Candidate Rlm6 resistance genes against Leptosphaeria. maculans identified through a genome-wide association study in Brassica juncea (L.) Czern.
Journal
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
17
11
2020
accepted:
23
02
2021
pubmed:
27
3
2021
medline:
23
9
2021
entrez:
26
3
2021
Statut:
ppublish
Résumé
One hundred and sixty-seven B. juncea varieties were genotyped on the 90K Brassica assay (42,914 SNPs), which led to the identification of sixteen candidate genes for Rlm6. Brassica species are at high risk of severe crop loss due to pathogens, especially Leptosphaeria maculans (the causal agent of blackleg). Brassica juncea (L.) Czern is an important germplasm resource for canola improvement, due to its good agronomic traits, such as heat and drought tolerance and high blackleg resistance. The present study is the first using genome-wide association studies to identify candidate genes for blackleg resistance in B. juncea based on genome-wide SNPs obtained from the Illumina Infinium 90 K Brassica SNP array. The verification of Rlm6 in B. juncea was performed through a cotyledon infection test. Genotyping 42,914 single nucleotide polymorphisms (SNPs) in a panel of 167 B. juncea lines revealed a total of seven SNPs significantly associated with Rlm6 on chromosomes A07 and B04 in B. juncea. Furthermore, 16 candidate Rlm6 genes were found in these regions, defined as nucleotide binding site leucine-rich-repeat (NLR), leucine-rich repeat RLK (LRR-RLK) and LRR-RLP genes. This study will give insights into the blackleg resistance in B. juncea and facilitate identification of functional blackleg resistance genes which can be used in Brassica breeding.
Identifiants
pubmed: 33768283
doi: 10.1007/s00122-021-03803-4
pii: 10.1007/s00122-021-03803-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2035-2050Subventions
Organisme : Australian Research Council (AU)
ID : DP1601004497
Organisme : Australian Research Council (AU)
ID : FT130100604
Organisme : Australian Research Council
ID : LP160100030
Références
Aitken K, Farmer A, Berkman P, Muller C, Wei X, Demano E, Jackson P, Magwire M, Dietrich B, Kota R (2017) Generation of a 345K sugarcane SNP chip. Int Sugar J 119:816–820
Akhatar J, Singh MP, Sharma A, Kaur H, Kaur N, Sharma S, Bharti B, Sardana VK, Banga SS (2020) Association mapping of seed quality traits under varying conditions of nitrogen application in Brassica juncea L. Czern Coss Front Genet 11:744. https://doi.org/10.3389/fgene.2020.00744
doi: 10.3389/fgene.2020.00744
pubmed: 33088279
Angadi SV, Cutforth HW, Miller PR, McConkey BG, Entz MH, Brandt SA, Volkmar KM (2000) Response of three Brassica species to high temperature stress during reproductive growth. Can J Plant Sci 80:693–701. https://doi.org/10.4141/P99-152
doi: 10.4141/P99-152
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 Breed 117:373–378. https://doi.org/10.1111/j.1439-0523.1998.tb01956.x
doi: 10.1111/j.1439-0523.1998.tb01956.x
Asimit J, Zeggini E (2010) Rare variant association analysis methods for complex traits. Annu Rev Genet 44:293–308. https://doi.org/10.1146/annurev-genet-102209-163421
doi: 10.1146/annurev-genet-102209-163421
pubmed: 21047260
Balesdent MH, Attard A, Kühn ML, Rouxel T (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathol 92:1122–1133. https://doi.org/10.1094/PHYTO.2002.92.10.1122
doi: 10.1094/PHYTO.2002.92.10.1122
Barret P, Guérif J, Reynoird JP, Delourme R, Eber F, Renard M, Chèvre AM (1998) Selection of stable Brassica napus-Brassica juncea recombinant lines resistant to blackleg (Leptosphaeria maculans). 2. A “to and fro” strategy to localise and characterise interspecific introgressions on the B. napus genome. Theor Appl Genet 96:1097–1103. https://doi.org/10.1007/s001220050844
doi: 10.1007/s001220050844
Bartoli C, Roux F (2017) Genome-wide association studies in plant pathosystems: toward an ecological genomics approach. Front Plant Sci 8:763. https://doi.org/10.3389/fpls.2017.00763
doi: 10.3389/fpls.2017.00763
pubmed: 28588588
pmcid: 5441063
Brachi B, Morris GP, Borevitz JO (2011) Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol 12:232. https://doi.org/10.1186/gb-2011-12-10-232
doi: 10.1186/gb-2011-12-10-232
pubmed: 22035733
pmcid: 3333769
Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B (2014) Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 345:950–953. https://doi.org/10.1126/science.1253435
doi: 10.1126/science.1253435
pubmed: 25146293
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 Breed 115:113–118. https://doi.org/10.1111/j.1439-0523.1996.tb00884.x
doi: 10.1111/j.1439-0523.1996.tb00884.x
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, hromosomal and genomic origin of the introgression. Theor Appl Genet 95:1104–1111. https://doi.org/10.1007/s001220050669
doi: 10.1007/s001220050669
Chèvre AM, Brun H, Eber F, Letanneur JC, Vallee P, Ermel M, Glais I, Li H, Sivasithamparam K, Barbetti MJ (2008) Stabilization of resistance to Leptosphaeria maculans in Brassica napus-B. juncea recombinant lines and its introgression into spring-type Brassica napus. Plant Dis 92:1208–1214. https://doi.org/10.1094/PDIS-92-8-1208
doi: 10.1094/PDIS-92-8-1208
pubmed: 30769494
Christianson JA, Rimmer SR, Good AG, Lydiate DJ (2006) Mapping genes for resistance to Leptosphaeria maculans in Brassica juncea. Genome 49:30–41. https://doi.org/10.1139/g05-085
doi: 10.1139/g05-085
pubmed: 16462899
Clarke WE, Higgins EE, Plieske J, Wieseke R, Sidebottom C, Khedikar Y, Batley J, Edwards D, Meng J, Li R, Lawley CT, Pauquet J, Laga B, Cheung W, Iniguez-Luy F, Dyrszka E, Rae S, Stich B, Snowdon RJ, Sharpe AG, Ganal MW, Parkin IAP (2016) A high-density SNP genotyping array for Brassica napus and its ancestral diploid species based on optimised selection of single-locus markers in the allotetraploid genome. Theor Appl Genet 129:1887–1899. https://doi.org/10.1007/s00122-016-2746-7
doi: 10.1007/s00122-016-2746-7
pubmed: 27364915
pmcid: 5025514
Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833. https://doi.org/10.1038/35081161
doi: 10.1038/35081161
pubmed: 11459065
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. https://doi.org/10.1094/PHYTO.2004.94.6.578
doi: 10.1094/PHYTO.2004.94.6.578
pubmed: 18943482
Delourme R, Chèvre 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. https://doi.org/10.1007/s10658-005-2108-9
doi: 10.1007/s10658-005-2108-9
Delourme R, Barbetti MJ, Snowdon R, Zhao J, Manazanares-Dauleux M (2011) Genetics and genomics of disease resistance. In: Edwards D, Batley J, Parkin I, Kole C (eds) Genetics, genomics and breeding of oilseed Brassicas. Science Publishers, Boca Raton, pp 276–318
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 Genet Evol 27:490–499. https://doi.org/10.1016/j.meegid.2013.12.019
doi: 10.1016/j.meegid.2013.12.019
pubmed: 24394446
Elliott VL, Marcroft SJ, Norton RM, Salisbury PA (2011) Reaction of Brassica juncea to Australian isolates of Leptosphaeria maculans and Leptosphaeria biglobosa “canadensis.” Can J Plant Pathol 33:38–48. https://doi.org/10.1080/07060661.2010.531544
doi: 10.1080/07060661.2010.531544
Ellis J, Dodds P, Tony P (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284. https://doi.org/10.1016/S1369-5266(00)00080-7
doi: 10.1016/S1369-5266(00)00080-7
pubmed: 10873844
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. https://doi.org/10.1371/journal.pone.0019379
doi: 10.1371/journal.pone.0019379
pubmed: 21573248
pmcid: 3087801
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. https://doi.org/10.1007/s10658-005-2233-5
doi: 10.1007/s10658-005-2233-5
Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296. https://doi.org/10.1146/annurev.py.09.090171.001423
doi: 10.1146/annurev.py.09.090171.001423
Fu F, Zhang X, Liu F, Peng G, Yu F, Fernando D (2020) Identification of resistance loci in Chinese and Canadian canola/rapeseed varieties against Leptosphaeria maculans based on genome-wide association studies. BMC Genom 21:501. https://doi.org/10.1186/s12864-020-06893-4
doi: 10.1186/s12864-020-06893-4
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. https://doi.org/10.1094/MPMI-20-4-0459
doi: 10.1094/MPMI-20-4-0459
pubmed: 17427816
Gacek K, Bayer PE, Bartkowiak-Broda I, Szala L, Bocianowski J, Edwards D, Batley J (2017) Genome-wide association study of genetic control of seed fatty acid biosynthesis in Brassica napus. Front Plant Sci 7:2062. https://doi.org/10.3389/fpls.2016.02062
doi: 10.3389/fpls.2016.02062
pubmed: 28163710
pmcid: 5247464
Ghanbarnia K, Lydiate DJ, Rimmer SR, Li G, Kutcher HR, Larkan NJ, McVetty PB, Fernando WG (2012) Genetic mapping of the Leptosphaeria maculans avirulence gene corresponding to the LepR1 resistance gene of Brassica napus. Theor Appl Genet 124:505–513. https://doi.org/10.1007/s00122-011-1724-3
doi: 10.1007/s00122-011-1724-3
pubmed: 22038486
Ghanbarnia K, Fudal I, Larkan NJ, Links MG, Balesdent MH, Profotova B, Fernando WGD, Rouxel T, Borhan MH (2015) Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2 using an intraspecific comparative genomics approach. Mol Plant Pathol 16:699–709. https://doi.org/10.1111/mpp.12228
doi: 10.1111/mpp.12228
pubmed: 25492575
pmcid: 6638346
Ghanbarnia K, Ma L, Larkan NJ, Haddadi P, Fernando WGD, Borhan MH (2018) Leptosphaeria maculans AvrLm9: A new player in the game of hide and seek with AvrLm4-7. Mol Plant Pathol 19:1754. https://doi.org/10.1111/mpp.12658
doi: 10.1111/mpp.12658
pubmed: 29330918
pmcid: 6638032
Gibson G (2012) Rare and common variants: twenty arguments. Nat Rev Genet 13:135. https://doi.org/10.1038/nrg3118
doi: 10.1038/nrg3118
pubmed: 22251874
pmcid: 4408201
Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011. https://doi.org/10.1016/S1097-2765(00)80265-8
doi: 10.1016/S1097-2765(00)80265-8
pubmed: 10911994
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. https://doi.org/10.1111/j.1365-2958.2006.05076.x
doi: 10.1111/j.1365-2958.2006.05076.x
pubmed: 16556221
Haddadi P, Larkan NJ, Borhan MH (2019) Dissecting R gene and host genetic background effect on the Brassica napus defense response to Leptosphaeria maculans. Sci Rep 9:6947. https://doi.org/10.1038/s41598-019-43419-9
doi: 10.1038/s41598-019-43419-9
pubmed: 31061421
pmcid: 6502879
Hayward A, McLanders J, Campbell E, Edwards D, Batley J (2012) Genomic advances will herald new insights into the Brassica: Leptosphaeria maculans pathosystem. Plant Biol 14:1–10. https://doi.org/10.1111/j.1438-8677.2011.00481.x
doi: 10.1111/j.1438-8677.2011.00481.x
pubmed: 21973193
He H, Zhu S, Zhao R, Jiang Z, Ji Y, Ji J, Qiu D, Li H, Bie T (2018) Pm21, encoding a typical CC-NBS-LRR protein, confers broad-spectrum resistance to wheat powdery mildew disease. Mol Plant 11:879–882. https://doi.org/10.1016/j.molp.2018.03.004
doi: 10.1016/j.molp.2018.03.004
pubmed: 29567454
Hind SR, Strickler SR, Boyle PC, Dunham DM, Bao Z, O’Doherty IM, Baccile JA, Hoki JS, Viox EG, Clarke CR (2016) Tomato receptor flagellin-sensing 3 binds flgII-28 and activates the plant immune system. Nat Plants 2:16128. https://doi.org/10.1038/nplants.2016.128
doi: 10.1038/nplants.2016.128
pubmed: 27548463
Huq MA, Akter S, Nou IS, Kim HT, Jung YJ, Kang KK (2016) Identification of functional SNPs in genes and their effects on plant phenotypes. J Plant Biotechnol 43:1–11. https://doi.org/10.5010/JPB.2016.43.1.1
doi: 10.5010/JPB.2016.43.1.1
Howlett BJ, Idnurm A, Pedras MS (2001) Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fungal Genet Biol 33:1–14. https://doi.org/10.1006/fgbi.2001.1274
doi: 10.1006/fgbi.2001.1274
pubmed: 11407881
Huang X, Han B (2014) Natural variations and genome-wide association studies in crop plants. Annu Rev Plant Biol 65:531–551. https://doi.org/10.1146/annurev-arplant-050213-035715
doi: 10.1146/annurev-arplant-050213-035715
pubmed: 24274033
Inturrisi FC, Barbetti MJ, Tirnaz S, Patel DA, Edwards D, Batley J (2020a) Molecular characterization of disease resistance in Brassica juncea – the current status and the way forward. Plant Pathol 00:1–22. https://doi.org/10.1111/ppa.13277
doi: 10.1111/ppa.13277
Inturrisi F, Bayer PE, Yang H, Tirnaz S, Edwards D, Batley J (2020b) Genome-wide identification and comparative analysis of resistance genes in Brassica juncea. Mol Breed 40:78. https://doi.org/10.1007/s11032-020-01159-z
doi: 10.1007/s11032-020-01159-z
Jiang N, Cui J, Meng J, Luan Y (2018) A tomato nucleotide binding sites−leucine-rich repeat gene is positively involved in plant resistance to Phytophthora infestans. Phytopathol 108:980–987. https://doi.org/10.1094/PHYTO-12-17-0389-R
doi: 10.1094/PHYTO-12-17-0389-R
Kaur J, Akhatar J, Goyal A, Kaur N, Kaur S, Mittal M, Kumar N, Sharma H, Banga S, Banga SS (2020) Genome wide association mapping and candidate gene analysis for pod shatter resistance in Brassica juncea and its progenitor species. Mol Biol Rep 47:2963–2974. https://doi.org/10.1007/s11033-020-05384-9
doi: 10.1007/s11033-020-05384-9
pubmed: 32219770
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinform 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
doi: 10.1093/bioinformatics/bts199
Kim CK, Seol YJ, Perumal S, Lee J, Waminal NE, Jayakodi M, Lee SC, Jin S, Choi BS, Yu Y, Ko HC (2018) Re-exploration of U’s triangle Brassica species based on chloroplast genomes and 45S nrDNA sequences. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-25585-4
doi: 10.1038/s41598-018-25585-4
Kimber D, McGregor D (1995) Brassica oilseeds: production and utilization. CAB International, Wallingford
Kirk J, Oram R (1978) Mustards as possible oil and protein crops for Australia. J Aust Inst Agric Sci 44:143–156
Koch E, Song K, Osborn T, Williams P (1991) Relationship between pathogenicity and phylogeny based on restriction fragment length polymorphism in Leptosphaeria maculans. Mol Plant-Microbe Interact 4:341–349. https://doi.org/10.1094/MPMI-4-341
doi: 10.1094/MPMI-4-341
Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29. https://doi.org/10.1186/1746-4811-9-29
doi: 10.1186/1746-4811-9-29
pubmed: 23876160
pmcid: 3750305
Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507. https://doi.org/10.1105/tpc.104.026765
doi: 10.1105/tpc.104.026765
pubmed: 15548740
pmcid: 535888
LaFramboise T (2009) Single nucleotide polymorphism arrays: a decade of biological, computational and technological advances. Nucleic Acids Res 37:4181–4193. https://doi.org/10.1093/nar/gkp552
doi: 10.1093/nar/gkp552
pubmed: 19570852
pmcid: 2715261
Larkan NJ, Kuzmicz S, Yu F, Lydiate D (2010) Genetic evidence for the recognition of the Leptosphaeria maculans avirulence gene AvrLm1 by two Brassica napus resistance genes: Rlm1 and LepR3. In: 17th Crucifer Genetics Workshop. Saskatoon, Canada, p 103
Larkan NJ, Lydiate DJ, Parkin IAP, 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. https://doi.org/10.1111/nph.12043
doi: 10.1111/nph.12043
pubmed: 23206118
Larkan NJ, Lydiate DJ, Yu F, Rimmer SR, Borhan MH (2014) Co-localisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10. BMC Plant Biol 14:387. https://doi.org/10.1186/s12870-014-0387-z
doi: 10.1186/s12870-014-0387-z
pubmed: 25551287
pmcid: 4302512
Larkan NJ, Ma L, Borhan MH (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. https://doi.org/10.1111/pbi.12341
doi: 10.1111/pbi.12341
pubmed: 25644479
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. https://doi.org/10.3389/fpls.2016.01771
doi: 10.3389/fpls.2016.01771
pubmed: 27965684
pmcid: 5124708
Larkan NJ, Ma L, Haddadi P, Buchwaldt M, Parkin IA, Djavaheri M, Borhan MH (2020) The Brassica napus wall-associated kinase-like (WAKL) gene Rlm9 provides race-specific blackleg resistance. Plant J. https://doi.org/10.1111/tpj.14966
doi: 10.1111/tpj.14966
pubmed: 32794614
pmcid: 7756564
Li P, Quan X, Jia G, Xiao J, Cloutier S, You FM (2016) RGAugury: a pipeline for genome-wide prediction of resistance gene analogs (RGAs) in plants. BMC Genom 17:852. https://doi.org/10.1186/s12864-016-3197-x
doi: 10.1186/s12864-016-3197-x
Li P, Zhang S, Li F, Zhang S, Zhang H, Wang X, Sun R, Bonnema G, Borm TJ (2017) A phylogenetic analysis of chloroplast genomes elucidates the relationships of the six economically important Brassica species comprising the triangle of U. Front Plant Sci 8:111. https://doi.org/10.3389/fpls.2017.00111
doi: 10.3389/fpls.2017.00111
pubmed: 28210266
pmcid: 5288352
Liban SH, Cross DJ, Kutcher HR, Peng G, Fernando WGD (2016) Race structure and frequency of avirulence genes in the western Canadian Leptosphaeria maculans pathogen population, the causal agent of blackleg in Brassica species. Plant Pathol 65:1161–1169. https://doi.org/10.1111/ppa.12489
doi: 10.1111/ppa.12489
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinform 28:2397–2399. https://doi.org/10.1093/bioinformatics/bts444
doi: 10.1093/bioinformatics/bts444
Lorenc MT, Hayashi S, Stiller J, Lee H, Manoli S, Ruperao P, Visendi P, Berkman PJ, Lai K, Batley J (2012) Discovery of single nucleotide polymorphisms in complex genomes using SGSautoSNP. Biology 1:370–382. https://doi.org/10.3390/biology1020370
doi: 10.3390/biology1020370
pubmed: 24832230
pmcid: 4009776
Lu K, Peng L, Zhang C, Lu J, Yang B, Xiao Z, Liang Y, Xu X, Qu C, Zhang K (2017) Genome-wide association and transcriptome analyses reveal candidate genes underlying yield-determining traits in Brassica napus. Front Plant Sci 8:206. https://doi.org/10.3389/fpls.2017.00206
doi: 10.3389/fpls.2017.00206
pubmed: 28261256
pmcid: 5309214
Ma L, Borhan MH (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. https://doi.org/10.3389/fpls.2015.00933
doi: 10.3389/fpls.2015.00933
pubmed: 26579176
pmcid: 4625043
Marcroft S, Wratten N, Purwantara A, Salisbury P, Potter T, Barbetti M, Khangura R, Howlett B (2002) Reaction of a range of Brassica species under Australian conditions to the fungus, Leptosphaeria maculans, the causal agent of blackleg. Aust J Exp Agric 42:587–594. https://doi.org/10.1071/EA01112
doi: 10.1071/EA01112
Mason AS, Higgins EE, Snowdon RJ, Batley J, Stein A, Werner C, Parkin IA (2017) A user guide to the Brassica 60K Illumina Infinium SNP genotyping array. Theor Appl Genet 130:621–633. https://doi.org/10.1007/s00122-016-2849-1
doi: 10.1007/s00122-016-2849-1
pubmed: 28220206
Mayerhofer R, Wilde K, Mayerhofer M, Lydiate D, Bansal V, Good A, Parkin I (2005) Complexities of chromosome landing in a highly duplicated genome: towards map based cloning of a gene controlling blackleg resistance in Brassica napus. Genetics 39:546. https://doi.org/10.1534/genetics.105.049098
doi: 10.1534/genetics.105.049098
Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92. https://doi.org/10.1046/j.1365-313X.2002.01404.x
doi: 10.1046/j.1365-313X.2002.01404.x
pubmed: 12366802
Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genom Res 8:1113–1130. https://doi.org/10.1101/gr.8.11.1113
doi: 10.1101/gr.8.11.1113
Nagaharu U (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. J Jpn Bot 7:389–452
Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, Meyers BC (2013) The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiol 162:1459–1472. https://doi.org/10.1104/pp.113.219162
doi: 10.1104/pp.113.219162
pubmed: 23735504
pmcid: 3707564
Neik TX, Amas J, Barbetti M, Edwards D, Batley J (2020) Understanding host–pathogen interactions in Brassica napus in the Omics era. Plants 9:1336. https://doi.org/10.3390/plants9101336
doi: 10.3390/plants9101336
pmcid: 7599536
Nishimura MT, Anderson RG, Cherkis KA, Law TF, Liu QL, Machius M, Nimchuk ZL, Yang L, Chung EH, El Kasmi F (2017) TIR-only protein RBA1 recognizes a pathogen effector to regulate cell death in Arabidopsis. Proc Natl Acad Sci 114:2053–2062. https://doi.org/10.1073/pnas.1620973114
doi: 10.1073/pnas.1620973114
Plissonneau C, Daverdin G, Ollivier B, Blaise F, Degrave A, Fudal I, Rouxel T, Balesdent MH (2016) A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. New Phytol 209:1613–1624. https://doi.org/10.1111/nph.13736
doi: 10.1111/nph.13736
pubmed: 26592855
Poland JA, Rife TW (2012) Genotyping-by-sequencing for plant breeding and genetics. Plant Genom 5:92–102. https://doi.org/10.3835/plantgenome2012.05.0005
doi: 10.3835/plantgenome2012.05.0005
Potter T, Burton W, Edwards J, Wratten N, Mailer R, Salisbury P, Pearce A (2016) Assessing progress in breeding to improve grain yield, quality and blackleg (Leptosphaeria maculans) resistance in selected Australian canola cultivars (1978–2012). Crop Pasture Sci 67:308–316. https://doi.org/10.1071/CP15290
doi: 10.1071/CP15290
Rahaman M, Mamidi S, Rahman M (2018) Genome-wide association study of heat stress-tolerance traits in spring-type Brassica napus L. under controlled conditions. Crop J 6:115–125. https://doi.org/10.1016/j.cj.2017.08.003
doi: 10.1016/j.cj.2017.08.003
Raman R, Taylor B, Lindbeck K, Coombes N, Barbulescu D, Salisbury P, Raman H (2012) Molecular mapping and validation of Rlm1 gene for resistance to Leptosphaeria maculans in canola (Brassica napus L.). Crop Pasture Sci 63:1007–1017. https://doi.org/10.1071/CP12255
doi: 10.1071/CP12255
Raman H, Raman R, Coombes N, Song J, Diffey S, Kilian A, Lindbeck K, Barbulescu DM, Batley J, Edwards D, Salisbury PA, Marcroft S (2016) Genome-wide association study identifies new loci for resistance to Leptosphaeria maculans in canola. Front Plant Sci 7:1513. https://doi.org/10.3389/fpls.2016.01513
doi: 10.3389/fpls.2016.01513
pubmed: 27822217
pmcid: 5075532
Rasheed A, Hao Y, Xia X, Khan A, Xu Y, Varshney RK, He Z (2017) Crop breeding chips and genotyping platforms: progress, challenges, and perspectives. Mol Plant 10:1047–1064. https://doi.org/10.1016/j.molp.2017.06.008
doi: 10.1016/j.molp.2017.06.008
pubmed: 28669791
Rashid MH, Zou Z, Fernando WD (2018) Development of molecular markers linked to the Leptosphaeria maculans resistance gene Rlm6 and inheritance of SCAR and CAPS markers in Brassica napus×Brassica juncea interspecific hybrids. Plant Breed 137:402–411. https://doi.org/10.1111/pbr.12587
doi: 10.1111/pbr.12587
Rimmer SR (2006) Resistance genes to Leptosphaeria maculans in Brassica napus. Can J Plant Pathol 28:S288–S297. https://doi.org/10.1080/07060660609507386
doi: 10.1080/07060660609507386
Rimmer SR, van den Berg CGJ (1992) Resistance of oilseed Brassica spp. to blackleg caused by Leptosphaeria maculans. Can J Plant Pathol 14:56–66. https://doi.org/10.1080/07060669209500906
doi: 10.1080/07060669209500906
Ritchie MD, Van Steen K (2018) The search for gene-gene interactions in genome-wide association studies: challenges in abundance of methods, practical considerations, and biological interpretation. Ann Transl Med 6:157. https://doi.org/10.21037/atm.2018.04.05
doi: 10.21037/atm.2018.04.05
pubmed: 29862246
pmcid: 5952010
Rouxel T, Balesdent M (2005) The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol Plant Pathol 6:225–241. https://doi.org/10.1111/j.1364-3703.2005.00282.x
doi: 10.1111/j.1364-3703.2005.00282.x
pubmed: 20565653
Roy N (1984) Interspecific transfer of Brassica juncea-type high blackleg resistance to Brassica napus. Euphytica 33:295–303. https://doi.org/10.1007/BF00021125
doi: 10.1007/BF00021125
Scheben A, Batley J, Edwards D (2017) Genotyping-by-sequencing approaches to characterize crop genomes: choosing the right tool for the right application. Plant Biotechnol J 15:149–161. https://doi.org/10.1111/pbi.12645
doi: 10.1111/pbi.12645
pubmed: 27696619
pmcid: 5258866
Scheben A, Verpaalen B, Lawley CT, Chan C-KK, Bayer PE, Edwards BJ (2019) CropSNPdb: a database of SNP array data for Brassica crops and hexaploid bread wheat. Plant J 98:142–152. https://doi.org/10.1111/tpj.14194
doi: 10.1111/tpj.14194
pubmed: 30548723
Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2013) Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS ONE 8:e54985. https://doi.org/10.1371/journal.pone.0054985
doi: 10.1371/journal.pone.0054985
pubmed: 23372807
pmcid: 3555945
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 Dis 90:190–198. https://doi.org/10.1094/PD-90-0190
doi: 10.1094/PD-90-0190
pubmed: 30786411
Staal J, Dixelius C (2008) RLM3, a potential adaptor between specific TIR-NB-LRR receptors and DZC proteins. Commun Integr Biol 1:59–61. https://doi.org/10.4161/cib.1.1.6394
doi: 10.4161/cib.1.1.6394
pubmed: 19513199
pmcid: 2633802
Staal J, Kaliff M, Bohman S, Dixelius C (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J 46:218–230. https://doi.org/10.1111/j.1365-313X.2006.02688.x
doi: 10.1111/j.1365-313X.2006.02688.x
pubmed: 16623885
Tang D, Wang G, Zhou JM (2017) Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell 29:618–637. https://doi.org/10.1105/tpc.16.00891
doi: 10.1105/tpc.16.00891
pubmed: 28302675
pmcid: 5435430
Thomson MJ (2014) High-throughput SNP genotyping to accelerate crop improvement. Plant Breed Biotechnol 2:195–212. https://doi.org/10.9787/PBB.2014.2.3.195
doi: 10.9787/PBB.2014.2.3.195
Ton LB, Neik TX, Batley J (2020) The use of genetic and gene technologies in shaping modern rapeseed cultivars (Brassica napus L.). Genes 11:1161. https://doi.org/10.3390/genes11101161
doi: 10.3390/genes11101161
pmcid: 7600269
Turner SD (2018) qqman: an R package for visualizing GWAS results using QQ and manhattan plots. J Open Source Softw 3:731. https://doi.org/10.21105/joss.00731
doi: 10.21105/joss.00731
Unterseer S, Bauer E, Haberer G, Seidel M, Knaak C, Ouzunova M, Meitinger T, Strom TM, Fries R, Pausch H, Bertani C (2014) A powerful tool for genome analysis in maize: development and evaluation of the high density 600 k SNP genotyping array. BMC Genom 15:823. https://doi.org/10.1186/1471-2164-15-823
doi: 10.1186/1471-2164-15-823
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. https://doi.org/10.1111/j.1365-3059.2008.01982.x
doi: 10.1111/j.1365-3059.2008.01982.x
Van de Wouw AP, Lowe RG, Elliott CE, Dubois DJ, Howlett BJ (2014a) An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars. Mol Plant Pathol 15:523–530. https://doi.org/10.1111/mpp.12105
doi: 10.1111/mpp.12105
pubmed: 24279453
Van de Wouw AP, Marcroft SJ, Ware A, Lindbeck K, Khangura R, Howlett BJ (2014b) Breakdown of resistance to the fungal disease, blackleg, is averted in commercial canola (Brassica napus) crops in Australia. Field Crop Res 166:144–151. https://doi.org/10.1016/j.fcr.2014.06.023
doi: 10.1016/j.fcr.2014.06.023
Van de Wouw AP, Marcroft SJ, Howlett BJ (2016) Blackleg disease of canola in Australia. Crop Pasture Sci 67:273–283. https://doi.org/10.1071/CP15221
doi: 10.1071/CP15221
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. https://doi.org/10.1071/CP16411
doi: 10.1071/CP16411
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L (2014) Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796. https://doi.org/10.1111/pbi.12183
doi: 10.1111/pbi.12183
pubmed: 24646323
pmcid: 4265271
Wang J, Chu S, Zhang H, Zhu Y, Cheng H, Yu D (2016) Development and application of a novel genome-wide SNP array reveals domestication history in soybean. Sci Rep 6:20728. https://doi.org/10.1038/srep20728
doi: 10.1038/srep20728
pubmed: 26856884
pmcid: 4746597
Winfield MO, Allen AM, Burridge AJ, Barker GL, Benbow HR, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G (2016) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J 14:1195–1206. https://doi.org/10.1111/pbi.12485
doi: 10.1111/pbi.12485
pubmed: 26466852
Wolf S (2017) Plant cell wall signalling and receptor-like kinases. Biochem J 474:471–492. https://doi.org/10.1042/BCJ20160238
doi: 10.1042/BCJ20160238
pubmed: 28159895
Xu C, Ren Y, Jian Y, Guo Z, Zhang Y, Xie C, Fu J, Wang H, Wang G, Xu Y (2017) Development of a maize 55K SNP array with improved genome coverage for molecular breeding. Mol Breed 37:20. https://doi.org/10.1007/s11032-017-0622-z
doi: 10.1007/s11032-017-0622-z
pubmed: 28255264
pmcid: 5311085
Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y, Yao P, Li X, Xie K, Zhang J, Wang J, Liu F, Ma W, Shopan J, Zheng H, Mackenzie SA, Zhang M (2016) The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet 48:1225. https://doi.org/10.1038/ng.3657
doi: 10.1038/ng.3657
pubmed: 27595476
You Q, Yang X, Peng Z, Xu L, Wang J (2018) Development and applications of a high throughput genotyping tool for polyploid crops: single nucleotide polymorphism (SNP) array. Front Plant Sci 9:104. https://doi.org/10.3389/fpls.2018.00104
doi: 10.3389/fpls.2018.00104
pubmed: 29467780
pmcid: 5808122
You Q, Yang X, Peng Z, Islam MS, Sood S, Luo Z, Comstock J, Xu L, Wang J (2019) Development of an Axiom Sugarcane100K SNP array for genetic map construction and QTL identification. Theor Appl Genet 132:2829–2845. https://doi.org/10.1007/s00122-019-03391-4
doi: 10.1007/s00122-019-03391-4
pubmed: 31321474
Zhang X, Fernando WD (2018) Insights into fighting against blackleg disease of Brassica napus in Canada. Crop Pasture Sci 69:40–47. https://doi.org/10.1071/CP16401
doi: 10.1071/CP16401
Zhang C, Liu L, Wang X, Vossen J, Li G, Li T, Zheng Z, Gao J, Guo Y, Visser RG (2014) The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to Phytophthora infestans. Theor Appl Genet 127:1353–1364. https://doi.org/10.1007/s00122-014-2303-1
doi: 10.1007/s00122-014-2303-1
pubmed: 24756242
pmcid: 4035550
Zhang X, Peng G, Kutcher HR, Balesdent MH, Delourme R, Fernando WD (2016) Breakdown of Rlm3 resistance in the Brassica napus–Leptosphaeria maculans pathosystem in western Canada. Eur J Plant Pathol 145:659–674. https://doi.org/10.1007/s10658-015-0819-0
doi: 10.1007/s10658-015-0819-0
Zipfel C, Oldroyd GED (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336. https://doi.org/10.1038/nature22009
doi: 10.1038/nature22009
pubmed: 28300100