The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1

New Phytologist

Volumn 197, Issue 2, 2013, Pages 595-605

  Larkan, N J ^a,b   Lydiate, D J ^a   Parkin, I A P ^a   Nelson, M N ^b   Epp, D J ^a   Cowling, W A ^b   Rimmer, S R ^a   Borhan, M H ^a  

^a SASKATOON RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Arabidopsis thaliana; Blackleg resistance; Brassica napus (canola oilseed rape); Brassica rapa; Collinearity; Leptosphaeria maculans; Receptor like protein

Indexed keywords

FUNGAL PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; VEGETABLE PROTEIN;

DICOTYLEDON; DISEASE RESISTANCE; FUNGAL DISEASE; GENETIC ANALYSIS; HOST-PATHOGEN INTERACTION; PHENOTYPE; PROTEIN; TRANSGENIC PLANT; VIRULENCE;

ARTICLE; ASCOMYCETES; CHROMOSOME MAP; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC TRANSFORMATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHENOTYPE; PHYSIOLOGY; PLANT CHROMOSOME; PLANT DISEASE; PLANT GENE; RAPESEED; SYNTENY; TRANSGENIC PLANT; VIRULENCE;

ASCOMYCOTA; BRASSICA NAPUS; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; DISEASE RESISTANCE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ASSOCIATION STUDIES; GENETIC LOCI; GENETIC MARKERS; MEMBRANE PROTEINS; PHENOTYPE; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA, MESSENGER; SYNTENY; TRANSFORMATION, GENETIC; VIRULENCE;

AUSTRALIA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA NAPUS; BRASSICA RAPA; LEPTOSPHAERIA MACULANS;

EID: 84871310889     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12043     Document Type: Article

References (73)

1. Altschul SF, Madden TL, Schaeffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
2. Ansan-Melayah D, Balesdent MH, Delourme R, Pilet ML, Tanguy X, Renard M, Rouxel T. 1998. Genes for race-specific resistance against blackleg disease in Brassica napus L. Plant Breeding 117: 373-378.
3. Arabidopsis Genome Initiative. 2000. Analysis of the genome of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
4. Balesdent MH, Attard A, Ansan-Melayah DA, 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: 70-76.
5. Balesdent MH, Attard A, Kuhn ML, Rouxel T. 2002. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92: 1122-1133.
6. Balesdent MH, 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.
7. Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Current Opinion in Plant Biology 7: 391-399.
8. Buzza G, Easton A. 2002. A new source of blackleg resistance from Brassica sylvestris. In: GCIRC Technical Meeting. Poznan, Poland. Bulletin No.18.
9. Cheung F, Trick M, Drou N, Lim YP, Park JY, Kwon SJ, Kim JA, Scott R, Pires CJ, Paterson AH et al. 2009. Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 21: 1912-1928.
10. Chèvre AM, Barret P, Eber F, Dupuy P, Brun H, Tanguy X, Renard M. 1997. Selection of stable Brassica 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 95: 1104-1111.
11. Chèvre AM, Eber F, This P, Barret P, Tanguy X, Brun H, Delseny M, Renard M. 1996. Characterization of Brassica nigra chromosomes and of blackleg resistance in B. napus-B. nigra addition lines. Plant Breeding 115: 113-118.
12. Christianson JA, Rimmer SR, Good AG, Lydiate DJ. 2006. Mapping genes for resistance to Leptosphaeria maculans in Brassica juncea. Genome 49: 30-41.
13. Covert SF, Kapoor P, Lee M-H, Briley A, Nairn CJ. 2001. Agrobacterium tumefaciens-mediated transformation of Fusarium circinatum. Mycological Research 105: 259-264.
14. Cozijnsen AJ, Popa KM, Purwantara A, Rolls BD, Howlett BJ. 2000. Genome analysis of the plant pathogenic ascomycete Leptosphaeria maculans; mapping mating type and host specificity loci. Molecular Plant Pathology 1: 293-302.
15. Crouch JH, Lewis BG, Mithen RF. 1994. The effect of A genome substitution on the resistance of Brassica napus to infection by Leptosphaeria maculans. Plant Breeding 112: 265-278.
16. Curtis MD, Grossniklaus U. 2003. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133: 462-469.
17. De Block M, De Brouwer D, Tenning P. 1989. Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the bar and neo genes in transgenic plants. Plant Physiology 91: 694-701.
18. Delourme R, Chevre AM, Brun H, Rouxel T, Balesdent MH, Dias JS, Salisbury P, Renard M, Rimmer SR. 2006. Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). European Journal of Plant Pathology 114: 41-52.
19. Delourme R, Pilet-Nayel ML, Archipiano M, Horvais R, Tanguy X, Rouxel T, Brun H, Renard M, Balesdent MH. 2004. A cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus. Phytopathology 94: 578-583.
20. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences, USA 100: 8024-8029.
21. Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang C-IA, Ayliffe MA, Kobe B, Ellis JG. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences, USA 103: 8888-8893.
22. Ferrier-Cana E, Macadre C, Sevignac M, David P, Langin T, Geffroy V. 2005. Distinct post-transcriptional modifications result into seven alternative transcripts of the CC-NBS-LRR gene JA1tr of Phaseolus vulgaris. Theoretical and Applied Genetics 110: 895-905.
23. Fitt BDL, Brun H, Barbetti MJ, Rimmer SR. 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.
24. Fritz-Laylin LK, Krishnamurthy N, Tor M, Sjolander KV, Jones JDG. 2005. Phylogenomic analysis of the Receptor-Like Proteins of rice and Arabidopsis. Plant Physiology 138: 611-623.
25. Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, Eckert MR, Cattolico L, Bernard-Samain S, Balesdent MH, Rouxel T. 2007. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Molecular Plant-Microbe Interactions 20: 459-470.
26. Gassmann W, Hinsch ME, Staskawicz BJ. 1999. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant Journal 20: 265-277.
27. Ghanbarnia K, Lydiate DJ, Rimmer SR, Li G, Kutcher HR, Larkan NJ, McVetty PBE, Fernando WGD. 2012. Genetic mapping of the Leptosphaeria maculans avirulence gene corresponding to the LepR1 resistance gene of Brassica napus. Theoretical and Applied Genetics 124: 505-513.
28. Gout L, Fudal I, Kuhn M-L, 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. Molecular Microbiology 60: 67-80.
29. Hammond-Kosack KE, Jones JDG. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8: 1773-1791.
30. Howlett BJ, Idnurm A, Pedras MSC. 2001. Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fungal Genetics and Biology 33: 1-14.
31. Hughes SL, Hunter PJ, Sharpe AG, Kearsey MJ, Lydiate DJ, Walsh JA. 2003. Genetic mapping of the novel Turnip mosaic virus resistance gene TuRB03 in Brassica napus. Theoretical and Applied Genetics 107: 1169-1173.
32. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO Journal 19: 4004-4014.
33. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789-793.
34. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444: 323-329.
35. Katagiri F, Tsuda K. 2010. Understanding the plant immune system. Molecular Plant-Microbe Interactions 23: 1531-1536.
36. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ et al. 2001. Tomato Ve disease resistance genes encode cell surface-like receptors. Proceedings of the National Academy of Sciences, USA 98: 6511-6515.
37. Koch E, Song K, Osborn TC, Williams PH. 1991. Relationship between pathogenicity and phylogeny based on restriction fragment length polymorphism in Leptosphaeria. Molecular Plant-Microbe Interactions 4: 341-349.
38. Kosambi DD. 1944. The estimation of map distances from recombination values. Annals of Eugenics 12: 172-175.
39. Kruijt M, De Kock MJD, De Wit PJGM. 2005. Receptor-like proteins involved in plant disease resistance. Molecular Plant Pathology 6: 85-97.
40. Kutcher HR, Balesdent MH, Rimmer SR, Rouxel T, Chevre AM, Delourme R, Brun H. 2010. Frequency of avirulence genes in Leptosphaeria maculans in western Canada. Canadian Journal of Plant Pathology 32: 77-85.
41. Lagercrantz U. 1998. Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150: 1217-1228.
42. Leflon M, Brun H, Eber F, Delourme R, Lucas MO, Vallée P, Ermel M, Balesdent MH, Chèvre AM. 2007. Detection, introgression and localization of genes conferring specific resistance to Leptosphaeria maculans from Brassica rapa into B. napus. Theoretical and Applied Genetics 115: 897-906.
43. Li CX, Cowling WA. 2003. Identification of a single dominant allele for resistance to blackleg in Brassica napus 'Surpass 400'. Plant Breeding 122: 485-488.
44. Li H, Kuo J, Barbetti MJ, Sivasithamparam K. 2007. Difference in the responses of stem tissues of spring-type Brassica napus cultivars with polygenic resistance and single dominant gene-based resistance to inoculation with Leptosphaeria maculans. Canadian Journal of Botany 85: 191-203.
45. Li H, Sivasithamparam K, Barbetti MJ, Kuo J. 2004. Germination and invasion by ascospores and pycnidiospores of Leptosphaeria maculans on spring-type Brassica napus canola varieties with varying susceptibility to blackleg. Journal of General Plant Pathology 70: 261-269.
46. Long Y, Wang Z, Sun Z, Fernando DWG, McVetty PBE, Li G. 2011. Identification of two blackleg resistance genes and fine mapping of one of these two genes in a Brassica napus canola cultivar 'Surpass 400'. Theoretical and Applied Genetics 122: 1223-1231.
47. Marathe R, Anandalakshmi R, Liu Y, Dinesh-Kumar SP. 2002. The tobacco mosaic virus resistance gene, N. Molecular Plant Pathology 3: 167-172.
48. Mayerhofer R, Wilde K, Mayerhofer M, Lydiate D, Bansal VK, Good AG, Parkin IAP. 2005. Complexities of chromosome landing in a highly duplicated genome: toward map-based cloning of a gene controlling blackleg resistance in Brassica napus. Genetics 171: 1977-1988.
49. McDowell JM, Woffenden BJ. 2003. Plant disease resistance genes: recent insights and potential applications. Trends in Biotechnology 21: 178-183.
50. Murray MG, Thompson WF. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8: 4321-4325.
51. Nelson MN, Lydiate DJ. 2006. New evidence from Sinapis alba L. for ancestral triplication in a crucifer genome. Genome 49: 230-238.
52. Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ. 2005. Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171: 765-781.
53. Parkin IAP, Lydiate DJ, Trick M. 2002. Assessing the level of collinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome 45: 356-366.
54. Parlange F, Daverdin G, Fudal I, Kuhn M-L, 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. Molecular Microbiology 71: 851-863.
55. Raman R, Taylor B, Marcroft S, Stiller J, Eckermann P, Coombes N, Rehman A, Lindbeck K, Luckett D, Wratten N et al. 2012. Molecular mapping of qualitative and quantitative loci for resistance to Leptosphaeria maculans causing blackleg disease in canola (Brassica napus L.). Theoretical and Applied Genetics 125: 405-418.
56. Rooney HCE, Van't Klooster JW, Van Der Hoorn RAL, Joosten MHAJ, Jones JDG, De Wit PJGM. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308: 1783-1786.
57. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S et al. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nature Communications 2: 202. doi:10.1038/ncomms1189.
58. Rouxel T, Willner E, Coudard L, Balesdent MH. 2003. Screening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions. Euphytica 133: 219-231.
59. Schornack S, Ballvora A, Gurlebeck D, Peart J, Ganal M, Baker B, Bonas U, Lahaye T. 2004. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant Journal 37: 46-60.
60. Singh RJ, ed. 2006. Genetic resources, chromosome engineering and crop improvement: oilseed crops. London, UK: CRC Press.
61. Sprague SJ, Marcroft SJ, Hayden HL, Howlett BJ. 2006. Major gene resistance to blackleg in Brassica napus overcome within three years of commercial production in Southeastern Australia. Plant Disease 90: 190-198.
62. Stam P. 1993. Construction of integrated genetic linkage maps by means of a new computer package: JOINMAP. Plant Journal 3: 739-744.
63. Szadkowski E, Eber F, Huteau V, Lodé M, Huneau C, Belcram H, Coriton O, Manzanares-Dauleux MJ, Delourme R, King GJ et al. 2010. The first meiosis of resynthesized Brassica napus, a genome blender. New Phytologist 186: 102-112.
64. Thomma BPHJ, Van Esse HP, Crous PW, De Wit PJGM. 2005. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Molecular Plant Pathology 6: 379-393.
65. Utermark J, Karlovsky P. 2008. Genetic transformation of filamentous fungi by Agrobacterium tumefaciens. In: Nature protocol exchange: Nature Publishing Group. URL: http://www.nature.com/protocolexchange/protocols/427
66. Van de Wouw AP, Cozijnsen AJ, Hane 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 Pathogens 6: e1001180. doi:10.1371/journal.ppat.1001180.
67. Van de Wouw AP, Marcroft SJ, Barbetti MJ, Hua L, Salisbury PA, Gout L, Rouxel T, Howlett BJ, Balesdent MH. 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.
68. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun J, Bancroft I, Cheng F et al. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43: 1035-1039.
69. Wulff BBH, Chakrabarti A, Jones DA. 2009. Recognitional specificity and evolution in the tomato-Cladosporium fulvum pathosystem. Molecular Plant-Microbe Interactions 22: 1191-1202.
70. Yang X, Deng F, Ramonell KM. 2012. Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity. Frontiers in Biology 7: 155-166.
71. Yu F, Lydiate DJ, Rimmer SR. 2005. Identification of two novel genes for blackleg resistance in Brassica napus. Theoretical and Applied Genetics 110: 969-979.
72. Yu F, Lydiate DJ, Rimmer SR. 2008. Identification and mapping of a third blackleg resistance locus in Brassica napus derived from B. rapa subsp. sylvestris. Genome 51: 64-72.
73. Ziolkowski PA, Kaczmarek M, Babula D, Sadowski J. 2006. Genome evolution in Arabidopsis/Brassica: conservation and divergence of ancient rearranged segments and their breakpoints. Plant Journal 47: 63-74.