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Theoretical and Applied Genetics

, Volume 132, Issue 3, pp 733–750 | Cite as

Connecting genome structural variation with complex traits in crop plants

  • Iulian Gabur
  • Harmeet Singh Chawla
  • Rod J. SnowdonEmail author
  • Isobel A. P. Parkin
Review Article
Part of the following topical collections:
  1. New technologies for plant breeding

Abstract

Key message

Structural genome variation is a major determinant of useful trait diversity. We describe how genome analysis methods are enabling discovery of trait-associated structural variants and their potential impact on breeding.

Abstract

As our understanding of complex crop genomes continues to grow, there is growing evidence that structural genome variation plays a major role in determining traits important for breeding and agriculture. Identifying the extent and impact of structural variants in crop genomes is becoming increasingly feasible with ongoing advances in the sophistication of genome sequencing technologies, particularly as it becomes easier to generate accurate long sequence reads on a genome-wide scale. In this article, we discuss the origins of structural genome variation in crops from ancient and recent genome duplication and polyploidization events and review high-throughput methods to assay such variants in crop populations in order to find associations with phenotypic traits. There is increasing evidence from such studies that gene presence–absence and copy number variation resulting from segmental chromosome exchanges may be at the heart of adaptive variation of crops to counter abiotic and biotic stress factors. We present examples from major crops that demonstrate the potential of pangenomic diversity as a key resource for future plant breeding for resilience and sustainability.

Notes

Funding

Deutscher Akademischer Austauschdienst and Deutsche Forschungsgemeinschaft (Grant No. SN14/17-1).

Compliance with ethical standards

Conflict of interest

All authors jointly state that there is no conflict of interest. IAPP and RJS serve on the editorial board for this journal, but this is not considered to constitute a conflict of interest.

References

  1. Alix K, Gérard PR, Schwarzacher T, Heslop-Harrison JSP (2017) Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 120(2):183–194.  https://doi.org/10.1093/aob/mcx079 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ali N, Heslop-Harrison JP, Ahmad H, Graybosch RA, Hein GL, Schwarzacher T (2016) Introgression of chromosome segments from multiple alien species in wheat breeding lines with wheat streak mosaic virus resistance. Heredity 117:114–123.  https://doi.org/10.1038/hdy.2016.36 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alkan C, Kidd JM, Marques-Bonet T, Aksay G, Antonacci F, Hormozdiari F, Kitzman JO, Baker C, Malig M, Mutlu O, Sahinalp SC, Gibbs RA, Eichler EE (2009) Personalized copy number and segmental duplication maps using next-generation sequencing. Nat Genet 41(10):1061–1067.  https://doi.org/10.1038/ng.437 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alkan C, Coe BP, Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12(5):363–376.  https://doi.org/10.1038/nrg2958 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Anderson JE, Kantar MB, Kono TY, Fu F, Stec AO, Song Q, Cregan PB, Specht JE, Diers BW, Cannon SB, McHale LK, Stupar RM (2014) A roadmap for functional structural variants in the soybean genome. G3 (Bethesda) 4(7):1307–1318.  https://doi.org/10.1534/g3.114.011551 CrossRefGoogle Scholar
  6. Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, Pozniak CJ, Choulet F, Distelfeld A, Poland J, Ronen G, Sharpe AG, Pozniak C, Barad O, Baruch K, Keeble-Gagnère G, Mascher M, Ben-Zvi G, Josselin A-A, Himmelbach A, Balfourier F, Gutierrez-Gonzalez J, Hayden M, Koh C, Muehlbauer G, Pasam RK, Paux E, Rigault P, Tibbits J, Tiwari V, Spannagl M, Lang D, Gundlach H, Haberer G, Mayer KFX, Ormanbekova D, Prade V, Šimková H, Wicker T, Swarbreck D, Rimbert H, Felder M, Guilhot N, Kaithakottil G, Keilwagen J, Leroy P, Lux T, Twardziok S, Venturini L, Juhász A, Abrouk M, Fischer I, Uauy C, Borrill P, Ramirez-Gonzalez RH, Arnaud D, Chalabi S, Chalhoub B, Cory A, Datla R, Davey MW, Jacobs J, Robinson SJ, Steuernagel B, van Ex F, Wulff BBH, Benhamed M, Bendahmane A, Concia L, Latrasse D, Alaux M, Bartoš J, Bellec A, Berges H, Doležel J, Frenkel Z, Gill B, Korol A, Letellier T, Olsen O-A, Singh K, Valárik M, van der Vossen E, Vautrin S, Weining S, Fahima T, Glikson V, Raats D, Číhalíková J, Toegelová H, Vrána J, Sourdille P, Darrier B, Barabaschi D, Cattivelli L, Hernandez P, Galvez S, Budak H, Jones JDG, Witek K, Yu G, Small I, Melonek J, Zhou R, Belova T, Kanyuka K, King R, Nilsen K, Walkowiak S, Cuthbert R, Knox R, Wiebe K, Xiang D, Rohde A, Golds T, Čížková J, Akpinar BA, Biyiklioglu S, Gao L, N’Daiye A, Kubaláková M, Šafář J, Alfama F, Adam-Blondon A-F, Flores R, Guerche C, Loaec M, Quesneville H, Condie J, Ens J, Maclachlan R, Tan Y, Alberti A, Aury J-M, Barbe V, Couloux A, Cruaud C, Labadie K, Mangenot S, Wincker P, Kaur G, Luo M, Sehgal S, Chhuneja P, Gupta OP, Jindal S, Kaur P, Malik P, Sharma P, Yadav B, Singh NK, Khurana J, Chaudhary C, Khurana P, Kumar V, Mahato A, Mathur S, Sevanthi A, Sharma N, Tomar RS, Holušová K, Plíhal O, Clark MD, Heavens D, Kettleborough G, Wright J, Balcárková B, Hu Y, Salina E, Ravin N, Skryabin K, Beletsky A, Kadnikov V, Mardanov A, Nesterov M, Rakitin A, Sergeeva E, Handa H, Kanamori H, Katagiri S, Kobayashi F, Nasuda S, Tanaka T, Wu J, Cattonaro F, Jiumeng M, Kugler K, Pfeifer M, Sandve S, Xun X, Zhan B, Batley J, Bayer PE, Edwards D, Hayashi S, Tulpová Z, Visendi P, Cui L, Du X, Feng K, Nie X, Tong W, Wang L (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science.  https://doi.org/10.1126/science.aar7191 CrossRefPubMedGoogle Scholar
  7. Bai Z, Chen J, Liao Y, Wang M, Liu R, Ge S, Wing RA, Chen M (2016) The impact and origin of copy number variations in the Oryza species. BMC Genomics 17:261.  https://doi.org/10.1186/s12864-016-2589-2 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Belay G, Merker A (2004) Cytogenetic studies in Ethiopian landraces of tetraploid wheat (Tviticum Turgidum L.). II. Spontaneous chromosome translocations and fertility. Hereditas 126(1):35–43.  https://doi.org/10.1111/j.1601-5223.1997.00035.x CrossRefGoogle Scholar
  9. Belay G, Merker A (2006) Cytogenetic analysis of a spontaneous 5B/6B translocation in tetraploid wheat landraces from Ethiopia, and implications for breeding. Plant Breed 117(6):537–542.  https://doi.org/10.1111/j.1439-0523.1998.tb02203.x CrossRefGoogle Scholar
  10. Beló A, Beatty MK, Hondred D, Fengler KA, Li B, Rafalski A (2010) Allelic genome structural variations in maize detected by array comparative genome hybridization. Theor Appl Genet 120(2):355–367.  https://doi.org/10.1007/s00122-009-1128-9 CrossRefPubMedGoogle Scholar
  11. Bridges CB (1936) The BAR “gene” a duplication. Science 83(2148):210–211.  https://doi.org/10.1126/science.83.2148.210 CrossRefPubMedGoogle Scholar
  12. Chaisson MJP, Huddleston J, Dennis MY, Sudmant PH, Malig M, Hormozdiari F, Antonacci F, Surti U, Sandstrom R, Boitano M, Landolin JM, Stamatoyannopoulos JA, Hunkapiller MW, Korlach J, Eichler EE (2014) Resolving the complexity of the human genome using single-molecule sequencing. Nature 517(7536):608–611.  https://doi.org/10.1038/nature13907 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Correa 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, Canaguier A, Chauveau A, Berard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, 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(6199):950–953.  https://doi.org/10.1126/science.1253435 CrossRefPubMedGoogle Scholar
  14. Chang C, Lu J, Zhang H-P, Ma C-X, Sun G (2016) Copy number variation of cytokinin oxidase gene Tackx4 associated with grain weight and chlorophyll content of flag leaf in common wheat. PLoS ONE 10(12):e0145970.  https://doi.org/10.1371/journal.pone.0145970 CrossRefGoogle Scholar
  15. Chen W, Kalscheuer V, Tzschach A, Menzel C, Ullmann R, Schulz MH, Erdogan F, Li N, Kijas Z, Arkesteijn G, Pajares IL, Goetz-Sothmann M, Heinrich U, Rost I, Dufke A, Grasshoff U, Glaeser B, Vingron M, Ropers HH (2008) Mapping translocation breakpoints by next-generation sequencing. Genome Res 18(7):1143–1149.  https://doi.org/10.1101/gr.076166.108 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chester M, Gallagher JP, Symonds VV, Cruz da Silva AV, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE (2012) Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc Natl Acad Sci USA 109(4):1176–1181.  https://doi.org/10.1073/pnas.1112041109 CrossRefPubMedGoogle Scholar
  17. Chia J-M, Song C, Bradbury PJ, Costich D, de Leon N, Doebley J, Elshire RJ, Gaut B, Geller L, Glaubitz JC, Gore M, Guill KE, Holland J, Hufford MB, Lai J, Li M, Liu X, Lu Y, McCombie R, Nelson R, Poland J, Prasanna BM, Pyhäjärvi T, Rong T, Sekhon RS, Sun Q, Tenaillon MI, Tian F, Wang J, Xu X, Zhang Z, Kaeppler SM, Ross-Ibarra J, McMullen MD, Buckler ES, Zhang G, Xu Y, Ware D (2012) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44:803.  https://doi.org/10.1038/ng.2313 CrossRefPubMedGoogle Scholar
  18. Clarke WE, Parkin IA, Gajardo HA, Gerhardt DJ, Higgins E, Sidebottom C, Sharpe AG, Snowdon RJ, Federico ML, Iniguez-Luy FL (2013) Genomic DNA enrichment using sequence capture microarrays: a novel approach to discover sequence nucleotide polymorphisms (SNP) in Brassica napus L. PLoS ONE 8(12):e81992.  https://doi.org/10.1371/journal.pone.0081992 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Colella S, Yau C, Taylor JM, Mirza G, Butler H, Clouston P, Bassett AS, Seller A, Holmes CC, Ragoussis J (2007) QuantiSNP: an objective Bayes hidden-Markov model to detect and accurately map copy number variation using SNP genotyping data. Nucleic Acids Res 35(6):2013–2025.  https://doi.org/10.1093/nar/gkm076 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang J, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338(6111):1206–1209.  https://doi.org/10.1126/science.1228746 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Darracq A, Vitte C, Nicolas S, Duarte J, Pichon J-P, Mary-Huard T, Chevalier C, Bérard A, Le Paslier M-C, Rogowsky P, Charcosset A, Joets J (2018) Sequence analysis of European maize inbred line F2 provides new insights into molecular and chromosomal characteristics of presence/absence variants. BMC Genomics 19(1):119.  https://doi.org/10.1186/s12864-018-4490-7 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (2012) Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes Is associated with altered flowering time in wheat (Triticum aestivum). PLoS ONE 7(3):e33234.  https://doi.org/10.1371/journal.pone.0033234 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Edwards D, Batley J, Snowdon RJ (2013) Accessing complex crop genomes with next-generation sequencing. Theor Appl Genet 126(1):1–11.  https://doi.org/10.1007/s00122-012-1964-x CrossRefPubMedGoogle Scholar
  24. English AC, Salerno WJ, Hampton OA, Gonzaga-Jauregui C, Ambreth S, Ritter DI, Beck CR, Davis CF, Dahdouli M, Ma S, Carroll A, Veeraraghavan N, Bruestle J, Drees B, Hastie A, Lam ET, White S, Mishra P, Wang M, Han Y, Zhang F, Stankiewicz P, Wheeler DA, Reid JG, Muzny DM, Rogers J, Sabo A, Worley KC, Lupski JR, Boerwinkle E, Gibbs RA (2015) Assessing structural variation in a personal genome—towards a human reference diploid genome. BMC Genomics 16(1):332.  https://doi.org/10.1186/s12864-015-1479-3 CrossRefGoogle Scholar
  25. Escaramís G, Docampo E, Rabionet R (2015) A decade of structural variants: description, history and methods to detect structural variation. Brief Funct Genomics 14(5):305–314.  https://doi.org/10.1093/bfgp/elv014 CrossRefPubMedGoogle Scholar
  26. Esteve-Codina A, Paudel Y, Ferretti L, Raineri E, Megens H-J, Silió L, Rodríguez MC, Am Groenen M, Ramos-Onsins SE, Pérez-Enciso M (2013) Dissecting structural and nucleotide genome-wide variation in inbred Iberian pigs. BMC Genomics 14(1):148.  https://doi.org/10.1186/1471-2164-14-148 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Fadista J, Thomsen B, Holm L-E, Bendixen C (2010) Copy number variation in the bovine genome. BMC Genomics 11(1):284.  https://doi.org/10.1186/1471-2164-11-284 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Francia E, Morcia C, Pasquariello M, Mazzamurro V, Milc JA, Rizza F, Terzi V, Pecchioni N (2016) Copy number variation at the HvCBF4HvCBF2 genomic segment is a major component of frost resistance in barley. Plant Mol Biol 92(1):161–175.  https://doi.org/10.1007/s11103-016-0505-4 CrossRefPubMedGoogle Scholar
  29. Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91(1):59–87.  https://doi.org/10.1007/BF00035277 CrossRefGoogle Scholar
  30. Gabur I, Chawla HS, Liu X, Kumar V, Faure S, von Tiedemann A, Jestin C, Dryzska E, Volkmann S, Breuer F, Delourme R, Snowdon R, Obermeier C (2018) Finding invisible quantitative trait loci with missing data. Plant Biotechnol J.  https://doi.org/10.1111/pbi.12942 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gaeta RT, Chris Pires J (2010) Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186(1):18–28.  https://doi.org/10.1111/j.1469-8137.2009.03089.x CrossRefPubMedGoogle Scholar
  32. Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95(5):1971.  https://doi.org/10.1073/pnas.95.5.1971 CrossRefPubMedGoogle Scholar
  33. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488(7412):535–539.  https://doi.org/10.1038/nature11346 CrossRefPubMedGoogle Scholar
  34. Ghosh S, Qu Z, Das PJ, Fang E, Juras R, Cothran EG, McDonell S, Kenney DG, Lear TL, Adelson DL, Chowdhary BP, Raudsepp T (2014) Copy number variation in the horse genome. PLoS Genet 10(10):e1004712.  https://doi.org/10.1371/journal.pgen.1004712 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Golicz AA, Batley J, Edwards D (2016a) Towards plant pangenomics. Plant Biotechnol J 14(4):1099–1105.  https://doi.org/10.1111/pbi.12499 CrossRefPubMedGoogle Scholar
  36. Golicz AA, Bayer PE, Barker GC, Edger PP, Kim H, Martinez PA, Chan CKK, Severn-Ellis A, McCombie WR, Parkin IAP, Paterson AH, Pires JC, Sharpe AG, Tang H, Teakle GR, Town CD, Batley J, Edwards D (2016b) The pangenome of an agronomically important crop plant Brassica oleracea. Nat Commun 7:13390.  https://doi.org/10.1038/ncomms13390 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gonzalez E (2005) The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307(5714):1434–1440.  https://doi.org/10.1126/science.1101160 CrossRefPubMedGoogle Scholar
  38. Grandke F, Snowdon R, Samans B (2016) gsrc: an R package for genome structure rearrangement calling. Bioinformatics 3:545–546.  https://doi.org/10.1093/bioinformatics/btw648 CrossRefGoogle Scholar
  39. Gu YQ, Coleman-Derr D, Kong X, Anderson OD (2004) Rapid genome evolution revealed by comparative sequence analysis of orthologous regions from four Triticeae Genomes. Plant Physiol 135(1):459.  https://doi.org/10.1104/pp.103.038083 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hajirasouliha I, Hormozdiari F, Alkan C, Kidd JM, Birol I, Eichler EE, Sahinalp SC (2010) Detection and characterization of novel sequence insertions using paired-end next-generation sequencing. Bioinformatics 26(10):1277–1283.  https://doi.org/10.1093/bioinformatics/btq152 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hardigan MA, Crisovan E, Hamilton JP, Kim J, Laimbeer P, Leisner CP, Manrique-Carpintero NC, Newton L, Pham GM, Vaillancourt B, Yang X, Zeng Z, Douches DS, Jiang J, Veilleux RE, Buell CR (2016) Genome reduction uncovers a large dispensable genome and adaptive role for copy number variation in asexually propagated Solanum tuberosum. Plant Cell 28(2):388–405.  https://doi.org/10.1105/tpc.15.00538 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10(8):551–564.  https://doi.org/10.1038/nrg2593 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hattori Y, Nagai K, Furukawa S, Song X-J, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460(7258):1026–1030.  https://doi.org/10.1038/nature08258 CrossRefPubMedGoogle Scholar
  44. Haun WJ, Hyten DL, Xu WW, Gerhardt DJ, Albert TJ, Richmond T, Jeddeloh JA, Jia G, Springer NM, Vance CP, Stupar RM (2010) The composition and origins of genomic variation among individuals of the soybean reference cultivar Williams 82. Plant Physiol 155(2):645–655.  https://doi.org/10.1104/pp.110.166736 CrossRefPubMedPubMedCentralGoogle Scholar
  45. He Z, Cheng F, Li Y, Wang X, Parkin IAP, Chalhoub B, Liu S, Bancroft I (2015) Construction of Brassica A and C genome-based ordered pan-transcriptomes for use in rapeseed genomic research. Data Brief 4:357–362.  https://doi.org/10.1016/j.dib.2015.06.016 CrossRefPubMedPubMedCentralGoogle Scholar
  46. He Z, Wang L, Harper AL, Havlickova L, Pradhan AK, Parkin IAP, Bancroft I (2016) Extensive homoeologous genome exchanges in allopolyploid crops revealed by mRNAseq-based visualization. Plant Biotech J 15:594–604.  https://doi.org/10.1111/pbi.12657 CrossRefGoogle Scholar
  47. Higgins EE, Clarke WE, Howell EC, Armstrong SJ, Parkin IAP (2018) Detecting de Novo homoeologous recombination events in cultivated Brassica napus using a genome-wide SNP array. G3 (Bethesda) 8(8):2673–2683.  https://doi.org/10.1534/g3.118.200118 CrossRefGoogle Scholar
  48. Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G, Vaillancourt B, Penagaricano 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 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Horn R, Snowdon R, Kusterer B (2002) Structural genome analysis using molecular cytogenetic techniques. In: Esser K, Lüttge U, Beyschlag W, Hellwig F (eds) Progress in botany: genetics, physiology, ecology. Springer, Berlin, pp 55–79CrossRefGoogle Scholar
  50. Hurgobin B, Golicz AA, Bayer PE, Chan C-KK, Tirnaz S, Dolatabadian A, Schiessl SV, Samans B, Montenegro JD, Parkin IAP, Pires JC, Chalhoub B, King GJ, Snowdon R, Batley J, Edwards D (2017) Homoeologous exchange is a major cause of gene presence/absence variation in the amphidiploid Brassica napus. Plant Biotechnol J 16(7):1265–1274.  https://doi.org/10.1111/pbi.12867 CrossRefGoogle Scholar
  51. Hyten DL, Song Q, Zhu Y, Choi I-Y, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 103(45):16666.  https://doi.org/10.1073/pnas.0604379103 CrossRefPubMedGoogle Scholar
  52. Iovene M, Zhang T, Lou Q, Buell CR, Jiang J (2013) Copy number variation in potato—an asexually propagated autotetraploid species. Plant J 75(1):80–89.  https://doi.org/10.1111/tpj.12200 CrossRefPubMedGoogle Scholar
  53. Jiao W-B, Schneeberger K (2017) The impact of third generation genomic technologies on plant genome assembly. Curr Opin Plant Biol 36:64–70.  https://doi.org/10.1016/j.pbi.2017.02.002 CrossRefPubMedGoogle Scholar
  54. Jiao Y, Zhao H, Ren L, Song W, Zeng B, Guo J, Wang B, Liu Z, Chen J, Li W, Zhang M, Xie S, Lai J (2012) Genome-wide genetic changes during modern breeding of maize. Nat Genet 44(7):812–815.  https://doi.org/10.1038/ng.2312 CrossRefPubMedGoogle Scholar
  55. Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin C-S, Guill K, Regulski M, Kumari S, Olson A, Gent J, Schneider KL, Wolfgruber TK, May MR, Springer NM, Antoniou E, McCombie WR, Presting GG, McMullen M, Ross-Ibarra J, Dawe RK, Hastie A, Rank DR, Ware D (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524.  https://doi.org/10.1038/nature22971 CrossRefPubMedGoogle Scholar
  56. Kallioniemi A, Kallioniemi OP, Sudar D, Rutovitz D, Gray JW, Waldman F, Pinkel D (1992) Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 258(5083):818.  https://doi.org/10.1126/science.1359641 CrossRefPubMedGoogle Scholar
  57. Keane TM, Wong K, Adams DJ, Flint J, Reymond A, Yalcin B (2014) Identification of structural variation in mouse genomes. Front Genet 5:1061.  https://doi.org/10.3389/fgene.2014.00192 CrossRefGoogle Scholar
  58. 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(1):21–35.  https://doi.org/10.1007/s00122-010-1288-7 CrossRefPubMedGoogle Scholar
  59. Korbel JO, Urban AE, Affourtit JP, Godwin B, Grubert F, Simons JF, Kim PM, Palejev D, Carriero NJ, Du L, Taillon BE, Chen Z, Tanzer A, Saunders ACE, Chi J, Yang F, Carter NP, Hurles ME, Weissman SM, Harkins TT, Gerstein MB, Egholm M, Snyder M (2007) Paired-end mapping reveals extensive structural variation in the human genome. Science 318(5849):420–426.  https://doi.org/10.1126/science.1149504 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Korn JM, Kuruvilla FG, McCarroll SA, Wysoker A, Nemesh J, Cawley S, Hubbell E, Veitch J, Collins PJ, Darvishi K, Lee C, Nizzari MM, Gabriel SB, Purcell S, Daly MJ, Altshuler D (2008) Integrated genotype calling and association analysis of SNPs, common copy number polymorphisms and rare CNVs. Nat Genet 40(10):1253–1260.  https://doi.org/10.1038/ng.237 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J 9(1):13–20CrossRefGoogle Scholar
  62. Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H, Liang H, Zhang X, Wang S, Chen S, Li J, Fu Y, Springer NM, Yang H, Wang J, Dai J, Schnable PS, Wang J (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 42(11):1027–1030.  https://doi.org/10.1038/ng.684 CrossRefPubMedGoogle Scholar
  63. Lam ET, Hastie A, Lin C, Ehrlich D, Das SK, Austin MD, Deshpande P, Cao H, Nagarajan N, Xiao M, Kwok P-Y (2012) Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nat Biotechnol 30(8):771–776.  https://doi.org/10.1038/nbt.2303 CrossRefPubMedGoogle Scholar
  64. Law CN, Worland AJ (2006) The control of adult-plant resistance to yellow rust by the translocated chromosome 5BS–7BS of bread wheat. Plant Breed 116(1):59–63.  https://doi.org/10.1111/j.1439-0523.1997.tb00975.x CrossRefGoogle Scholar
  65. Lee JA, Carvalho CMB, Lupski JR (2007) A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131(7):1235–1247.  https://doi.org/10.1016/j.cell.2007.11.037 CrossRefPubMedGoogle Scholar
  66. Lee TG, Kumar I, Diers BW, Hudson ME (2015) Evolution and selection of Rhg1, a copy-number variant nematode-resistance locus. Mol Ecol 24(8):1774–1791.  https://doi.org/10.1111/mec.13138 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Li W, Olivier M (2013) Current analysis platforms and methods for detecting copy number variation. Physiol Genom 45(1):1–16.  https://doi.org/10.1152/physiolgenomics.00082.2012 CrossRefGoogle Scholar
  68. Li Y, Xiao J, Wu J, Duan J, Liu Y, Ye X, Zhang X, Guo X, Gu Y, Zhang L, Jia J, Kong X (2012) A tandem segmental duplication (TSD) in green revolution gene Rht-D1b region underlies plant height variation. New Phytol 196(1):282–291.  https://doi.org/10.1111/j.1469-8137.2012.04243.x CrossRefPubMedGoogle Scholar
  69. Li Y, Zhou G, Ma J, Jiang W, Jin L, Zhang Z, Guo Y, Zhang J, Sui Y, Zheng L, Zhang S, Zuo Q, Shi X, Li Y, Zhang W, Hu Y, Kong G, H-l H, Tan B, Song J, Liu Z, Wang Y, Ruan H, Yeung CKL, Liu J, Wang H, Zhang L, Guan R, Wang K, Li W, Chen S, Chang R, Jiang Z, Jackson SA, Li R, Qiu L (2014) De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol 32(10):1045–1052.  https://doi.org/10.1038/nbt.2979 CrossRefPubMedGoogle Scholar
  70. Lin K, Zhang N, Severing EI, Nijveen H, Cheng F, Visser RGF, Wang X, de Ridder D, Bonnema G (2014) Beyond genomic variation—comparison and functional annotation of three Brassica rapagenomes: a turnip, a rapid cycling and a Chinese cabbage. BMC Genomics 15(1):250.  https://doi.org/10.1186/1471-2164-15-250 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Liu J, Zhang L, Xu L, Ren H, Lu J, Zhang X, Zhang S, Zhou X, Wei C, Zhao F, Du L (2013) Analysis of copy number variations in the sheep genome using 50 K SNP BeadChip array. BMC Genomics 14(1):229.  https://doi.org/10.1186/1471-2164-14-229 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Liu M, Stiller J, Holušová K, Vrána J, Liu D, Doležel J, Liu C (2016) Chromosome-specific sequencing reveals an extensive dispensable genome component in wheat. Sci Rep.  https://doi.org/10.1038/srep36398 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Liu S, Kandoth PK, Lakhssassi N, Kang J, Colantonio V, Heinz R, Yeckel G, Zhou Z, Bekal S, Dapprich J, Rotter B, Cianzio S, Mitchum MG, Meksem K (2017) The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode. Nat Commun 8:14822.  https://doi.org/10.1038/ncomms14822 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Lu F, Romay MC, Glaubitz JC, Bradbury PJ, Elshire RJ, Wang T, Li Y, Li Y, Semagn K, Zhang X, Hernandez AG, Mikel MA, Soifer I, Barad O, Buckler ES (2015) High-resolution genetic mapping of maize pan-genome sequence anchors. Nat Commun.  https://doi.org/10.1038/ncomms7914 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Lupski JR (1998) Genomic disorders: structural features of the genome can lead to DNA rearrangements and human disease traits. Trends Genet 14(10):417–422.  https://doi.org/10.1016/S0168-9525(98)01555-8 CrossRefPubMedGoogle Scholar
  76. Ma L, Chung WK (2001) Quantitative analysis of copy number variants based on real-time lightcycler PCR. In: Haines JL, Korf BR, Morton CC, Seidman CE, Seidman JG, Smith DR (eds) Current protocols in human genetics, vol 107. Wiley, Hoboken, pp 7.21.1–7.21.8Google Scholar
  77. Ma J, Stiller J, Zheng Z, Wei Y, Zheng Y-L, Yan G, Doležel J, Liu C (2015) Putative interchromosomal rearrangements in the hexaploid wheat (Triticum aestivum L.) genotype ‘Chinese Spring’ revealed by gene locations on homoeologous chromosomes. BMC Evol Biol 15:37.  https://doi.org/10.1186/s12862-015-0313-5 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Mace ES, Tai S, Gilding EK, Li Y, Prentis PJ, Bian L, Campbell BC, Hu W, Innes DJ, Han X, Cruickshank A, Dai C, Frère C, Zhang H, Hunt CH, Wang X, Shatte T, Wang M, Su Z, Li J, Lin X, Godwin ID, Jordan DR, Wang J (2013) Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat Commun 4:2320.  https://doi.org/10.1038/ncomms3320 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Mace E, Tai S, Innes D, Godwin I, Hu W, Campbell B, Gilding E, Cruickshank A, Prentis P, Wang J, Jordan D (2014) The plasticity of NBS resistance genes in sorghum is driven by multiple evolutionary processes. BMC Plant Biol.  https://doi.org/10.1186/s12870-014-0253-z CrossRefPubMedPubMedCentralGoogle Scholar
  80. Mamtani M, Anaya J-M, He W, Ahuja SK (2010) Association of copy number variation in the FCGR3B gene with risk of autoimmune diseases. Genes Immun 11(2):155–160.  https://doi.org/10.1038/gene.2009.71 CrossRefPubMedGoogle Scholar
  81. Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Pineros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci USA 110(13):5241–5246.  https://doi.org/10.1073/pnas.1220766110 CrossRefPubMedGoogle Scholar
  82. Mascher M, Richmond TA, Gerhardt DJ, Himmelbach A, Clissold L, Sampath D, Ayling S, Steuernagel B, Pfeifer M, D’Ascenzo M, Akhunov ED, Hedley PE, Gonzales AM, Morrell PL, Kilian B, Blattner FR, Scholz U, Mayer KFX, Flavell AJ, Muehlbauer GJ, Waugh R, Jeddeloh JA, Stein N (2013) Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J 76(3):494–505.  https://doi.org/10.1111/tpj.12294 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 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 X-Q, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín 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, Doležel 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(7651):427–433.  https://doi.org/10.1038/nature22043 CrossRefGoogle Scholar
  84. Mason AS, Snowdon RJ (2016) Oilseed rape: learning about ancient and recent polyploid evolution from a recent crop species. Plant Biol (Stuttg) 18(6):883–892.  https://doi.org/10.1111/plb.12462 CrossRefGoogle Scholar
  85. Mason AS, Higgins EE, Snowdon RJ, Batley J, Stein A, Werner C, Parkin IAP (2017) A user guide to the Brassica 60 K Illumina Infinium™ SNP genotyping array. Theor Appl Genet 130(4):621–633.  https://doi.org/10.1007/s00122-016-2849-1 CrossRefPubMedGoogle Scholar
  86. McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM (2012) Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol 159(4):1295–1308.  https://doi.org/10.1104/pp.112.194605 CrossRefPubMedPubMedCentralGoogle Scholar
  87. McVey M, Lee SE (2008) MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24(11):529–538.  https://doi.org/10.1016/j.tig.2008.08.007 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Montenegro JD, Golicz AA, Bayer PE, Hurgobin B, Lee H, Chan C-KK, Visendi P, Lai K, Doležel J, Batley J, Edwards D (2017) The pangenome of hexaploid bread wheat. Plant J 90(5):1007–1013.  https://doi.org/10.1111/tpj.13515 CrossRefPubMedGoogle Scholar
  89. Moore JK, Haber JE (1996) Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol Cell Biol 16(5):2164–2173.  https://doi.org/10.1128/MCB.16.5.2164 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Morgante M, de Paoli E, Radovic S (2007) Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10(2):149–155.  https://doi.org/10.1016/j.pbi.2007.02.001 CrossRefPubMedGoogle Scholar
  91. Mostovoy Y, Levy-Sakin M, Lam J, Lam ET, Hastie AR, Marks P, Lee J, Chu C, Lin C, Džakula Ž, Cao H, Schlebusch SA, Giorda K, Schnall-Levin M, Wall JD, Kwok P-Y (2016) A hybrid approach for de novo human genome sequence assembly and phasing. Nat Methods 13(7):587–590.  https://doi.org/10.1038/nmeth.3865 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Muñoz-Amatriaín M, Eichten SR, Wicker T, Richmond TA, Mascher M, Steuernagel B, Scholz U, Ariyadasa R, Spannagl M, Nussbaumer T, Mayer KFX, Taudien S, Platzer M, Jeddeloh JA, Springer NM, Muehlbauer GJ, Stein N (2013) Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol 14(6):203.  https://doi.org/10.1186/gb-2013-14-6-r58 CrossRefGoogle Scholar
  93. Neik TX, Barbetti MJ, Batley J (2017) Current status and challenges in identifying disease resistance genes in Brassica napus. Front Plant Sci 8:1788.  https://doi.org/10.3389/fpls.2017.01788 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Nelson JC, Sorrells ME, Van-Deynze AE, Lu YH, Atkinson M, Bernard M, Leroy P, Faris JD, Anderson JA (1995) Molecular mapping of wheat: major genes and rearrangements in homoeologous groups 4, 5, and 7. Genetics 141(2):721–731PubMedPubMedCentralGoogle Scholar
  95. Nishida H, Yoshida T, Kawakami K, Fujita M, Long B, Akashi Y, Laurie DA, Kato K (2013) Structural variation in the 5′ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time. Mol Breeding 31(1):27–37.  https://doi.org/10.1007/s11032-012-9765-0 CrossRefGoogle Scholar
  96. Osborn TC, Butrulle DV, Sharpe AG, Pickering KJ, Parkin IAP, Parker JS, Lydiate DJ (2003) Detection and effects of a homeologous reciprocal transposition in Brassica napus. Genetics 165(3):1569–1577PubMedPubMedCentralGoogle Scholar
  97. Parkin IAP, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38(6):1122–1131.  https://doi.org/10.1139/g95-149 CrossRefPubMedGoogle Scholar
  98. Parkin IAP, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires JC, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15(6):R77.  https://doi.org/10.1186/gb-2014-15-6-r77 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP, Sparks CA, Al-Kaff N, Korolev A, Boulton MI, Phillips AL, Hedden P, Nicholson P, Thomas SG (2011) Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157(4):1820.  https://doi.org/10.1104/pp.111.183657 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Pires JC, Zhao JW, Schranz ME, Leon EJ, Quijada PA, Lukens LN, Osborn TC (2004) Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc Lond 82(4):675–688.  https://doi.org/10.1111/j.1095-8312.2004.00350.x CrossRefGoogle Scholar
  101. Qian L, Voss-Fels K, Cui Y, Jan HU, Samans B, Obermeier C, Qian W, Snowdon RJ (2016) Deletion of a stay-green gene associates with adaptive selection in Brassica napus. Mol Plant 9(12):1559–1569.  https://doi.org/10.1016/j.molp.2016.10.017 CrossRefPubMedGoogle Scholar
  102. Reeves TG, Rajaram S, van Ginkel M, Trethowan R, Braun H, Cassaday K (1999) New wheats for a secure, sustainable future. CIMMYT, MexicoGoogle Scholar
  103. Richter TE, Pryor TJ, Bennetzen JL, Hulbert SH (1995) New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141(1):373–381PubMedPubMedCentralGoogle Scholar
  104. Riley R, Coucoli H, Chapman V (1967) Chromosomal interchanges and the phylogeny of wheat. Heredity 22:233.  https://doi.org/10.1038/hdy.1967.29 CrossRefGoogle Scholar
  105. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerrière A, Vital A, Dumanchin C, Feuillette S, Brice A, Vercelletto M, Dubas F, Frebourg T, Campion D (2006) APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 38(1):24–26.  https://doi.org/10.1038/ng1718 CrossRefPubMedGoogle Scholar
  106. Samans B, Chalhoub B, Snowdon RJ (2017) Surviving a genome collision: genomic signatures of allopolyploidization in the recent crop species. Plant Genome.  https://doi.org/10.3835/plantgenome2017.02.0013 CrossRefPubMedGoogle Scholar
  107. Saxena RK, Edwards D, Varshney RK (2014) Structural variations in plant genomes. Brief Funct Genomics 13(4):296–307.  https://doi.org/10.1093/bfgp/elu016 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Schiessl S, Huettel B, Kuehn D, Reinhardt R, Snowdon R (2017a) Post-polyploidisation morphotype diversification associates with gene copy number variation. Sci Rep 7:41845.  https://doi.org/10.1038/srep41845 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Schiessl S, Huettel B, Kuehn D, Reinhardt R, Snowdon RJ (2017b) Targeted deep sequencing of flowering regulators in Brassica napus reveals extensive copy number variation. Sci Data.  https://doi.org/10.1038/sdata.2017.13 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Schiessl S-V, Katche E, Ihien E, Chawla HS, Mason AS (2018) The role of genomic structural variation in the genetic improvement of polyploid crops. Crop J.  https://doi.org/10.1016/j.cj.2018.07.006 CrossRefGoogle Scholar
  111. Schmidt MH-W, Vogel A, Denton AK, Istace B, Wormit A, van de Geest H, Bolger ME, Alseekh S, Maß J, Pfaff C, Schurr U, Chetelat R, Maumus F, Aury J-M, Koren S, Fernie AR, Zamir D, Bolger AM, Usadel B (2017) De novo Assembly of a new Solanum pennellii accession using nanopore sequencing. Plant Cell 29(10):2336–2348.  https://doi.org/10.1105/tpc.17.00521 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, van Buren P, Vaughn MW, Ying K, Yeh C-T, Emrich SJ, Jia Y, Kalyanaraman A, Hsia A-P, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia J-M, Deragon J-M, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115.  https://doi.org/10.1126/science.1178534 CrossRefPubMedGoogle Scholar
  113. Schröder J, Hsu A, Boyle SE, Macintyre G, Cmero M, Tothill RW, Johnstone RW, Shackleton M, Papenfuss AT (2014) Socrates: identification of genomic rearrangements in tumour genomes by re-aligning soft clipped reads. Bioinformatics 30(8):1064–1072.  https://doi.org/10.1093/bioinformatics/btt767 CrossRefPubMedPubMedCentralGoogle Scholar
  114. Sears ER (1939) Cytogenetic studies with polyploid species of wheat. I. chromosomal aberrations in the progeny of a haploid of Triticum Vulgare. Genetics 24(4):509–523PubMedPubMedCentralGoogle Scholar
  115. Sharp AJ, Cheng Z, Eichler EE (2006) Structural variation of the human genome. Annu Rev Genomics Hum Genet 7:407–442.  https://doi.org/10.1146/annurev.genom.7.080505.115618 CrossRefPubMedGoogle Scholar
  116. Sharpe AG, Parkin IA, Keith DJ, Lydiate DJ (1995) Frequent nonreciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus). Genome 38(6):1112–1121CrossRefGoogle Scholar
  117. Sieber A-N, Longin CFH, Leiser WL, Würschum T (2016) Copy number variation of CBF-A14 at the Fr-A2 locus determines frost tolerance in winter durum wheat. Theor Appl Genet 129(6):1087–1097.  https://doi.org/10.1007/s00122-016-2685-3 CrossRefPubMedGoogle Scholar
  118. Singleton AB (2003) Synuclein locus triplication causes Parkinson’s disease. Science 302(5646):841.  https://doi.org/10.1126/science.1090278 CrossRefPubMedGoogle Scholar
  119. Snowdon RJ (2007) Cytogenetics and genome analysis in Brassica crops. Chromosome Res 15(1):85–95.  https://doi.org/10.1007/s10577-006-1105-y CrossRefPubMedGoogle Scholar
  120. Springer NM, Ying K, Fu Y, Ji T, Yeh C-T, Jia Y, Wu W, Richmond T, Kitzman J, Rosenbaum H, Iniguez AL, Barbazuk WB, Jeddeloh JA, Nettleton D, Schnable PS, Ecker JR (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5(11):e1000734.  https://doi.org/10.1371/journal.pgen.1000734 CrossRefPubMedPubMedCentralGoogle Scholar
  121. Stankiewicz P, Lupski JR (2010) Structural variation in the human genome and its role in disease. Annu Rev Med 61(1):437–455.  https://doi.org/10.1146/annurev-med-100708-204735 CrossRefPubMedGoogle Scholar
  122. Stein N, Mascher M (2019) Capturing pangenome diversity for breeding: a case study in barley. Theor Appl Genet (to be published in same special issue) Google Scholar
  123. Stein A, Coriton O, Rousseau-Gueutin M, Samans B, Schiessl SV, Obermeier C, Parkin IAP, Chèvre A-M, Snowdon RJ (2017) Mapping of homoeologous chromosome exchanges influencing quantitative trait variation in Brassica napus. Plant Biotechnol J 15(11):1478–1489.  https://doi.org/10.1111/pbi.12732 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Sun S, Zhou Y, Chen J, Shi J, Zhao H, Zhao H, Song W, Zhang M, Cui Y, Dong X, Liu H, Ma X, Jiao Y, Wang B, Wei X, Stein JC, Glaubitz JC, Lu F, Yu G, Liang C, Fengler K, Li B, Rafalski A, Schnable PS, Ware DH, Buckler ES, Lai J (2018) Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nat Genet 50(9):1289–1295.  https://doi.org/10.1038/s41588-018-0182-0 CrossRefPubMedGoogle Scholar
  125. Sutton T, Baumann U, Hayes J, Collins NC, Shi B-J, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M, Langridge P (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318(5855):1446–1449.  https://doi.org/10.1126/science.1146853 CrossRefPubMedGoogle Scholar
  126. Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC, Ware D, Springer NM (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res 20(12):1689–1699.  https://doi.org/10.1101/gr.109165.110 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Tang H, Woodhouse MR, Cheng F, Schnable JC, Pedersen BS, Conant G, Wang X, Freeling M, Pires JC (2012) Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics 190(4):1563–1574.  https://doi.org/10.1534/genetics.111.137349 CrossRefPubMedPubMedCentralGoogle Scholar
  128. Taylor CM, Kamphuis LG, Zhang W, Garg G, Berger JD, Mousavi-Derazmahalleh M, Bayer PE, Edwards D, Singh KB, Cowling WA, Nelson MN (2018) INDEL variation in the regulatory region of the major flowering time gene LanFTc1 is associated with vernalization response and flowering time in narrow-leafed lupin (Lupinus angustifolius L.). Plant Cell Environ.  https://doi.org/10.1111/pce.13320 CrossRefPubMedGoogle Scholar
  129. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, DeBoy RT, Davidsen TM, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, Connor KJB, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA 102(39):13950.  https://doi.org/10.1073/pnas.0506758102 CrossRefPubMedGoogle Scholar
  130. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796.  https://doi.org/10.1038/35048692 CrossRefGoogle Scholar
  131. The International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345(6194):1251788.  https://doi.org/10.1126/science.1251788 CrossRefGoogle Scholar
  132. Tranchida-Lombardo V, Aiese Cigliano R, Anzar I, Landi S, Palombieri S, Colantuono C, Bostan H, Termolino P, Aversano R, Batelli G, Cammareri M, Carputo D, Chiusano ML, Conicella C, Consiglio F, D’Agostino N, de Palma M, Di Matteo A, Grandillo S, Sanseverino W, Tucci M, Grillo S (2018) Whole-genome re-sequencing of two Italian tomato landraces reveals sequence variations in genes associated with stress tolerance, fruit quality and long shelf-life traits. DNA Res 25(2):149–160.  https://doi.org/10.1093/dnares/dsx045 CrossRefPubMedGoogle Scholar
  133. Tseng S-H, Peng S-F, Cheng Y-M (2017) Analysis of B chromosome nondisjunction induced by the r-X1 deficiency in maize. Chromosome Res 42(2):223.  https://doi.org/10.1007/s10577-017-9567-7 CrossRefGoogle Scholar
  134. Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homologous recombination in four mapping populations of Brassica napus L. Genetics 169(2):967–979.  https://doi.org/10.1534/genetics.104.033209 CrossRefPubMedPubMedCentralGoogle Scholar
  135. Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45(9):1097–1102.  https://doi.org/10.1038/ng.2725 CrossRefPubMedGoogle Scholar
  136. Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K (2009) The flowering world: a tale of duplications. Trends Plant Sci 14(12):680–688.  https://doi.org/10.1016/j.tplants.2009.09.001 CrossRefPubMedGoogle Scholar
  137. Vialette-Guiraud ACM, Adam H, Finet C, Jasinski S, Jouannic S, Scutt CP (2011) Insights from ANA-grade angiosperms into the early evolution of CUP-SHAPED COTYLEDON genes. Ann Bot 107(9):1511–1519.  https://doi.org/10.1093/aob/mcr024 CrossRefPubMedPubMedCentralGoogle Scholar
  138. Villareal RL, Toro E, Mujeeb-Kazi A, Rajaram S (1995) The 1BL/1RS chromosome translocation effect on yield characteristics in a Triticum aestivum L. cross. Plant Breed 114(6):497–500.  https://doi.org/10.1111/j.1439-0523.1995.tb00843.x CrossRefGoogle Scholar
  139. Voss-Fels K, Snowdon RJ (2016) Understanding and utilizing crop genome diversity via high-resolution genotyping. Plant Biotechnol J 14(4):1086–1094.  https://doi.org/10.1111/pbi.12456 CrossRefPubMedGoogle Scholar
  140. Wang W, Wang S, Hou C, Xing Y, Cao J, Wu K, Liu C, Zhang D, Zhang L, Zhang Y, Zhou H (2014) Genome-wide detection of copy number variations among diverse horse breeds by array CGH. PLoS ONE 9(1):e86860.  https://doi.org/10.1371/journal.pone.0086860 CrossRefPubMedPubMedCentralGoogle Scholar
  141. Wang Y, Xiong G, Hu J, Jiang L, Yu H, Xu J, Fang Y, Zeng L, Xu E, Xu J, Ye W, Meng X, Liu R, Chen H, Jing Y, Wang Y, Zhu X, Li J, Qian Q (2015) Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat Genet 47:944.  https://doi.org/10.1038/ng.3346 CrossRefPubMedGoogle Scholar
  142. Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48(10):1233–1241.  https://doi.org/10.1038/ng.3636 CrossRefPubMedGoogle Scholar
  143. Wulff BBH, Moscou MJ (2014) Strategies for transferring resistance into wheat: from wide crosses to GM cassettes. Front Plant Sci 5:692.  https://doi.org/10.3389/fpls.2014.00692 CrossRefPubMedPubMedCentralGoogle Scholar
  144. Würschum T, Boeven PHG, Langer SM, Longin CFH, Leiser WL (2015) Multiply to conquer: copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat. BMC Genet 16(1):949.  https://doi.org/10.1186/s12863-015-0258-0 CrossRefGoogle Scholar
  145. Würschum T, Longin CFH, Hahn V, Tucker MR, Leiser WL (2016) Copy number variations of CBF genes at the Fr-A2 locus are essential components of winter hardiness in wheat. Plant J 89(4):764–773.  https://doi.org/10.1111/tpj.13424 CrossRefGoogle Scholar
  146. Xiong Z, Pires JC (2011) Karyotype and identification of all homoeologous chromosomes of allopolyploid Brassica napus and its diploid progenitors. Genetics 187(1):37–49.  https://doi.org/10.1534/genetics.110.122473 CrossRefPubMedPubMedCentralGoogle Scholar
  147. Xiong Z, Gaeta RT, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci USA 108(19):7908–7913.  https://doi.org/10.1073/pnas.1014138108 CrossRefPubMedGoogle Scholar
  148. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708.  https://doi.org/10.1038/nature04920 CrossRefPubMedGoogle Scholar
  149. Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, Li J, He W, Zhang G, Zheng X, Zhang F, Li Y, Yu C, Kristiansen K, Zhang X, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30(1):105–111.  https://doi.org/10.1038/nbt.2050 CrossRefGoogle Scholar
  150. Yao W, Li G, Zhao H, Wang G, Lian X, Xie W (2015) Exploring the rice dispensable genome using a metagenome-like assembly strategy. Genome Biol 16:187.  https://doi.org/10.1186/s13059-015-0757-3 CrossRefPubMedPubMedCentralGoogle Scholar
  151. Yang S, Li J, Zhang X, Zhang Q, Huang J, Chen J-Q, Hartl DL, Tian D (2013) Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease. Proc Natl Acad Sci USA 110(46):18572–18577.  https://doi.org/10.1073/pnas.1318211110 CrossRefPubMedGoogle Scholar
  152. Ye K, Schulz MH, Long Q, Apweiler R, Ning Z (2009) Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25(21):2865–2871.  https://doi.org/10.1093/bioinformatics/btp394 CrossRefPubMedPubMedCentralGoogle Scholar
  153. Yu P, Wang C, Xu Q, Feng Y, Yuan X, Yu H, Wang Y, Tang S, Wei X (2011) Detection of copy number variations in rice using array-based comparative genomic hybridization. BMC Genomics 12(1):372.  https://doi.org/10.1186/1471-2164-12-372 CrossRefPubMedPubMedCentralGoogle Scholar
  154. Yu P, Wang C-H, Xu Q, Feng Y, Yuan X-P, Yu H-Y, Wang Y-P, Tang S-X, Wei X-H (2013) Genome-wide copy number variations in Oryza sativa L. BMC Genomics 14(1):649.  https://doi.org/10.1186/1471-2164-14-649 CrossRefPubMedPubMedCentralGoogle Scholar
  155. Zhang Z, Mao L, Chen H, Bu F, Li G, Sun J, Li S, Sun H, Jiao C, Blakely R, Pan J, Cai R, Luo R, Van de Peer Y, Jacobsen E, Fei Z, Huang S (2015) Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber. Plant Cell 27(6):1595–1604.  https://doi.org/10.1105/tpc.114.135848 CrossRefPubMedPubMedCentralGoogle Scholar
  156. Zhao Q, Feng Q, Lu H, Li Y, Wang A, Tian Q, Zhan Q, Lu Y, Zhang L, Huang T, Wang Y, Fan D, Zhao Y, Wang Z, Zhou C, Chen J, Zhu C, Li W, Weng Q, Xu Q, Wang Z-X, Wei X, Han B, Huang X (2018) Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet 50(2):278–284.  https://doi.org/10.1038/s41588-018-0041-z CrossRefPubMedGoogle Scholar
  157. Zheng L-Y, Guo X-S, He B, Sun L-J, Peng Y, Dong S-S, Liu T-F, Jiang S, Ramachandran S, Liu C-M, Jing H-C (2011) Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol 12(11):R114.  https://doi.org/10.1186/gb-2011-12-11-r114 CrossRefPubMedPubMedCentralGoogle Scholar
  158. Zhou P, Silverstein KAT, Ramaraj T, Guhlin J, Denny R, Liu J, Farmer AD, Steele KP, Stupar RM, Miller JR, Tiffin P, Mudge J, Young ND (2017) Exploring structural variation and gene family architecture with de novo assemblies of 15 Medicago genomes. BMC Genomics 18(1):261.  https://doi.org/10.1186/s12864-017-3654-1 CrossRefPubMedPubMedCentralGoogle Scholar
  159. Żmieńko A, Samelak A, Kozłowski P, Figlerowicz M (2014) Copy number polymorphism in plant genomes. Theor Appl Genet 127(1):1–18.  https://doi.org/10.1007/s00122-013-2177-7 CrossRefPubMedGoogle Scholar
  160. Zou J, Hu D, Mason AS, Shen X, Wang X, Wang N, Grandke F, Wang M, Chang S, Snowdon RJ, Meng J (2018) Genetic changes in a novel breeding population of Brassica napus synthesized from hundreds of crosses between B. rapa and B. carinata. Plant Biotechnol J 16(2):507–519.  https://doi.org/10.1111/pbi.12791 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plant BreedingJustus Liebig UniversityGiessenGermany
  2. 2.Agriculture and Agri-Food CanadaSaskatoonCanada

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