Genome-wide identification and comparative analysis of NBS-LRR resistance genes in Brassica napus
Salman Alamery A D , Soodeh Tirnaz B , Philipp Bayer A B , Reece Tollenaere A , Boulos Chaloub C , David Edwards A B and Jacqueline Batley A B E
+ Author Affiliations
- Author Affiliations
A School of Agriculture and Food Sciences, University of Queensland, St Lucia, Qld 4072, Australia.
B School of Biological Sciences, University of Western Australia, Crawley, WA 6009, Australia.
C URGV (Institut National de la Recherche Agronomique, Université Evry Val d’Essonne), Evry, France.
D Department of Biochemistry, College of Science, King Saud University, Riyadh, Saudi Arabia.
E Corresponding author. Email: jacqueline.batley@uwa.edu.au
Crop and Pasture Science 69(1) 72-93 https://doi.org/10.1071/CP17214
Submitted: 12 June 2017 Accepted: 30 August 2017 Published: 3 October 2017
Abstract
Plant disease-resistance genes play a critical role in providing resistance against pathogens. The largest family of resistance genes are the nucleotide-binding site (NBS) and leucine-rich repeat (LRR) genes. They are classified into two major subfamilies, toll/interleukin-1 receptor (TIR)-NBS-LRR (TNL) and coiled-coil (CC)-NBS-LRR (CNL) proteins. We have identified and characterised 641 NBS-LRR genes in Brassica napus, 249 in B. rapa and 443 in B. oleracea. A ratio of 1 : 2 of CNL : TNL genes was found in the three species. Domain structure analysis revealed that 57% of the NBS-LRR genes are typical resistance genes and contain all three domains (TIR/CC, NBS, LRR), whereas the remaining genes are partially deleted or truncated. Of the NBS-LRR genes, 59% were found to be physically clustered, and individual genes involved in clusters were more polymorphic than those not clustered. Of the NBS-LRR genes in B. napus, 50% were identified as duplicates, reflecting a high level of genomic duplication and rearrangement. Comparative analysis between B. napus and its progenitor species indicated that >60% of NBS-LRR genes are conserved in B. napus. This study provides a valuable resource for the identification and characterisation of candidate NBS-LRR genes.
Additional keywords: comparative genomics, disease resistance, gene cluster, gene duplication.
References
Altschul SF, Madden TL, Schäffer 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.| Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=24c6d034e5e781c520f7adcaf7979bc8CAS |
Ameline-Torregrosa C, Wang B-B, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiology 146, 5–21.
| Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFCms78%3D&md5=89879c8c7555a6573b1a426950c76e2cCAS |
Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site–leucine-rich repeat genes in cereals. Genome Research 12, 1871–1884.
| Diversity in nucleotide binding site–leucine-rich repeat genes in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsVOqtbc%3D&md5=d122849e08355cfdf3e3b8091ee0475cCAS |
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Research 37, W202–W208.
| MEME Suite: tools for motif discovery and searching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFSksb0%3D&md5=a9790c32833f592d0813b7e1e3e04c59CAS |
Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL (2011) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proceedings of the National Academy of Sciences of the United States of America 108, 16463–16468.
| Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Khsb3F&md5=cd4f714755e0ec358db3906a859375e4CAS |
Cannon S, Zhu H, Baumgarten A, Spangler R, May G, Cook D, Young N (2002) Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. Journal of Molecular Evolution 54, 548–562.
| Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Ggu70%3D&md5=3d9a8adab15dd3130dce32f3d1c5b698CAS |
Cannon S, Mitra A, Baumgarten A, Young N, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology 4, 10
| The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier M-C, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee T-H, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury J-M, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345, 950–953.
| Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlOmsr%2FK&md5=1a8efabc0ad3089b351cba8f65b3c609CAS |
Collier SM, Hamel L-P, Moffett P (2011) Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Molecular Plant-Microbe Interactions 24, 918–931.
| Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlegt7c%3D&md5=6ac3c155bb3c6250d9ff7c5a868e284cCAS |
Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341, 746–751.
| Pivoting the plant immune system from dissection to deployment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1GhurjL&md5=2364ca7414ac10393ee6cc233c55d647CAS |
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.
| A cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFynurs%3D&md5=6faddd726e5cabb60afeec4005237f85CAS |
Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Current Opinion in Plant Biology 13, 472–477.
| NB-LRR proteins: pairs, pieces, perception, partners, and pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Ojsrc%3D&md5=e13853646e1ab6720614e05a9ebe17afCAS |
Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Current Opinion in Plant Biology 3, 278–284.
| Structure, function and evolution of plant disease resistance genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsV2mt74%3D&md5=d40cee783bb966c00d3dcbf4754b724aCAS |
Fourmann M, Charlot F, Froger N, Delourme R, Brunel D (2001) Expression, mapping, and genetic variability of Brassica napus disease resistance gene analogues. Genome 44, 1083–1099.
| Expression, mapping, and genetic variability of Brassica napus disease resistance gene analogues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvVOnug%3D%3D&md5=9e6cdd4af912e69284c728f8f9ceca85CAS |
Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E (2012) The genome of melon (Cucumis melo L.). Proceedings of the National Academy of Sciences of the United States of America 109, 11872–11877.
| The genome of melon (Cucumis melo L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1eqtLrK&md5=f99a09e610b9f66fed7a77127d8996e0CAS |
Grant MR, McDowell JM, Sharpe AG, De Torres Zabala M, Lydiate DJ, Dangl JL (1998) Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 95, 15843–15848.
| Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFenug%3D%3D&md5=308ccde854e0a4d51dd3e2e4f2f5e910CAS |
Guo Y-L, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiology 157, 757–769.
| Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlahu7fP&md5=eb05581425d62016a52cfce243553a36CAS |
Hammond-Kosack KE, Jones JDG (1997) Plant disease resistance genes. Annual Review of Plant Biology 48, 575–607.
| Plant disease resistance genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1elsr0%3D&md5=fc31ab03d209e6f00c07c9335590d622CAS |
Hofberger JA, Zhou B, Tang H, Jones JD, Schranz ME (2014) A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants. BMC Genomics 15, 966
| A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants.Crossref | GoogleScholarGoogle Scholar |
Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nature Reviews. Genetics 2, 516–527.
| The arms race is ancient history in Arabidopsis, the wildflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVCksLs%3D&md5=2c2663636524155bb4f28543ca37fdf3CAS |
Huang YJ, Jestin C, Welham SJ, King GJ, Manzanares-Dauleux MJ, Fitt BDL, Delourme R (2016) Identification of environmentally stable QTL for resistance against Leptosphaeria maculans in oilseed rape (Brassica napus). Theoretical and Applied Genetics 129, 169–180.
| Identification of environmentally stable QTL for resistance against Leptosphaeria maculans in oilseed rape (Brassica napus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC28zntFKgug%3D%3D&md5=d7cc200276a826d4eddaceb1d98d71a0CAS |
Hulbert S, Webb C, Smith S, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annual Review of Phytopathology 39, 285–312.
| Resistance gene complexes: evolution and utilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvVygsLw%3D&md5=6d9425b9b80dab094e239931aeaa2b4eCAS |
Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Frontiers in Immunology 4,
| Evolution and conservation of plant NLR functions.Crossref | GoogleScholarGoogle Scholar |
Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240.
| InterProScan 5: genome-scale protein function classification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvFCjsr4%3D&md5=a2ac0fc809bf705e13d75e3ee891da91CAS |
Jupe F, Pritchard L, Etherington G, MacKenzie K, Cock P, Wright F, Sharma SK, Bolser D, Bryan G, Jones J, Hein I (2012) Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics 13, 75
| Identification and localisation of the NB-LRR gene family within the potato genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktlSktbY%3D&md5=6b8d2725328c64b0294420c8a8a63ca6CAS |
Kale SM, Pardeshi VC, Barvkar VT, Gupta VS, Kadoo NY (2013) Genome-wide identification and characterization of nucleotide binding site leucine-rich repeat genes in linseed reveal distinct patterns of gene structure. Genome 56, 91–99.
| Genome-wide identification and characterization of nucleotide binding site leucine-rich repeat genes in linseed reveal distinct patterns of gene structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Chu70%3D&md5=6c820956f245a06190b075589336ef85CAS |
Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers B, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Molecular Biology 66, 619–636.
| Genome-wide identification of NBS resistance genes in Populus trichocarpa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFWlsrc%3D&md5=d7670388381aac5952d914a66858a728CAS |
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 Biology 14, 387
| Co-localisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10.Crossref | GoogleScholarGoogle Scholar |
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 Biotechnology Journal 13, 983–992.
| The Brassica napus receptor‐like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtl2murjM&md5=74eebfc0f5ce202b9e254b8c3a71f008CAS |
Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends in Genetics: TIG 20, 116–122.
| Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsV2nu78%3D&md5=ebe0dcf2b512579c442712a35ffa5661CAS |
Liu J, Liu X, Dai L, Wang G (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. Journal of Genetics and Genomics 34, 765–776.
| Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants.Crossref | GoogleScholarGoogle Scholar |
Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IAP, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang T-J, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, Jin D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park B-S, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee T-H, Wang J, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nature Communications 5, art3930
| The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes.Crossref | GoogleScholarGoogle Scholar |
Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G (2012) Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum Group Phureja. PLoS One 7, e34775
| Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum Group Phureja.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVyrsb8%3D&md5=c5bebc37d87a9a2af41497d088c1539cCAS |
Lozano R, Hamblin MT, Prochnik S, Jannink J-L (2015) Identification and distribution of the NBS-LRR gene family in the Cassava genome. BMC Genomics 16, 360
| Identification and distribution of the NBS-LRR gene family in the Cassava genome.Crossref | GoogleScholarGoogle Scholar |
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.
| Complexities of chromosome landing in a highly duplicated genome: toward map-based cloning of a gene controlling blackleg resistance in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVOqug%3D%3D&md5=856fdf92c80bdd793bccd9eeee351221CAS |
McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biology 7, 212
| Plant NBS-LRR proteins: adaptable guards.Crossref | GoogleScholarGoogle Scholar |
Meyers B, Dickerman A, Michelmore R, Sivaramakrishnan S, Sobral B, Young N (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. The Plant Journal 20, 317–332.
| Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsF2kug%3D%3D&md5=abcbc99f194087ce7d1cf933f401ebe3CAS |
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. The Plant Journal 32, 77–92.
| TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosFGksbY%3D&md5=0138a24f9488bdb40deb375223897880CAS |
Meyers B, Kozik A, Griego A, Kuang H, Michelmore R (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. The Plant Cell 15, 809–834.
| Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFSlsLo%3D&md5=f4230628744d6dcac2bdd7ffdd7f0a9aCAS |
Michelmore R, Meyers B (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Research 8, 1113–1130.
| Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVWhurg%3D&md5=73542cf46be331c1f9ef8e2018377b81CAS |
Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theoretical and Applied Genetics 109, 1434–1447.
| Full-genome analysis of resistance gene homologues in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVahtbfE&md5=0fee5ddafba849fa1394be714a0deeffCAS |
Mun J, Yu H, Park S, Park B (2009) Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Molecular Genetics and Genomics 282, 617–631.
| Genome-wide identification of NBS-encoding resistance genes in Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVWms77P&md5=95fcab0218bdfa3755a88a6703c760e0CAS |
Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. Journal of Molecular Evolution 50, 203–213.
| Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVKgt7k%3D&md5=f0ff57f5225589a8c6b9d0bcc3c86077CAS |
Parkin IAP, Sharpe AG, Lydiate DJ (2003) Patterns of genome duplication within the Brassica napus genome. Genome 46, 291–303.
| Patterns of genome duplication within the Brassica napus genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtlynsbw%3D&md5=b2eb5211041eb83b9eebced9e6e80e9fCAS |
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.
| Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Ohu7vP&md5=46f382f3a61d191d212fc3f34dee632cCAS |
Parkin IAP, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biology 15, R77
| Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea.Crossref | GoogleScholarGoogle Scholar |
Parniske M, Jones JDG (1999) Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proceedings of the National Academy of Sciences of the United States of America 96, 5850–5855.
| Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtFCnu7g%3D&md5=6d1ed5784de2149ada99c022954c958eCAS |
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob Ur R, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–556.
| The Sorghum bicolor genome and the diversification of grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOmsb4%3D&md5=db4349e9d38b0f2613d455a101e5811dCAS |
Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ (2009) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Molecular Genetics and Genomics 281, 609–626.
| Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKhtLk%3D&md5=e3d07c20e293abc42cd92766436c7171CAS |
Raman R, Taylor B, Marcroft S, Stiller J, Eckermann P, Coombes N, Rehman A, Lindbeck K, Luckett D, Wratten N, Batley J, Edwards D, Wang X, Raman H (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.
| Molecular mapping of qualitative and quantitative loci for resistance to Leptosphaeria maculans causing blackleg disease in canola (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotlKntrc%3D&md5=06af036683ec51fd2f5807f818f71473CAS |
Rana D, van den Boogaart T, O’Neill CM, Hynes L, Bent E, Macpherson L, Park JY, Lim YP, Bancroft I (2004) Conservation of the microstructure of genome segments in Brassica napus and its diploid relatives. The Plant Journal 40, 725–733.
| Conservation of the microstructure of genome segments in Brassica napus and its diploid relatives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFWhuw%3D%3D&md5=d579f754b2e28a0f44f65b2636d4f914CAS |
Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Molecular Biology and Evolution 19, 76–84.
| Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFCitg%3D%3D&md5=2e8680a2356791201d0ff471cf573069CAS |
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
Shao Z-Q, Zhang Y-M, Hang Y-Y, Xue J-Y, Zhou G-C, Wu P, Wu X-Y, Wu X-Z, Wang Q, Wang B (2014) Long-term evolution of nucleotide-binding site-leucine-rich repeat genes: understanding gained from and beyond the legume family. Plant Physiology 166, 217–234.
| Long-term evolution of nucleotide-binding site-leucine-rich repeat genes: understanding gained from and beyond the legume family.Crossref | GoogleScholarGoogle Scholar |
Shao Z-Q, Wang B, Chen J-Q (2016a) Tracking ancestral lineages and recent expansions of NBS-LRR genes in angiosperms. Plant Signaling & Behavior 170, e1197470
Shao Z-Q, Xue J-Y, Wu P, Zhang Y-M, Wu Y, Hang Y-Y, Wang B, Chen J-Q (2016b) Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiology 170, 2095–109.
| Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes reveal three anciently diverged classes with distinct evolutionary patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVyrtLnE&md5=c1767cbfd4b484383572f9be2dc62f85CAS |
Song Q, Chen ZJ (2015) Epigenetic and developmental regulation in plant polyploids. Current Opinion in Plant Biology 24, 101–109.
| Epigenetic and developmental regulation in plant polyploids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjs1GqtLg%3D&md5=5bf057b73171b2b24eec8835e416444eCAS |
Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews. Immunology 12, 89–100.
| How do plants achieve immunity? Defence without specialized immune cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1arsb8%3D&md5=4062a0f0649843eb1b676149590340f3CAS |
Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG (1995) Molecular genetics of plant disease resistance. Science 268, 661–667.
| Molecular genetics of plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsVGjurg%3D&md5=0b2eb2f5c52188e1d25552459dc0e461CAS |
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=6b5fd3f49c6d0a44d08a848473b09769CAS |
Tan X, Meyers BC, Kozik A, West MA, Morgante M, St Clair DA, Bent AF, Michelmore RW (2007) Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biology 7,
| Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Tarr D, Alexander H (2009) TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders. BMC Research Notes 2, 197
| TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders.Crossref | GoogleScholarGoogle Scholar |
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=6e8c1141a696de2507188e4f81874524CAS |
Tollenaere R, Hayward A, Dalton-Morgan J, Campbell E, Lee JRM, Lorenc MT, Manoli S, Stiller J, Raman R, Raman H, Edwards D, Batley J (2012) Identification and characterization of candidate Rlm4 blackleg resistance genes in Brassica napus using next-generation sequencing. Plant Biotechnology Journal 10, 709–715.
| Identification and characterization of candidate Rlm4 blackleg resistance genes in Brassica napus using next-generation sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWgu77P&md5=5499612b5a9e8e8adbe0ff8cba6698c0CAS |
Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics 45, 487–494.
| The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksVOjsLk%3D&md5=e4716a901acbed6fd2265e9afd0f1e20CAS |
Vicente JG, King GJ (2001) Characterisation of disease resistance gene-like sequences in Brassica oleracea L. Theoretical and Applied Genetics 102, 555–563.
| Characterisation of disease resistance gene-like sequences in Brassica oleracea L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlKgu7k%3D&md5=579fb205f28c66c855e7469e599863aeCAS |
Wan H, Yuan W, Ye Q, Wang R, Ruan M, Li Z, Zhou G, Yao Z, Zhao J, Liu S, Yang Y (2012) Analysis of TIR- and non-TIR-NBS-LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns. BMC Genomics 13, 502
| Analysis of TIR- and non-TIR-NBS-LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslehs7jO&md5=977c68d73a510a5cebddf5b69ce856b8CAS |
Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J (2013) Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics 14, 109
| Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVSnsr8%3D&md5=0dc46814b5aa8ce8ebd7b9069b1bdbcbCAS |
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun J-H, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park B-S, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IAP, Batley J, Kim J-S, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon S-J, Choi S-R, Lee T-H, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, et al. (2011) The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43, 1035–1039.
| The genome of the mesopolyploid crop species Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gtrbL&md5=05695d7ea614b936d5dab41e8ae9d47eCAS |
Wei H, Li W, Sun X, Zhu S, Zhu J (2013) Systematic analysis and comparison of nucleotide-binding site disease resistance genes in a diploid cotton Gossypium raimondii. PLoS One 8, e68435
| Systematic analysis and comparison of nucleotide-binding site disease resistance genes in a diploid cotton Gossypium raimondii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlajs7nJ&md5=52c94d3863dc74440203bbd08f0dacf7CAS |
Xiao S, Emerson B, Ratanasut K, Patrick E, O’Neill C, Bancroft I, Turner JG (2004) Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Molecular Biology and Evolution 21, 1661–1672.
| Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntVCitL8%3D&md5=e88a83917cbc65b1740d4d40d6f1b37fCAS |
Yang S, Zhang X, Yue J-X, Tian D, Chen J-Q (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Molecular Genetics and Genomics 280, 187–198.
| Recent duplications dominate NBS-encoding gene expansion in two woody species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCqsbjF&md5=8eb565c456da55958a73be4854c0f532CAS |
Yu J, Tehrim S, Zhang F, Tong C, Huang J, Cheng X, Dong C, Zhou Y, Qin R, Hua W, Liu S (2014) Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genomics 15, 3
| Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Zhang YM, Shao ZQ, Wang Q, Hang YY, Xue JY, Wang B, Chen JQ (2016) Uncovering the dynamic evolution of nucleotide‐binding site‐leucine‐rich repeat (NBS‐LRR) genes in Brassicaceae. Journal of Integrative Plant Biology 58, 165–177.
| Uncovering the dynamic evolution of nucleotide‐binding site‐leucine‐rich repeat (NBS‐LRR) genes in Brassicaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhslyruro%3D&md5=bd2c3f3fa36f04f57c18cdb60be03908CAS |
Zheng F, Wu H, Zhang R, Li S, He W, Wong F-L, Li G, Zhao S, Lam H-M (2016) Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genomics 17, S1
| Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family.Crossref | GoogleScholarGoogle Scholar |
Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Molecular Genetics and Genomics 271, 402–415.
| Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVSgurY%3D&md5=81c295386dafcee5b1b49fbefdfb6666CAS |
Zhou F, Guo Y, Qiu L-J (2016) Genome-wide identification and evolutionary analysis of leucine-rich repeat receptor-like protein kinase genes in soybean. BMC Plant Biology 16, 58
| Genome-wide identification and evolutionary analysis of leucine-rich repeat receptor-like protein kinase genes in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXmtlGru70%3D&md5=048911d7fc61bb06e5ea9ae288ad5900CAS |
Zhu H, Cannon SB, Young ND, Cook DR (2002) Phylogeny and genomic organization of the TIR and Non-TIR NBS-LRR resistance gene family in Medicago truncatula. Molecular Plant-Microbe Interactions 15, 529–539.
| Phylogeny and genomic organization of the TIR and Non-TIR NBS-LRR resistance gene family in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlSntro%3D&md5=10ab3dae76c2fdf35f850845ccf170f2CAS |
