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Prospects of pan-genomics in barley

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Abstract

The concept of a pan-genome refers to intraspecific diversity in genome content and structure, encompassing both genes and intergenic space. Pan-genomic studies employ a combination of de novo sequence assembly and reference-based alignment to discover and genotype structural variants. The large size and complex structure of Triticeae genomes were for a long time an obstacle for genomic research in barley and its relatives. Now that a reference genome is available, computational pipelines for high-quality sequence assembly are in place, and sequence costs continue to drop, investigations into the structural diversity of the barley genome seem within reach. Here, we review the recent progress on pan-genomics in the model grass Brachypodium distachyon, and the cereal crops rice and maize, and devise a multi-tiered strategy for a pan-genome project in barley. Our design involves: (1) the construction of high-quality de novo sequence assemblies for a small core set of representative genotypes, (2) short-read sequencing of a large diversity panel of genebank accessions to medium coverage and (3) the use of complementary methods such as chromosome-conformation capture sequencing and k-mer-based association genetics. The in silico representation of the barley pan-genome may inform about the mechanisms of structural genome evolution in the Triticeae and supplement quantitative genetics models of crop performance for better accuracy and predictive ability.

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References

  • Antonacci F, Kidd JM, Marques-Bonet T, Ventura M, Siswara P, Jiang Z, Eichler EE (2009) Characterization of six human disease-associated inversion polymorphisms. Hum Mol Genet 18:2555–2566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora S, Steuernagel B, Chandramohan S, Long Y, Matny O, Johnson R, Enk J, Periyannan S, Hatta MAM, Athiyannan N (2018) Resistance gene discovery and cloning by sequence capture and association genetics. bioRxiv: 248146

  • Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97

    Article  CAS  PubMed  Google Scholar 

  • Bauer E, Schmutzer T, Barilar I, Mascher M, Gundlach H, Martis MM, Twardziok SO, Hackauf B, Gordillo A, Wilde P (2017) Towards a whole-genome sequence for rye (Secale cereale L.). Plant J 89:853–869

    Article  CAS  PubMed  Google Scholar 

  • Bayer MM, Rapazote-Flores P, Ganal M, Hedley PE, Macaulay M, Plieske J, Ramsay L, Russell J, Shaw PD, Thomas W (2017) Development and evaluation of a barley 50 k iSelect SNP array. Front Plant Sci 8:1792

    Article  PubMed  PubMed Central  Google Scholar 

  • Beier S, Himmelbach A, Schmutzer T, Felder M, Taudien S, Mayer KF, Platzer M, Stein N, Scholz U, Mascher M (2016) Multiplex sequencing of bacterial artificial chromosomes for assembling complex plant genomes. Plant Biotechnol J 14:1511–1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beier S, Himmelbach A, Colmsee C, Zhang X-Q, Barrero RA, Zhang Q, Li L, Bayer M, Bolser D, Taudien S (2017) Construction of a map-based reference genome sequence for barley, Hordeum vulgare L. Sci Data 4:170044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blattner FR (2018) Taxonomy of the genus Hordeum and barley (Hordeum vulgare). In: Stein N, Muehlbauer GJ (eds) The barley genome. Springer, Berlin, pp 11–23

    Chapter  Google Scholar 

  • Brkljacic J, Grotewold E, Scholl R, Mockler T, Garvin DF, Vain P, Brutnell T, Sibout R, Bevan M, Budak H, Caicedo AL, Gao C, Gu Y, Hazen SP, Holt BF, Hong SY, Jordan M, Manzaneda AJ, Mitchell-Olds T, Mochida K, Mur LA, Park CM, Sedbrook J, Watt M, Zheng SJ, Vogel JP (2011) Brachypodium as a model for the grasses: today and the future. Plant Physiol 157(1):3–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ (2013) Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:1213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burton JN, Adey A, Patwardhan RP, Qiu R, Kitzman JO, Shendure J (2013) Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol 31:1119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chong Z, Ruan J, Gao M, Zhou W, Chen T, Fan X, Ding L, Lee AY, Boutros P, Chen J (2017) novoBreak: local assembly for breakpoint detection in cancer genomes. Nat Methods 14:65

    Article  CAS  PubMed  Google Scholar 

  • Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345:1249721

    Article  CAS  PubMed  Google Scholar 

  • Clark AG, Hubisz MJ, Bustamante CD, Williamson SH, Nielsen R (2005) Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15:1496–1502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Comadran J, Kilian B, Russell J, Ramsay L, Stein N, Ganal M, Shaw P, Bayer M, Thomas W, Marshall D (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44:1388

    Article  CAS  PubMed  Google Scholar 

  • Dai F, Wang X, Zhang XQ, Chen Z, Nevo E, Jin G, Wu D, Li C, Zhang G (2018) Assembly and analysis of a qingke reference genome demonstrate its close genetic relation to modern cultivated barley. Plant Biotechnol J 16:760–770

    Article  CAS  PubMed  Google Scholar 

  • Dawson IK, Russell J, Powell W, Steffenson B, Thomas WT, Waugh R (2015) Barley: a translational model for adaptation to climate change. New Phytol 206:913–931

    Article  PubMed  Google Scholar 

  • De Beukelaer H, Davenport GF, Fack V (2018) Core Hunter 3: flexible core subset selection. BMC Bioinform 19:203

    Article  Google Scholar 

  • Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295:1306–1311

    Article  CAS  PubMed  Google Scholar 

  • Denton JF, Lugo-Martinez J, Tucker AE, Schrider DR, Warren WC, Hahn MW (2014) Extensive error in the number of genes inferred from draft genome assemblies. PLoS Comput Biol 10:e1003998

    Article  PubMed  PubMed Central  Google Scholar 

  • Dick KJ, Nelson CP, Tsaprouni L, Sandling JK, Aïssi D, Wahl S, Meduri E, Morange P-E, Gagnon F, Grallert H (2014) DNA methylation and body-mass index: a genome-wide analysis. Lancet 383:1990–1998

    Article  CAS  PubMed  Google Scholar 

  • Doležel J, Greilhuber J, Lucretti S, Meister A, Lysák M, Nardi L, Obermayer R (1998) Plant genome size estimation by flow cytometry: inter-laboratory comparison. Ann Bot 82:17–26

    Article  Google Scholar 

  • Draper J, Mur LA, Jenkins G, Ghosh-Biswas GC, Bablak P, Hasterok R, Routledge AP (2001) Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol 127:1539–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAOSTAT (2017) Statistical data. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Feuk L, Marshall CR, Wintle RF, Scherer SW (2006) Structural variants: changing the landscape of chromosomes and design of disease studies. Hum Mol Genet 15:R57–R66

    Article  CAS  PubMed  Google Scholar 

  • Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci 108:1513–1518

    Article  CAS  PubMed  Google Scholar 

  • Gordon SP, Contreras-Moreira B, Woods DP, Des Marais DL, Burgess D, Shu S, Stritt C, Roulin AC, Schackwitz W, Tyler L (2017) Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nat Commun 8:2184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruissem W, Lee C-H, Oliver M, Pogson B (2012) The global plant council: increasing the impact of plant research to meet global challenges. J Plant Biol 55:343–348

    Article  Google Scholar 

  • Guillot G, Foll M (2009) Correcting for ascertainment bias in the inference of population structure. Bioinformatics 25:552–554

    Article  CAS  PubMed  Google Scholar 

  • Harewood L, Kishore K, Eldridge MD, Wingett S, Pearson D, Schoenfelder S, Collins VP, Fraser P (2017) Hi-C as a tool for precise detection and characterisation of chromosomal rearrangements and copy number variation in human tumours. Genome Biol 18:125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Himmelbach A, Liu L, Zierold U, Altschmied L, Maucher H, Beier F, Müller D, Hensel G, Heise A, Schützendübel A (2010) Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. Plant Cell 22:937–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Himmelbach A, Ruban A, Walde I, Šimková H, Doležel J, Hastie A, Stein N, Mascher M (2018a) Discovery of multi-megabase polymorphic inversions by chromosome conformation capture sequencing in large-genome plant species. Plant J. https://doi.org/10.1111/tpj.14109

    Article  PubMed  Google Scholar 

  • Himmelbach A, Walde I, Mascher M, Stein N (2018b) Tethered chromosome conformation capture sequencing in Triticeae: a valuable tool for genome assembly. Bio-protocol 8:e2955

    Article  Google Scholar 

  • Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G, Vaillancourt B, Peñagaricano F, Lindquist E, Pedraza MA, Barry K, de Leon N, Kaeppler SM, Buell CR (2014) Insights into the maize pan-genome and pan-transcriptome. Plant Cell 26(1):121–135. https://doi.org/10.1105/tpc.113.119982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirsch CN, Hirsch CD, Brohammer AB, Bowman MJ, Soifer I, Barad O, Shem-Tov D, Baruch K, Lu F, Hernandez AG, Fields CJ, Wright CL, Koehler K, Springer NM, Buckler E, Buell CR, de Leon N, Kaeppler SM, Childs KL, Mikel MA (2016) Draft assembly of elite inbred line PH207 provides insights into genomic and transcriptome diversity in maize. Plant Cell 28(11):2700–2714. https://doi.org/10.1105/tpc.16.00353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Kurata N, Wang Z-X, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497

    Article  CAS  PubMed  Google Scholar 

  • Hübner S, Höffken M, Oren E, Haseneyer G, Stein N, Graner A, Schmid K, Fridman E (2009) Strong correlation of wild barley (Hordeum spontaneum) population structure with temperature and precipitation variation. Mol Ecol 18:1523–1536

    Article  PubMed  Google Scholar 

  • International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711

    Article  CAS  Google Scholar 

  • International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763

    Article  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793

    Article  CAS  Google Scholar 

  • Jakob SS, Rodder D, Engler JO, Shaaf S, Ozkan H, Blattner FR, Kilian B (2014) Evolutionary history of wild barley (Hordeum vulgare subsp. spontaneum) analyzed using multilocus sequence data and paleodistribution modeling. Genome Biol Evol 6:685–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan N, Dekker J (2013) High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat Biotechnol 31:1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knox AK, Dhillon T, Cheng H, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35

    Article  PubMed  Google Scholar 

  • Korneliussen TS, Albrechtsen A, Nielsen R (2014) ANGSD: analysis of next generation sequencing data. BMC Bioinform 15:356

    Article  Google Scholar 

  • Kremling K, Diepenbrock C, Gore M, Buckler E, Bandillo N (2018) Transcriptome-wide association supplements genome-wide association in Zea mays. bioRxiv: 363242

  • Krumm N, Sudmant PH, Ko A, O’Roak BJ, Malig M, Coe BP, Quinlan AR, Nickerson DA, Eichler EE (2012) Copy number variation detection and genotyping from exome sequence data. Genome Res 22:1525–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412

    PubMed  PubMed Central  Google Scholar 

  • Lam ET, Hastie A, Lin C, Ehrlich D, Das SK, Austin MD, Deshpande P, Cao H, Nagarajan N, Xiao M (2012) Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nat Biotechnol 30:771

    Article  CAS  PubMed  Google Scholar 

  • Lehmann CO, Mansfeld R (1957) Zur Technik der Sortimentserhaltung. Die Kulturpflanze 5:108–138

    Article  Google Scholar 

  • Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci 95:370–375

    Article  CAS  PubMed  Google Scholar 

  • Li H (2015) FermiKit: assembly-based variant calling for Illumina resequencing data. Bioinformatics 31:3694–3696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H (2018) Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 1:7

    Google Scholar 

  • Li YH, Zhou G, Ma J, Jiang W, Jin LG, Zhang Z, Guo Y, Zhang J, Sui Y, Zheng L, Zhang SS (2014) De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol 32:1045–1052

    Article  CAS  PubMed  Google Scholar 

  • Lieberman-Aiden E, Van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Bayer M, Druka A, Russell JR, Hackett CA, Poland J, Ramsay L, Hedley PE, Waugh R (2014) An evaluation of genotyping by sequencing (GBS) to map the Breviaristatum-e (ari-e) locus in cultivated barley. BMC Genom 15:104

    Article  CAS  Google Scholar 

  • Lu F, Romay MC, Glaubitz JC, Bradbury PJ, Elshire RJ, Wang T, Li Y, Li Y, Semagn K, Zhang X (2015) High-resolution genetic mapping of maize pan-genome sequence anchors. Nat Commun 6:6914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A (2018) MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol 14:e1005944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang XQ, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Simkova H, Stankova H, Vrana J, Chan S, Munoz-Amatriain M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Dolezel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    Article  CAS  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milner SG, Jost M, Taketa S, Rey Mazon E, Himmelbach A, Oppermann M et al (2018) Genebank genomics reveals the diversity of a global barley collection. Nat Genet. https://doi.org/10.1038/s41588-018-0266-x

    Article  PubMed  Google Scholar 

  • Montenegro JD, Golicz AA, Bayer PE, Hurgobin B, Lee H, Chan CK, Visendi P, Lai K, Doležel J, Batley J, Edwards D (2017) The pangenome of hexaploid bread wheat. Plant J 90:1007–1013

    Article  CAS  PubMed  Google Scholar 

  • Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997

    Article  CAS  PubMed  Google Scholar 

  • Morgante M, De Paoli E, Radovic S (2007) Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10:149–155

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Amatriaín M, Eichten SR, Wicker T, Richmond TA, Mascher M, Steuernagel B, Scholz U, Ariyadasa R, Spannagl M, Nussbaumer T (2013) Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol 14:R58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muñoz-Amatriaín M, Cuesta-Marcos A, Endelman JB, Comadran J, Bonman JM, Bockelman HE, Chao S, Russell J, Waugh R, Hayes PM (2014) The USDA barley core collection: genetic diversity, population structure, and potential for genome-wide association studies. PLoS ONE 9:e94688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy TM, Mill J (2014) Epigenetics in health and disease: heralding the EWAS era. Lancet 383:1952–1954

    Article  PubMed  Google Scholar 

  • Nielsen R, Signorovitch J (2003) Correcting for ascertainment biases when analyzing SNP data: applications to the estimation of linkage disequilibrium. Theor Popul Biol 63:245–255

    Article  PubMed  Google Scholar 

  • Odong T, Jansen J, Van Eeuwijk F, van Hintum TJ (2013) Quality of core collections for effective utilisation of genetic resources review, discussion and interpretation. Theor Appl Genet 126:289–305

    Article  CAS  PubMed  Google Scholar 

  • Oppermann M, Weise S, Dittmann C, Knüpffer H (2015) GBIS: the information system of the German Genebank. Database. https://doi.org/10.1093/database/bav021

    Article  PubMed  PubMed Central  Google Scholar 

  • Pankin A, Altmüller J, Becker C, von Korff M (2018) Targeted resequencing reveals genomic signatures of barley domestication. New Phytol 218:1247–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551

    Article  CAS  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7:e32253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pourkheirandish M, Hensel G, Kilian B, Senthil N, Chen G, Sameri M, Azhaguvel P, Sakuma S, Dhanagond S, Sharma R, Mascher M, Himmelbach A, Gottwald S, Nair SK, Tagiri A, Yukuhiro F, Nagamura Y, Kanamori H, Matsumoto T, Willcox G, Middleton CP, Wicker T, Walther A, Waugh R, Fincher GB, Stein N, Kumlehn J, Sato K, Komatsuda T (2015) Evolution of the grain dispersal system in barley. Cell 162:527–539

    Article  CAS  PubMed  Google Scholar 

  • Putnam NH, O’Connell BL, Stites JC, Rice BJ, Blanchette M, Calef R, Troll CJ, Fields A, Hartley PD, Sugnet CW (2016) Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res 26:342–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman A, Hallgrímsdóttir I, Eisen MB, Pachter L (2017) Association mapping from sequencing reads using k-mers. bioRxiv: 141267

  • Rakyan VK, Down TA, Balding DJ, Beck S (2011) Epigenome-wide association studies for common human diseases. Nat Rev Genet 12:529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riedelsheimer C, Czedik-Eysenberg A, Grieder C, Lisec J, Technow F, Sulpice R, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat Genet 44:217

    Article  CAS  PubMed  Google Scholar 

  • Russell J, Dawson IK, Flavell AJ, Steffenson B, Weltzien E, Booth A, Ceccarelli S, Grando S, Waugh R (2011) Analysis of > 1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome-level differences in diversity around domestication genes. New Phytol 191:564–578

    Article  PubMed  Google Scholar 

  • Russell J, Mascher M, Dawson IK, Kyriakidis S, Calixto C, Freund F, Bayer M, Milne I, Marshall-Griffiths T, Heinen S (2016) Exome sequencing of geographically diverse barley landraces and wild relatives gives insights into environmental adaptation. Nat Genet 48:1024–1030

    Article  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin Y-K, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

    Article  CAS  PubMed  Google Scholar 

  • Sato K, Tanaka T, Shigenobu S, Motoi Y, Wu J, Itoh T (2015) Improvement of barley genome annotations by deciphering the Haruna Nijo genome. DNA Res 23:21–28

    PubMed  PubMed Central  Google Scholar 

  • Schatz MC, Maron LG, Stein JC, Wences AH, Gurtowski J, Biggers E, Lee H, Kramer M, Antoniou E, Ghiban E (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

    PubMed  PubMed Central  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Schreiber M, Stein N, Mascher M (2018) Genomic approaches for studying crop evolution. Genome Biol 19:140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulte D, Close TJ, Graner A, Langridge P, Matsumoto T, Muehlbauer G, Sato K, Schulman AH, Waugh R, Wise RP (2009) The international barley sequencing consortium—at the threshold of efficient access to the barley genome. Plant Physiol 149:142–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seifert F, Thiemann A, Schrag TA, Rybka D, Melchinger AE, Frisch M, Scholten S (2018) Small RNA-based prediction of hybrid performance in maize. BMC Genom 19:371

    Article  CAS  Google Scholar 

  • Stein N, Mascher M (2018) Barley genome sequencing and assembly—a first version reference sequence. In: Stein N, Muehlbauer GJ (eds) The barley genome. Springer, Berlin, pp 57–71

    Chapter  Google Scholar 

  • Sutton T, Baumann U, Hayes J, Collins NC, Shi B-J, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449

    Article  CAS  PubMed  Google Scholar 

  • Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci 102:13950–13955

    Article  CAS  PubMed  Google Scholar 

  • The International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191

    Article  CAS  PubMed  Google Scholar 

  • van Hintum TJL, Knüpffer H (1995) Duplication within and between germplasm collections. Genet Resour Crop Evol 42:127–133

    Article  Google Scholar 

  • Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes R, Zhang F (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557:43–49

    Article  CAS  PubMed  Google Scholar 

  • Wei F, Wing RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weisenfeld NI, Kumar V, Shah P, Church DM, Jaffe DB (2017) Direct determination of diploid genome sequences. Genome Res 27:757–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendler N, Mascher M, Himmelbach A, Johnston P, Pickering R, Stein N (2015) Bulbosum to go: a toolbox to utilize Hordeum vulgare/bulbosum introgressions for breeding and beyond. Mol Plant 8:1507–1519

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105

    Article  CAS  Google Scholar 

  • Zeng X, Long H, Wang Z, Zhao S, Tang Y, Huang Z, Wang Y, Xu Q, Mao L, Deng G (2015) The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau. Proc Natl Acad Sci 112:1095–1100

    Article  CAS  PubMed  Google Scholar 

  • Zhao Q, Feng Q, Lu H, Li Y, Wang A, Tian Q, Zhan Q, Lu Y, Zhang L, Huang T (2018) Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet 50:278

    Article  CAS  PubMed  Google Scholar 

  • Ziems LA, Hickey LT, Platz GJ, Franckowiak JD, Dracatos PM, Singh D, Park RF (2017) Characterization of Rph24: a gene conferring adult plant resistance to Puccinia hordei in barley. Phytopathology 107:834–841

    Article  CAS  Google Scholar 

  • Zimin AV, Puiu D, Hall R, Kingan S, Clavijo BJ, Salzberg SL (2017) The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum. Gigascience

  • Zohary D, Hopf M, Weiss E (2012) Domestication of plants in the old world: the origin and spread of domesticated plants in Southwest Asia, Europe, and the Mediterranean Basin. Oxford University Press, Oxford

    Book  Google Scholar 

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Acknowledgements

This work was supported by a grant of the Leibniz Association to N.S. (Pakt für Forschung und Innovation: SAW-2015-IPK-1) and the German Federal Ministry of Education and Research (BMBF Grant 031B0190A ‘SHAPE’) to N.S. and M.M.

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Correspondence to Martin Mascher.

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This manuscript is part of the special volume on New technologies for plant breeding.

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Monat, C., Schreiber, M., Stein, N. et al. Prospects of pan-genomics in barley. Theor Appl Genet 132, 785–796 (2019). https://doi.org/10.1007/s00122-018-3234-z

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