1,244
Views
21
CrossRef citations to date
0
Altmetric
Reviews and symposia articles/Articles de revue

Advances in understanding the Leptosphaeria maculans - Brassica pathosystem and their impact on disease management

&
Pages 149-163 | Accepted 03 Jul 2019, Published online: 16 Aug 2019

References

  • Balesdent MH, Attard A, Kuhn ML, Rouxel T. 2002. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology. 92:1122–1133.
  • Balesdent MH, Barbetti MJ, Li H, Sivasithamparam K, Gout L, Rouxel T. 2005. Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology. 95:1061–1071.
  • Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J, Eber F, Chevre AM, Leflon M, Rouxel T. 2013. The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol. 198:887–898.
  • Becker M, Zhang X, Walker P, Wan J, Millar J, Khan D, Granger M, Cavers J, Chan A, Fernando DWG, et al. 2017. Transcriptome analysis of the Brassica napus-Leptosphaeria maculans pathosystem identifies receptor, signalling and structural genes underlying plant resistance. Plant J. 90:573–586.
  • Blondeau K, Blaise F, Graille M, Kale SD, Linglin J, Ollivier B, Labarde A, Lazar N, Daverdin G, Balesdent MH, et al. 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.
  • Bousset L, Sprague SJ, Thrall PH, Barrett LG. 2018. Spatio-temporal connectivity and host resistance influence evolutionary and epidemiological dynamics of the canola pathogen Leptosphaeria maculans. Evolutionary Appl. 11:1354–1370.
  • Brun H, Chevre AM, Fitt BD, Powers S, Besnard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard M, et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185:285–299.
  • Cai X, Huang Y, Jiang D, Fitt B, Li G, Yang L. 2018. Evaluation of oilseed rape seed yield losses caused by Leptosphaeria biglobosa in central China. Eur J Plant Pathol. 150:179–190.
  • 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 Leptoaphaeria maculans, a fungal pathogen of Brassica napus. Ann Appl Biol. 164:430–444.
  • Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, et al. 2014. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science. 345:950–953.
  • Chen CY, Howlett BJ. 1996. Rapid necrosis of gaurd cells is associated with the arrest of fungal growth in leaves of Indian mustard (Brassica juncea) inoculated with avirulent isolates of Leptosphaeria maculans. Physiol Mol Plant Pathol. 48:73–81.
  • Cheng F, Wu J, Cai C, Fu L, Liang J, Borm T, Zhuang M, Zhang Y, Zhang F, Bonnema G, et al. 2016. Genome requencing and comparative variome analysis in a Brassica rapa and Brassica oleracea collection. Sci Data. 20:160119.
  • Chévre AM, Barrett 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. Theor Appl Genet. 95:1104–1111.
  • Cornelsen J, Jurke C, Rempel C. 2019. Joint meeting of the Canadian Phytopathological Society and the Quebec Society for the protection of plants, 2018. Can J Plant Pathol. 21:138–167.
  • Daverdin G, Rouxel T, Gout L, Aubertot JN, Fudal I, Meyer M, Parlange F, Carpezat J, Balesdent MH. 2012. Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathog. 8:e1003020.
  • Delourme R, Bousset L, Ermel M, Duffe P, Besnard AL, Marquer B, Fudal I, Linglin J, Chadoeuf J, Brun H. 2014. Quantitative resistance affects the speed of frequency increase but not the diversity of the virulence alleles overcoming a major resistance gene to Leptosphaeria maculans in oilseed rape. Infect Gen Evol. 27:490–499.
  • 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). Eur J Plant Pathol. 114:41–52.
  • Dutreux F, Da Silva C, d’Agata L, Couloux A, Gay E, Istace B, Lapalu N, Lemainque A, Linglin J, Noel B, et al. 2018. De novo assembly and annotation of three Leptosphaeria genomes using Oxford Nanopore MinION sequencing. Sci Data. 5:180235.
  • Eckert M, Rossall S, Selley A, Fitt B. 2010. Effects of fungicides on in vitro spore germination and mycelial growth of the phytopathogens Leptosphaeria maculans and L. biglobosa (phoma stem canker of oilseed rape). Pest Manag Sci. 66:396–405.
  • Elliott VL, Marcroft SJ, Howlett BJ, Van de Wouw AP. 2016. Gene-for-gene resistance is expressed in cotyledons, leaves and pods in the Leptosphaeria maculans-Brassica napus pathosystem but not during stem colonisation. Plant Breed. 135:200–207.
  • Fernando DWG. 2018. [updated 2018 Nov 11; accessed 2018 Nov]. http://www.australianoilseeds.com/__data/assets/pdf_file/0010/12601/Session_7-1.50pm_Dilantha_Fernando_AusCanola_2018_Aug_31.pdf.
  • 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). Eur J Plant Pathol. 114:3–15.
  • Fitt BDL, Hu BC, Li ZQ, Liu SY, Lange RM, Kharbanda PD, Butterworth MH, White RP. 2008. Strategies to prevent spread of Leptosphaeria maculans (phoma stem canker) onto oilseed rape crops in China; costs and benefits. Plant Pathol. 57:652–664.
  • Fraser M, Hwang SF, Ahmed HU, Akhavan A, Stammler G, Barton W, Strelkov SE. 2017. Sensitivity of Leptosphaeria maculans to pyraclostrobin in Alberta, Canada. Can J Plant Sci. 97:83–91.
  • Fudal I, Ross S, Brun H, Besnard AL, Ermel M, Kuhn ML, Balesdent MH, Rouxel T. 2009. Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant Microbe Interact. 22:932–941.
  • 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. Mol Plant Microbe Interact. 20:459–470.
  • Gervais J, Plissonneau C, Linglin J, Meyer M, Labadie K, Cruaud C, Fudal I, Rouxel T, Balesdent MH. 2017. Different waves of effector genes with contrasted genomic location are expressed by Leptosphaeria maculans during cotyledon and stem colonization of oilseed rape. Mol Plant Pathol. 18:1113–1126.
  • Ghanbarnia K, Fudal I, Larkan NJ, Links MG, Balesdent M, Profotova B, Fernando DWG, Rouxel T, Borhan H. 2015. Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2 using an intraspecific comparative genomics approach. Mol Plant Pathol. 16:699–709.
  • Ghanbarnia K, Ma L, Larkan NJ, Haddadi P, Fernando DWG, Borhan MH. 2018. Leptosphaeria maculans AvrLm9: a new player in the game of hide and seek with AvrLm4-7. Mol Plant Pathol. 19:1754–1764.
  • Golicz AA, Bayer PE, Barker GC, Edger PP, Kim H, Martinez PA, Chan CKK, Severn-Ellis A, McCombie WR, Parkin IA, et al. 2016. The pangenome of an agronomically important crop plant Brassica oleracea. Nature Comm. 7:13390.
  • Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, Balesdent MH, Rouxel T. 2006. Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol. 60:67–80.
  • Gout L, Kuhn ML, Vincenot L, Bernard-Samain S, Cattolico L, Barbetti M, Moreno-Rico O, Balesdent MH, Rouxel T. 2007. Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ Microbiol. 9:2978–2992.
  • Grandaubert J, Lowe RG, Soyer JL, Schoch CL, Van de Wouw AP, Fudal I, Robbertse B, Lapalu N, Links MG, Ollivier B, et al. 2014. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics. 15:891.
  • Haddadi P, Ma L, Wang H, Borhan MH. 2016. Genome-wide transcriptomic analyses provide insightes into the lifestyle transition and effector repertoire of Leptosphaeria maculans during colonization of Brassica napus seedlings. Mol Plant Pathol. 17:1196–1210.
  • Hammond KE, Lewis BG. 1987. Differential responses of oilseed rape leaves to Leptosphaeria maculans. Trans Br Mycol Soc. 88:329–333.
  • Hammond KE, Lewis BG, Musa TM. 1985. A systemic pathway in the infection of oilseed rape plants by Leptosphaeria maculans. Plant Pathol. 34:557–565.
  • Howlett BJ. 2004. Current knowledge of the Brassica napus-Leptosphaeria maculans interaction: a review. Can J Plant Pathol. 53:468–474.
  • Huang YJ, Hood JR, Eckert M, Stonard JF, Cools H, King GJ, Rossall S, Ashworth M, Fitt BDL. 2011. Effects of fungicide on growth of Leptosphaeria maculans and L. biglobosa in relation to development of phoma stem canker on oilseed rape (Brassica napus). Plant Pathol. 60:607–620.
  • Huang YJ, Qi A, King GJ, Fitt BD. 2014. Assessing quantitative resistance against Leptosphaeria maculans (phoma stem canker) in Brassica napus (oilseed rape) in young plants. PLoS One. 9:e84924.
  • Idnurm A, Urquhart AS, Vummadi DR, Chang S, Van de Wouw AP, Lõpez-Ruiz FJ. 2017. Spontaneous and CRISPR/Cas9-induced mutation of the osmosensor histidine kinase of the canola pathogen Leptosphaeria maculans. Fungal Biol Biotechnol. 4:12.
  • Kaczmarek J, Latunde-Dada AO, Irzykowski W, Cools H, Stonard JF, Brachaczek A, Jedryczka M. 2014. Molecular screening for avirulence alleles AvrLm1 and AvrLm6 in airborne inoculum of Leptosphaeria maculans and winter oilseed rape (Brassica napus) plants from Poland and the UK. J Appl Gen. 55:529–539.
  • Larkan NJ, Lydiate DJ, Parkin IA, Nelson MN, Epp DJ, Cowling WA, Rimmer SR, Borhan MH. 2013. The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 197:595–605.
  • Larkan NJ, Ma L, Borhan H. 2015. The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotechnol J. 13:983–992.
  • Lawrenson T, Shorinola O, Stacey N, Li C, Ostergaard L, Patron N, Uauy C, Harwood W. 2015. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol. 16:258.
  • Liu C, Fernando DWG, Gan YT, Kutcher HR, Peng G. 2013. Baseline sensitivity of Leptosphaeria maculans to strobilurin fungicides. Can J Plant Pathol. 35:192–199.
  • Liu Z, Akinwunmi O, Latunde-Dada AO, Hall AM, Fitt BDL. 2014. Phoma stem canker disease on oilseed rape (Brassica napus) in China is caused by Leptosphaeria biglobosa ‘brassicae’. Eur J Plant Pathol. 140:841–857.
  • 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 cultivar ‘Surpass400ʹ. Theor Appl Gen. 122:1223–1231.
  • Lowe R, Cassin A, Grandaubert J, Clark BL, Van de Wouw AP, Rouxel T, Howlett BJ. 2014. Genomes and transcriptomes of partners in plant-fungal-interactions between canola (Brassica napus) and two Leptosphaeria species. PLoS One. 9:e103098.
  • Ma L, Borhan H. 2015. The receptor-like kinase SOBIR1 interacts with Brassica napus LepR3 and is required for Leptosphaeria maculans AvrLm1-triggered immunity. Front Plant Sci. 6:933.
  • Ma L, Djavaheri M, Wang H, Larkan NJ, Haddadi P, Beynon E, Gropp G, Borhan MH. 2018. Leptosphaeria maculans effector protein AvrLm1 modulates plant immunity by enhancing MAP Kinase 9 phosphorylation. iScience. 3:177–191.
  • Marcroft SJ, Elliott 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. 63:338–350.
  • Murovec J, Gucek K, Bohanec B, Avbelj M, Jerala R. 2018. DNA-free genome editing of Brassica oleracia and B. rapa protoplasts using CRISPR-Cas9 Ribonucleoprotein complexes. Front Plant Sci. 9:1594.
  • Neik T, Barbetti M, Batley J. 2017. Current status and challenges in identifying disease resistance genes in Brassica napus. Front Plant Sci. 8:1788.
  • Nováková M, Sasek V, Trdá L, Krutinová H, Mongin T, Valentová O, Balesdent MH, Rouxel T, Burketová L. 2015. Leptosphaeria maculans effector AvrLm4-7 affects salicylic acid (SA) and ethylene (ET) signalling and hydrogen peroxide (H2O2) accumulation in Brassica napus. Mol Plant Pathol. 17:818–831.
  • Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent MH, 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. 71:851–863.
  • Petit-Houdent Y, Degrave A, Meyer M, Blaise F, Ollivier B, Marais CL, Jauneau A, Audran C, Rivas S, Veneault-Fourrey C, et al. 2019. A two genes-for-one gene interaction between Leptosphearia maculans and Brassica napus. New Phytol. 223:397–411. doi:10.1111/nph.15762
  • Plissonneau C, Blaise F, Ollivier B, Leflon M, Carpezat J, Rouxel T, Balesdent MH. 2017a. Unusual evolutionary mechanisms to escape effector-triggered immunity in the fungal phytopathogen Leptosphaeria maculans. Mol Ecol. 26:2183–2198.
  • Plissonneau C, Daverdin G, Ollivier B, Blaise F, Degrave A, Fudal I, Rouxel T, Balesdent M. 2016. A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. New Phytol. 209:1613–1624.
  • Plissonneau C, Rouxel T, Chevre AM, Van de Wouw AP, Balesdent MH. 2017b. One gene-one name: the AvrLmJ1 avirulence gene of Leptosphaeria maculans is AvrLm5. Mol Plant Pathol. 19:1012–1016.
  • Raman H, Raman R, Coombes N, Song J, Diffey S, Klilian A, Lindbeck K, Barbulescu DM, Batley J, Edwards D, et al. 2016. Genome-wide association study identified new loci for resistance to Leptosphaeria maculans in Canola. Front Plant Sci. 7:1513.
  • Raman H, Raman R, Diffey S, Qiu Y, McVittie B, Barbulescu DM, Salisbury P, Marcroft S, Delourme R. 2018. Stable quantitative resistance loci to blackleg disease in canola (Brassica napus L.) over continents. Front Plant Sci. 9:1622.
  • Rouxel T, Balesdent MH. 2017. Life, death and rebirth of avirulence effectors in a fungal pathogen of Brassica crops, Leptosphaeria maculans. New Phytol. 214:526–532.
  • 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. Nat Commun. 2:n202.
  • Rouxel T, Penaud A, Pinochet X, Brun H, Gout L, Delourme R, Schmit J, Balesdent MH. 2003. A 10-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur J Plant Pathol. 109:871–881.
  • Sasek V, Nováková M, Jindrichová B, Bóka K, Valentová O, Burketová L. 2012. Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptopshaeria maculans triggers salicylic acid and ethylene signalling in Brassica napus. Mol Plant Microbe Interact. 25:1238–1250.
  • Selker EU. 1990. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Gen. 24:579–613.
  • Selker EU, Cambareri EB, Jensen BC, Haack KR. 1987. Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell. 51:741–752.
  • Simes J. 2018. [accessed 2018 Nov]. https://www.producer.com/2018/04/new-lab-test-helps-farmers-protect-against-blackleg/.
  • Sonah H, Zhang X, Deshmukh R, Borhan H, Fernando DWG, Belanger R. 2016. Comparative transcriptomic analysis of virulence factors in Leptosphaeria maculans during compatible and incompatible interactions with canola. Front Plant Sci. 7:1784.
  • Sprague SJ, Balesdent MH, Brun H, Hayden HL, Marcroft SJ, Pinochet X, Rouxel T, Howlett BJ. 2006a. 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. 114:33–44.
  • Sprague SJ, Marcroft SJ, Hayden HL, Howlett BJ. 2006b. Major gene resistance to blackleg in Brassica napus overcome within three years of commercial production in southeastern Australia. Plant Dis. 90:190–198.
  • Sprague SJ, Marcroft SJ, Lindbeck KD, Ware AH, Khangura RK, Van de Wouw AP. 2018. Detection, prevalence and severity of upper canopy infection on mature Brassica napus plants caused by Leptosphaeria maculans. Crop Pasture Sci. 69:65–78.
  • Stuthmann DD, Leonard JJ, Miller-Garvin J. 2007. Breeding crops for durable resistance to disease. Adv Agron. 95:319–367.
  • [USDA] United States Department of Agriculture. 2019. Oilseeds: world markets and trade.
  • Van de Wouw AP, Cozijnsen AJ, Hane JK, Brunner PC, McDonald BA, Oliver RP, Howlett BJ. 2010a. Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog. 6:e1001180.
  • Van de Wouw AP, Elliott CE, Howlett BJ. 2014a. Transformation of fungal isolates with avirulence genes provides tools for identification of corresponding resistance genes in the host plant. Eu J Plant Pathol. 140:875–882.
  • Van de Wouw AP, Elliott CE, Popa KM, Idnurm A. 2019. Analysis of repeat induced point (RIP) mutations in Leptosphaeria maculans indicates variability in the RIP process between fungal species. Genetics. 211:89–104.
  • Van de Wouw AP, Elliott VL, Chang S, López-Ruiz F, Marcroft SJ, Idnurm A. 2017. Identification of isolates of the plant pathogen Leptosphaeria maculans with resistance to the triazole fungicide fluquinconazole using a novel in planta assay. PLoS One. 12:e0188106.
  • Van de Wouw AP, Howlett BJ. 2012. Estimating frequencies of virulent isolates in field populations of a plant pathogenic fungus, Leptosphaeria maculans, using high-throughput pyrosequencing. J Appl Microbiol. 113:1145–1153.
  • 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. 69:20–29.
  • Van de Wouw AP, Lowe RGT, Elliott CE, Dubois DJ, Howlett BJ. 2014b. An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars. Mol Plant Pathol. 15:523–530.
  • 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 Pathol. 58:305–313.
  • Van de Wouw AP, Marcroft SJ, Howlett BJ. 2016. Blackleg disease of canola in Australia. Crop Pasture Sci. 67:273–282.
  • Van de Wouw AP, Marcroft SJ, Ware A, Lindbeck K, Khangura R, Howlett BJ. 2014c. Breakdown of resistance to the fungal disease, blackleg, is averted in commercial canola (Brassica napus) crops in Australia. Field Crops Res. 166:144–151.
  • Van de Wouw AP, Stonard JF, Howlett BJ, West JS, Fitt BD, Atkins SD. 2010b. Determining frequencies of avirulent alleles in airborne Leptosphaeria maculans inoculum using quantitative PCR. Plant Pathol. 59:809–818.
  • 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. Nat Gen. 43:1035–1039.
  • West JS, Kharbanda PD, Barbetti M, Fitt BDL. 2001. Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathol. 50:10–27.
  • Yang H, Wu J, Tang T, Liu K, Dai C. 2017. CRISPR/Cas-9-mediated genome editing efficiently creates specific mutations at multiple loci using one sgRNA in Brassica napus. Sci Rep. 7:7289.
  • Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y, et al. 2016. The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Gen. 48:1225–1232.
  • Yu F, Gugel RK, Kutcher R, Peng G, Rimmer SR. 2013. Identification and mapping of a novel blackleg resistance locus LepR4 in the progenies from Brassica napus x B. rapa subsp. sylvestris. Theor Appl Genet. 126:307–315.
  • Yu F, Lydiate DJ, Rimmer SR. 2005. Identification of two novel genes for blackleg resistance in Brassica napus. Theor Appl Genet. 110:969–979.
  • 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.
  • Zhang L, Cai X, Wu J, Liu M, Grob S, Cheng F, Liang J, Cai C, Liu Z, Liu B, et al. 2018. Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hort Res. 5:50.
  • Zhang X, Fernando DWG. 2018. Insights into fighting against blackleg disease of Brassica napus in Canada. Crop Pasture Sci. 69:40–47.
  • Zhang X, Peng G, Kutcher HR, Balesdent MH, Delourme R, Fernando DWG. 2016. Breakdown of Rlm3 resistance in the Brassica napus-Leptosphaeria maculans pathosystem in western Canada. Eur J Plant Pathol. 145:659–674.
  • Zhang X, White RP, Demir E, Jedryczka M, Lange RM, Islam M, Li ZQ, Huang YJ, Hall AM, Zhou G, et al. 2014. Leptosphaeria spp., phoma stem canker and potential spread of L. maculans on oilseed rape crops in China. Plant Pathol. 63:598–612.
  • Zou Z, Liu F, Fernando DWG. 2018. Rapid detection of Leptosphaeria maculans avirulence gene AvrLm4-7 conferring the avirulence/virulence specificity on Brassica napus using a tetra-primer ARMS-PCR. Eur J Plant Pathol. 152:515–520.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.