Genome assembly and characterization of a complex zfBED-NLR gene-containing disease resistance locus in Carolina Gold Select rice with Nanopore sequencing
Autoři:
Andrew C. Read aff001; Matthew J. Moscou aff002; Aleksey V. Zimin aff003; Geo Pertea aff003; Rachel S. Meyer aff004; Michael D. Purugganan aff004; Jan E. Leach aff006; Lindsay R. Triplett aff006; Steven L. Salzberg aff003; Adam J. Bogdanove aff001
Působiště autorů:
Plant Pathology and Plant Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States of America
aff001; The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
aff002; Center for Computational Biology, Johns Hopkins University, Baltimore, MD, United States of America
aff003; Center for Genomics and Systems Biology, New York University, New York, NY, United States of America
aff004; Center for Genomics and Biology, New York University Abu Dhabi, Saadiyat Island, Abu Dhabi, United Arab Emirates
aff005; Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, United States of America
aff006; Departments of Biomedical Engineering, Computer Science, and Biostatistics, Johns Hopkins University, Baltimore, MD, United States of America
aff007
Vyšlo v časopise:
Genome assembly and characterization of a complex zfBED-NLR gene-containing disease resistance locus in Carolina Gold Select rice with Nanopore sequencing. PLoS Genet 16(1): e1008571. doi:10.1371/journal.pgen.1008571
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008571
Souhrn
Long-read sequencing facilitates assembly of complex genomic regions. In plants, loci containing nucleotide-binding, leucine-rich repeat (NLR) disease resistance genes are an important example of such regions. NLR genes constitute one of the largest gene families in plants and are often clustered, evolving via duplication, contraction, and transposition. We recently mapped the Xo1 locus for resistance to bacterial blight and bacterial leaf streak, found in the American heirloom rice variety Carolina Gold Select, to a region that in the Nipponbare reference genome is NLR gene-rich. Here, toward identification of the Xo1 gene, we combined Nanopore and Illumina reads and generated a high-quality Carolina Gold Select genome assembly. We identified 529 complete or partial NLR genes and discovered, relative to Nipponbare, an expansion of NLR genes at the Xo1 locus. One of these has high sequence similarity to the cloned, functionally similar Xa1 gene. Both harbor an integrated zfBED domain, and the repeats within each protein are nearly perfect. Across diverse Oryzeae, we identified two sub-clades of NLR genes with these features, varying in the presence of the zfBED domain and the number of repeats. The Carolina Gold Select genome assembly also uncovered at the Xo1 locus a rice blast resistance gene and a gene encoding a polyphenol oxidase (PPO). PPO activity has been used as a marker for blast resistance at the locus in some varieties; however, the Carolina Gold Select sequence revealed a loss-of-function mutation in the PPO gene that breaks this association. Our results demonstrate that whole genome sequencing combining Nanopore and Illumina reads effectively resolves NLR gene loci. Our identification of an Xo1 candidate is an important step toward mechanistic characterization, including the role(s) of the zfBED domain. Finally, the Carolina Gold Select genome assembly will facilitate identification of other useful traits in this historically important variety.
Klíčová slova:
Genetic loci – Genome sequencing – Phylogenetic analysis – Plant genomics – Protein domains – Rice – Sequence alignment – Sequence assembly tools
Zdroje
1. Sedlazeck FJ, Lee H, Darby CA, Schatz MC (2018) Piercing the dark matter: bioinformatics of long-range sequencing and mapping. Nat Rev Genet 19: 329–346. doi: 10.1038/s41576-018-0003-4 29599501
2. Payne A, Holmes N, Rakyan V, Loose M (2018) BulkVis: a graphical viewer for Oxford nanopore bulk FAST5 files. Bioinformatics: bty841.
3. Rang FJ, Kloosterman WP, de Ridder J (2018) From squiggle to basepair: computational approaches for improving nanopore sequencing read accuracy. Genome Biol 19: 90. doi: 10.1186/s13059-018-1462-9 30005597
4. Michael TP, Jupe F, Bemm F, Motley ST, Sandoval JP, et al. (2018) High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell. Nat Comm 9: 541.
5. Schmidt MH, Vogel A, Denton AK, Istace B, Wormit A, et al. (2017) De novo assembly of a new Solanum pennellii accession using nanopore sequencing. Plant Cell 29: 2336–2348. doi: 10.1105/tpc.17.00521 29025960
6. Jupe F, Rivkin AC, Michael TP, Zander M, Motley ST, et al. (2019) The complex architecture and epigenomic impact of plant T-DNA insertions. PLoS Genet 15: e1007819. doi: 10.1371/journal.pgen.1007819 30657772
7. Giolai M, Paajanen P, Verweij W, Witek K, Jones JDG, et al. (2017) Comparative analysis of targeted long read sequencing approaches for characterization of a plant's immune receptor repertoire. BMC Genomics 18: 564. doi: 10.1186/s12864-017-3936-7 28747151
8. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, et al. (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18: 2024–2033. doi: 10.1101/gr.080200.108 18818371
9. Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, et al. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317: 338–342. doi: 10.1126/science.1138632 17641193
10. Li J, Ding J, Zhang W, Zhang Y, Tang P, et al. (2010) Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol Genet Genomics 283: 427–438. doi: 10.1007/s00438-010-0527-6 20217430
11. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809–834. doi: 10.1105/tpc.009308 12671079
12. Zhou T, Wang Y, Chen J-Q, Araki H, Jing Z, et al. (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 271: 402–415. doi: 10.1007/s00438-004-0990-z 15014983
13. Sun X, Cao Y, Yang Z, Xu C, Li X, et al. (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37: 517–527. doi: 10.1046/j.1365-313x.2003.01976.x 14756760
14. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8: 1113–1130. doi: 10.1101/gr.8.11.1113 9847076
15. Hall SA, Allen RL, Baumber RE, Baxter LA, Fisher K, et al. (2009) Maintenance of genetic variation in plants and pathogens involves complex networks of gene-for-gene interactions. Mol Plant Pathol 10: 449–457. doi: 10.1111/j.1364-3703.2009.00544.x 19523099
16. Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Front Immunol 4: 297. doi: 10.3389/fimmu.2013.00297 24093022
17. Schatz MC, Maron LG, Stein JC, Wences AH, Gurtowski J, et al. (2014) Whole genome de novo assemblies of three divergent strains of rice, Oryza sativa, document novel gene space of aus and indica. Genome Biol 15: 506. doi: 10.1186/s13059-014-0506-z 25468217
18. Yu P, Wang C, Xu Q, Feng Y, Yuan X, et al. (2011) Detection of copy number variations in rice using array-based comparative genomic hybridization. BMC Genomics 12: 372. doi: 10.1186/1471-2164-12-372 21771342
19. Zheng L-Y, Guo X-S, He B, Sun L-J, Peng Y, et al. (2011) Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol 12: R114. doi: 10.1186/gb-2011-12-11-r114 22104744
20. Xu X, Liu X, Ge S, Jensen JD, Hu F, et al. (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30: 105–111.
21. Bush SJ, Castillo-Morales A, Tovar-Corona JM, Chen L, Kover PX, et al. (2013) Presence–absence variation in A. thaliana is primarily associated with genomic signatures consistent with relaxed selective constraints. Mol Biol Evol 31: 59–69. doi: 10.1093/molbev/mst166 24072814
22. Kroj T, Chanclud E, Michel‐Romiti C, Grand X, Morel JB (2016) Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytol 210: 618–626. doi: 10.1111/nph.13869 26848538
23. Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14: 8. doi: 10.1186/s12915-016-0228-7 26891798
24. Bailey PC, Schudoma C, Jackson W, Baggs E, Dagdas G, et al. (2018) Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions. Genome Biol 19: 23. doi: 10.1186/s13059-018-1392-6 29458393
25. Triplett LR, Cohen SP, Heffelfinger C, Schmidt CL, Huerta A, et al. (2016) A resistance locus in the American heirloom rice variety Carolina Gold Select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola. Plant J 87: 472–483. doi: 10.1111/tpj.13212 27197779
26. McClung A, Fjellstrom R (2010) Using molecular genetics as a tool to identify and refine “Carolina Gold”. In: Shields DS, editor. The golden seed: writings on the history and culture of Carolina gold rice. Beaufort, South Carolina: Douglas W. Bostick for the Carolina Gold Rice Foundation. pp. 37–41.
27. Duitama J, Silva A, Sanabria Y, Cruz DF, Quintero C, et al. (2015) Whole genome sequencing of elite rice cultivars as a comprehensive information resource for marker assisted selection. PLoS One 10: e0124617. doi: 10.1371/journal.pone.0124617 25923345
28. Ayres NM, McClung AM, Larkin PD, Bligh HFJ, Jones CA, et al. (1997) Microsatellites and a single-nucleotide polymorphism differentiate apparent amylose classes in an extended pedigree of US rice germ plasm. Theor Appl Genet 94: 773–781.
29. Sakaguchi S (1967) Linkage studies on the resistance to bacterial leaf blight, Xanthomonas oryzae (Uyeda et Ishiyama) Dowson, in rice. Bull Natl Inst Agric Sci Ser D 16: 1–18.
30. He Q, Li D, Zhu Y, Tan M, Zhang D, et al. (2006) Fine mapping of Xa2, a bacterial blight resistance gene in rice. Mol Breed 17: 1–6.
31. Ise K, Li CY, Ye CR, and Sun YQ (1998) Inheritance of resistance to bacterial leaf blight in differential rice variety Asominori. Int Rice Res Notes 23: 13–14.
32. Endo T, Yamaguchi M, Kaji R, Nakagomi K, Kataoka T, et al. (2012) Close linkage of a blast resistance gene, Pias(t), with a bacterial leaf blight resistance gene, Xa1-as(t), in a rice cultivar ‘Asominori’. Breed Sci 62: 334–339. doi: 10.1270/jsbbs.62.334 23341747
33. Ogawa T, Morinaka T, Fujii K, Kimura T (1978) Inheritance of Resistance of Rice Varieties Kogyoku and Java 14 to Bacterial Group V of Xanthomonas oryzae. Jap J Phytopathol 44: 137–141.
34. Taura S, Ogawa T, Tabien R, Khush G, Yoshimura A, et al. (1987) The specific reaction of Taichung Native 1 to Philippine races of bacterial blight and inheritance of resistance resistance to race 5 (PX0112). Rice Genet Newsl 4: 101–102.
35. Wang C, Wen G, Lin X, Liu X, Zhang D (2009) Identification and fine mapping of the new bacterial blight resistance gene, Xa31(t), in rice. Eur J Plant Pathol 123: 235–240.
36. Cheema KK, Grewal NK, Vikal Y, Sharma R, Lore JS, et al. (2008) A novel bacterial blight resistance gene from Oryza nivara mapped to 38 kb region on chromosome 4L and transferred to Oryza sativa L. Genet Res 90: 397–407.
37. Aravind L (2000) The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases. Trends Biochem Sci 25: 421–423. doi: 10.1016/s0968-0004(00)01620-0 10973053
38. Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang Z-X, et al. (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95: 1663–1668. doi: 10.1073/pnas.95.4.1663 9465073
39. Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13: 394–401. doi: 10.1016/j.pbi.2010.04.010 20570209
40. Hutin M, Perez-Quintero AL, Lopez C, Szurek B (2015) MorTAL Kombat: the story of defense against TAL effectors through loss-of-susceptibility. Front Plant Sci 6: 535. doi: 10.3389/fpls.2015.00535 26236326
41. Zhang J, Yin Z, White F (2015) TAL effectors and the executor R genes. Front Plant Sci 6.
42. Schornack S, Ballvora A, Gürlebeck D, Peart J, Ganal M, et al. (2004) The tomato resistance protein Bs4 is a predicted non‐nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37: 46–60. doi: 10.1046/j.1365-313x.2003.01937.x 14675431
43. Ji Z, Ji C, Liu B, Zou L, Chen G, et al. (2016) Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat Comm 7: 13435.
44. Read AC, Rinaldi FC, Hutin M, He Y-Q, Triplett LR, et al. (2016) Suppression of Xo1-mediated disease resistance in rice by a truncated, non-DNA-binding TAL effector of Xanthomonas oryzae. Front Plant Sci 7: 1516. doi: 10.3389/fpls.2016.01516 27790231
45. Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, et al. (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6: 4. doi: 10.1186/1939-8433-6-4 24280374
46. Kolmogorov M, Yuan J, Lin Y, Pevzner PA (2019) Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37: 540–546. doi: 10.1038/s41587-019-0072-8 30936562
47. Zimin AV, Puiu D, Luo MC, Zhu T, Koren S, et al. (2017) Hybrid assembly of the large and highly repetitive genome of Aegilops tauschii, a progenitor of bread wheat, with the MaSuRCA mega-reads algorithm. Genome Res 27: 787–792. doi: 10.1101/gr.213405.116 28130360
48. Marcais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, et al. (2018) MUMmer4: A fast and versatile genome alignment system. PLoS Comp Biol 14: e1005944.
49. Steuernagel B, Jupe F, Witek K, Jones JD, Wulff BB (2015) NLR-parser: rapid annotation of plant NLR complements. Bioinformatics 31: 1665–1667. doi: 10.1093/bioinformatics/btv005 25586514
50. Bayer PE, Edwards D, Batley J (2018) Bias in resistance gene prediction due to repeat masking. Nat Plants 4: 762–765. doi: 10.1038/s41477-018-0264-0 30287950
51. Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, et al. (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50: 285–296. doi: 10.1038/s41588-018-0040-0 29358651
52. Wilkins KE, Booher NJ, Wang L, Bogdanove AJ (2015) TAL effectors and activation of predicted host targets distinguish Asian from African strains of the rice pathogen Xanthomonas oryzae pv. oryzicola while strict conservation suggests universal importance of five TAL effectors. Front Plant Sci 6: 536. doi: 10.3389/fpls.2015.00536 26257749
53. Chaisson MJ, Tesler G (2012) Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinformatics 13: 238. doi: 10.1186/1471-2105-13-238 22988817
54. Bendahmane A, Farnham G, Moffett P, Baulcombe DC (2002) Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J 32: 195–204. doi: 10.1046/j.1365-313x.2002.01413.x 12383085
55. van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, et al. (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59: 1383–1397. doi: 10.1093/jxb/ern045 18390848
56. Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, et al. (1997) Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9: 641–651. doi: 10.1105/tpc.9.4.641 9144966
57. Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11: 495–506. doi: 10.1105/tpc.11.3.495 10072407
58. Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195–1206. doi: 10.1105/tpc.7.8.1195 7549479
59. Chen J, Huang Q, Gao D, Wang J, Lang Y, et al. (2013) Whole-genome sequencing of Oryza brachyantha reveals mechanisms underlying Oryza genome evolution. Nat Comm 4: 1595.
60. Wang M, Yu Y, Haberer G, Marri PR, Fan C, et al. (2014) The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat Genet 46: 982–988. doi: 10.1038/ng.3044 25064006
61. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20: 116–122. doi: 10.1016/j.tig.2004.01.007 15049302
62. Germain H, Seguin A (2011) Innate immunity: has poplar made its BED? New Phytol 189: 678–687. doi: 10.1111/j.1469-8137.2010.03544.x 21087262
63. Van de Weyer A-L, Monteiro F, Furzer OJ, Nishimura MT, Cevik V, et al. (2019) The Arabidopsis thaliana pan-NLRome. bioRxiv: 537001.
64. Marchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B, et al. (2018) BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nat Plants 4: 662–668. doi: 10.1038/s41477-018-0236-4 30150615
65. Kanzaki H, Yoshida K, Saitoh H, Tamiru M, Terauchi R (2014) Protoplast cell death assay to study Magnaporthe oryzae AVR gene function in rice. Methods Mol Biol 1127: 269–275. doi: 10.1007/978-1-62703-986-4_20 24643567
66. Cesari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V, et al. (2014) The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J 33: 1941–1959. doi: 10.15252/embj.201487923 25024433
67. Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D, et al. (2015) A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161: 1074–1088. doi: 10.1016/j.cell.2015.04.025 26000483
68. Brabham HJ, Hernández-Pinzón I, Holden S, Lorang J, Moscou MJ (2018) An ancient integration in a plant NLR is maintained as a trans-species polymorphism. bioRxiv: 239541.
69. Lam E, Kano-Murakami Y, Gilmartin P, Niner B, Chua NH (1990) A metal-dependent DNA-binding protein interacts with a constitutive element of a light-responsive promoter. Plant Cell 2: 857–866. doi: 10.1105/tpc.2.9.857 2152132
70. Coupe SA, Deikman J (1997) Characterization of a DNA-binding protein that interacts with 5′ flanking regions of two fruit-ripening genes. Plant J 11: 1207–1218. doi: 10.1046/j.1365-313x.1997.11061207.x 9225464
71. Bundock P, Hooykaas P (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436: 282–284. doi: 10.1038/nature03667 16015335
72. Xu X, Chen H, Fujimura T, Kawasaki S (2008) Fine mapping of a strong QTL of field resistance against rice blast, Pikahei-1(t), from upland rice Kahei, utilizing a novel resistance evaluation system in the greenhouse. Theor Appl Genet 117: 997–1008. doi: 10.1007/s00122-008-0839-7 18758744
73. Xu X, Hayashi N, Wang C-T, Fukuoka S, Kawasaki S, et al. (2014) Rice blast resistance gene Pikahei-1(t), a member of a resistance gene cluster on chromosome 4, encodes a nucleotide-binding site and leucine-rich repeat protein. Mol Breed 34: 691–700.
74. Smith CW (2002) Rice: origin, history, technology, and production; Smith CW, editor. United States of America: John Wiley & Sons. 642 p.
75. Yu Y, Tang T, Qian Q, Wang Y, Yan M, et al. (2008) Independent losses of function in a polyphenol oxidase in rice: differentiation in grain discoloration between subspecies and the role of positive selection under domestication. Plant Cell 20: 2946–2959. doi: 10.1105/tpc.108.060426 19033526
76. Jupe F, Witek K, Verweij W, Śliwka J, Pritchard L, et al. (2013) Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J 76: 530–544. doi: 10.1111/tpj.12307 23937694
77. Witek K, Jupe F, Witek AI, Baker D, Clark MD, et al. (2016) Accelerated cloning of a potato late blight-resistance gene using RenSeq and SMRT sequencing. Nat Biotechnol 34: 656–660. doi: 10.1038/nbt.3540 27111721
78. Steuernagel B, Periyannan SK, Hernandez-Pinzon I, Witek K, Rouse MN, et al. (2016) Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol 34: 652–655. doi: 10.1038/nbt.3543 27111722
79. Stam R, Scheikl D, Tellier A (2016) Pooled enrichment sequencing identifies diversity and evolutionary pressures at NLR resistance genes within a wild tomato population. Genome Biol Evol 8: 1501–1515. doi: 10.1093/gbe/evw094 27189991
80. Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, et al. (2014) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14: 120. doi: 10.1186/1471-2229-14-120 24885638
81. Giolai M, Paajanen P, Verweij W, Percival-Alwyn L, Baker D, et al. (2016) Targeted capture and sequencing of gene-sized DNA molecules. BioTechniques 61: 315. doi: 10.2144/000114484 27938323
82. Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, et al. (2019) Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat Biotechnol 37: 139–143. doi: 10.1038/s41587-018-0007-9 30718880
83. Meyer RS, Choi JY, Sanches M, Plessis A, Flowers JM, et al. (2016) Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat Genet 48: 1083. doi: 10.1038/ng.3633 27500524
84. Zimin AV, Puiu D, Hall R, Kingan S, Clavijo BJ, et al. (2017) The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum. Gigascience 6: 1–7.
85. Jain M, Koren S, Miga KH, Quick J, Rand AC, et al. (2018) Nanopore sequencing and assembly of a human genome with ultra-long reads. Nat Biotechnol 36: 338–345. doi: 10.1038/nbt.4060 29431738
86. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168
87. Garrison EM, Gabor (2012) Haplotype-based variant detection from short-read sequencing. arXiv: 1207.3907.
88. Kersey PJ, Allen JE, Allot A, Barba M, Boddu S, et al. (2018) Ensembl Genomes 2018: an integrated omics infrastructure for non-vertebrate species. Nucleic Acids Res 46: D802–D808. doi: 10.1093/nar/gkx1011 29092050
89. Wu TD, Watanabe CK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859–1875. doi: 10.1093/bioinformatics/bti310 15728110
90. Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12: 656–664. doi: 10.1101/gr.229202 11932250
91. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14: 417–419. doi: 10.1038/nmeth.4197 28263959
92. Steuernagel B, Witek K, Krattinger SG, Ramirez-Gonzalez RH, Schoonbeek H-j, et al. (2018) Physical and transcriptional organisation of the bread wheat intracellular immune receptor repertoire. bioRxiv: 339424.
93. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278
94. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. doi: 10.1093/bioinformatics/btu033 24451623
95. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44: W242–W245. doi: 10.1093/nar/gkw290 27095192
96. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, et al. (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45: D200–D203. doi: 10.1093/nar/gkw1129 27899674
97. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573–580. doi: 10.1093/nar/27.2.573 9862982
98. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188–1190. doi: 10.1101/gr.849004 15173120
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