science ®Google Scholar
• Erali M, Voelkerding KV, Wittwer CT. 2008. High resolution melting applications for clinical laboratory medicine. Exp Mol Pathol. 85(1):50–58. doi:10.1016/j.yexmp.2008.03.012.
   PubMed Web of Science ®Google Scholar
• Fernando D, Zhang X, Selin C, Zou Z, Liban SH, McLaren DL, Kubinec A, Parks PS, Rashid MH, Padmathilake KR. 2018. A six-year investigation of the dynamics of avirulence allele profiles, blackleg incidence, and mating type alleles of Leptosphaeria maculans populations associated with canola crops in Manitoba, Canada. Plant Dis. 102(4):790–798. doi:10.1094/PDIS-05-17-0630-RE.
   PubMed Web of Science ®Google Scholar
• Flor HH. 1971. Current status of the gene-for-gene concept. Annu Rev Phytopathol. 9(1):275–296. doi:10.1146/annurev.py.09.090171.001423.
   Web of Science ®Google Scholar
• Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, Eckert MR, Cattolico L, Bernard-Samain S, Balesdent M-H, Rouxel T. 2007. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol Plant Microbe Interact. 20(4):459–470. doi:10.1094/MPMI-20-4-0459.
   PubMed Web of Science ®Google Scholar
• Ghanbarnia K, Fudal I, Larkan NJ, Links MG, Balesdent M-H, Profotova B, Borhan MH. 2015. Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2 using an intraspecific comparative genomics approach. Mol Plant Pathol. 16(7):699–709. doi:10.1111/mpp.12228.
   PubMed Web of Science ®Google Scholar
• Ghanbarnia K, Ma L, Larkan NJ, Haddadi P, Fernando D, Borhan MH. 2018. Leptosphaeria maculans AvrLm9: a new player in the game of hide and seek with AvrLm4‐7. Mol Plant Pathol. 19(7):1754–1764. doi:10.1111/mpp.12658.
   PubMed Web of Science ®Google Scholar
• Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, Balesdent M-H, Rouxel T. 2006. Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol. 60(1):67–80. doi:10.1111/j.1365-2958.2006.05076.x.
   PubMed Web of Science ®Google Scholar
• Hammond-Kosack KE, Jones JD. 1997. Plant disease resistance genes. Annu Rev Plant Phys. 48(1):575–607. doi:10.1146/annurev.arplant.48.1.575.
   Google Scholar
• Jones JD, Dangl JL. 2006. The plant immune system. Nature. 444(7117):323–329. doi:10.1038/nature05286.
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 33:1870–1874. doi:10.1093/molbev/msw054.
   PubMed Web of Science ®Google Scholar
• Kutcher HR, Yu F, Brun H. 2010. Improving blackleg disease management of Brassica napus from knowledge of genetic interactions with Leptosphaeria maculans †. Can J Plant Pathol. 32(1):29–34. doi:10.1080/07060661003620961.
   Web of Science ®Google Scholar
• Larkan NJ, Lydiate DJ, Yu F, Rimmer SR, Borhan MH. 2014. Colocalisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10. BMC Plant Biol. 14(1):387–396. doi:10.1186/s12870-014-0387-z.
   PubMedGoogle Scholar
• Larkan NJ, Yu F, Lydiate DJ, Rimmer SR, Borhan MH. 2016. Single R gene introgression lines for accurate dissection of the Brassica–Leptosphaeria pathosystem. Front Plant Sci. 7:1771. doi:10.3389/fpls.2016.01771.
   PubMed Web of Science ®Google Scholar
• Larkan NJ, Ma L, Haddadi P, Buchwaldt M, Parkin I, Djavaheri M, Borhan MH. 2020. The Brassica napus wall-associated kinase-like (WAKL) gene Rlm9 provides race-specific blackleg resistance. Plant J. 104(4):892–900. doi:10.1111/tpj.14966.
   PubMed Web of Science ®Google Scholar
• Marcroft SJ, Elliot VL, Cozijnsen AJ, Salisbury PA, Howlett BJ, Van de Wouw AP. 2012. Identifying resistance genes to Leptosphaeria maculans in Australian Brassica napus cultivars based on reactions to isolates with known avirulence genotypes. Crop Pasture Sci. 63(4):338–350. doi:10.1071/CP11341.
   Web of Science ®Google Scholar
• Neik TX, Ghanbarnia K, Ollivier B, Scheben A, Severn-Ellis A, Larkan NJ, Haddadi P, Fernando WGD, Rouxel T, Batley J, et al. 2022. Two independent approaches converge to the cloning of a new Leptosphaeria maculans avirulence effector gene, AvrLmS-Lep2. Mol. Plant. Pathol. 23(5):733–748. doi:10.1111/mpp.13194.
   Google Scholar
• Orquera-Tornakian GK, Garrido P, Kronmiller B, Hunger R, Tyler BM, Garzon CD, Marek SM. 2017. Identification and characterization of simple sequence repeats (SSRs) for population studies of Puccinia novopanici. J Microbiol Meth. 139:113–122. doi:10.1016/j.mimet.2017.04.011.
   PubMed Web of Science ®Google Scholar
• Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent M-H, Blaise F, Grezes-Besset B, 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. Mol Microbiol. 71(4):851–863. doi:10.1111/j.1365-2958.2008.06547.x.
   PubMed Web of Science ®Google Scholar
• Patel DA, Zander M, Van de Wouw AP, Mason AS, Edwards D, Batley J. 2015. Population diversity of Leptosphaeria maculans in Australia. Int J Biol. 7(3):18–36. doi:10.5539/ijb.v7n3p18.
   Google Scholar
• Petit‐Houdenot Y, Degrave A, Meyer M, Blaise F, Ollivier B, Marais C-L, Jauneau A, Audran C, Rivas S, Veneault-Fourrey C, et al. 2019. A two genes–for–one gene interaction between Leptosphaeria maculans and Brassica napus. New Phytol. 223:397–411. doi:10.1111/nph.15762.
   PubMed Web of Science ®Google Scholar
• Plissonneau C, Daverdin G, Ollivier B, Blaise F, Degrave A, Fudal I, Rouxel T, Balesdent M-H. 2016. A game of hide and seek between avirulence genes AvrLm4‐7 and AvrLm3 in Leptosphaeria maculans. New Phytol. 209(4):1613–1624. doi:10.1111/nph.13736.
   PubMed Web of Science ®Google Scholar
• Plissonneau C, Blaise F, Ollivier B, Lefton M, Carpezat J, Rouxel T, Balesdent M-H. 2017. Unusual evolutionary mechanisms to escape effector-triggered immunity in the fungal phytopathogen Leptosphaeria maculans. Mol Ecol. 26(7):2183–2198. doi:10.1111/mec.14046.
   PubMed Web of Science ®Google Scholar
• Plissonneau C, Rouxel T, Chèvre AM, Van De Wouw AP, Balesdent M-H. 2018. One gene-one name: the AvrLmJ1 avirulence gene of Leptosphaeria maculans is AvrLm5. Mol Plant Pathol. 19(4):1012–1016. doi:10.1111/mpp.12574.
   PubMed Web of Science ®Google Scholar
• Rife C, Auld D, Sunderman H, Heer W, Baltensperger D, Nelson L, Johnson D, Bordovsky D, Minor H. 2001. Registration of “Wichita” rapeseed. Crop Sci. 41(1):263–264. doi:10.2135/cropsci2001.411263-ax.
   Web of Science ®Google Scholar
• Rouxel T, Willner E, Coudard L, Balesdent M-H. 2003. Screening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions. Euphytica. 133(2):219–231. doi:10.1023/A:1025597622490.
   Web of Science ®Google Scholar
• Rouxel T, Balesdent M-H. 2005. The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol Plant Pathol. 6(3):225–241. doi:10.1111/j.1364-3703.2005.00282.x.
   PubMed Web of Science ®Google Scholar
• Rouxel T, Balesdent M-H. 2017. Life, death and rebirth of avirulence effectors in a fungal pathogen of Brassica crops, Leptosphaeria maculans. New Phytol. 214(2):526–532. doi:10.1111/nph.14411.
   PubMed Web of Science ®Google Scholar
• Skeeles LE, Fleming JL, Mahaler KL, Toland AE. 2013. The impact of 3’ UTR variants on differential expression of candidate cancer susceptibility genes. PloS one. 8(3):e58609. doi:10.1371/journal.pone.0058609.
   PubMed Web of Science ®Google Scholar
• Sprague SJ, Balesdent M-H, Brun H, Hayden HL, Marcroft SJ, Pinochet X, Rouxel T, Howlett BJ. 2006. Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur J Plant Pathol. 114(1):33–40. doi:10.1007/s10658-005-3683-5.
   Web of Science ®Google Scholar
• Stachowiak A, Olechnowicz J, Jedryczka M, Rouxel T, Balesdent MH, Happstadius I, Gladders P, Latunde-Dada A, Evans N. 2006. Frequency of avirulence alleles in field populations of Leptosphaeria maculans in Europe. Eur J Plant Pathol. 114(1):67–75. doi:10.1007/s10658-005-2931-z.
   Web of Science ®Google Scholar
• Stamm M, Berrada A, Buck J, Cabot P, Claassen M, Cramer G, Dooley S, Godsey C, Heer W, Holman J. 2012. Registration of “Riley” winter canola. J Plant Regist. 6(3):243–245. doi:10.3198/jpr2011.10.0555crc.
   Web of Science ®Google Scholar
• Van de Wouw AP, Cozijnsen AJ, Hayne JK, Brunner PC, McDonald BA, Oliver RP, Howlett BJ. 2010. Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog. 6(11):e1001180. doi:10.1371/journal.ppat.1001180.
   PubMed Web of Science ®Google Scholar
• Van de Wouw AP, Howlet BJ. 2012. Estimating frequencies of virulent isolates in field populations of a plant pathogenic fungus, Leptosphaeria maculans, using high-throughput pyrosequencing. J Appl Microbiol. 113(5):1145–1153. doi:10.1111/j.1365-2672.2012.05413.x.
   PubMed Web of Science ®Google Scholar
• Van de Wouw AP, Howlett BJ, Idnurm A. 2018. Changes in allele frequencies of avirulence genes in the blackleg fungus, Leptosphaeria maculans, over two decades in Australia. Crop Pasture Sci. 69(1):20–29. doi:10.1071/CP16411.
   Web of Science ®Google Scholar
• Weising K, Atkinson RG, Gardner RC. 1995. Genomic fingerprinting by microsatellite-primed PCR: a critical evaluation. Genome Res. 4(5):249–255. doi:10.1101/gr.4.5.249.
   Google Scholar
• West JS, Kharbanda PD, Barbetti MJ, Fitt BD. 2001. Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathol. 50(1):10–27. doi:10.1046/j.1365-3059.2001.00546.x.
   Web of Science ®Google Scholar
• Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ. 2003. High-resolution genotyping by amplicon melting analysis using Lcgreen. Clinl Chem. 49:853–860.
   PubMed Web of Science ®Google Scholar
• Wittwer CT. 2009. High‐resolution DNA melting analysis: advancements and limitations. Hum Mutat. 30(6):857–859. doi:10.1002/humu.20951.
   PubMed Web of Science ®Google Scholar
• Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31(13):3406–3415. doi:10.1093/nar/gkg595.
   PubMed Web of Science ®Google Scholar