Sequence Diversity and Structural Variation

  • María Muñoz-AmatriaínEmail author
  • Martin Mascher
Part of the Compendium of Plant Genomes book series (CPG)


Barley is a phenotypically and genetically diverse crop that has adapted successfully to many agricultural environments. Moreover, its wild progenitor species is still abundant in Western Asia and provides a large untapped reservoir of allelic variation. Deriving a complete inventory of sequence variants of the barley genome for targeted utilization of natural diversity in crop improvement has long been a key goal of barley research. While the assessment of genetic diversity has traditionally focused on a few selected—mostly genic—loci, recent technology advances have made it possible to simultaneously obtain genome-wide sequence information for genes and noncoding regions alike. In addition to small-scale sequence changes, larger scale structural variation such as presence–absence or copy number variants are widespread throughout the barley genome. These types of variation can affect large genomic regions, possibly containing multiple genes or adjacent regulatory regions. Here, we review the recent progress on assaying genetic variants, large and small, in barley, understanding the mutational processes underlying them, and their relationship to phenotype and ultimately crop performance.


Barley Copy number variation (CNV) Genetic diversity Genome-wide association studies (GWAS) Structural variation Single-nucleotide polymorphism (SNP) 


  1. Agmon N, Pur S, Liefshitz B, Kupiec M (2009) Analysis of repair mechanism choice during homologous recombination. Nucleic Acids Res 37:5081–5092CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aliyeva-Schnorr L, Beier S, Karafiatova M, Schmutzer T, Scholz U, Dolezel J, Stein N, Houben A (2015) Cytogenetic mapping with centromeric bacterial artificial chromosomes contigs shows that this recombination-poor region comprises more than half of barley chromosome 3H. Plant J 84:385–394CrossRefPubMedGoogle Scholar
  3. Alkan C, Coe BP, Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12:363–376CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ames N, Dreiseitl A, Steffenson BJ, Muehlbauer GJ (2015) Mining wild barley for powdery mildew resistance. Plant Pathol 64:1396–1406CrossRefGoogle Scholar
  5. Badr A, Sch R, El Rabey H, Effgen S, Ibrahim H, Pozzi C, Rohde W, Salamini F (2000) On the origin and domestication history of barley (Hordeum vulgare). Mol Biol Evol 17:499–510CrossRefPubMedGoogle Scholar
  6. Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356:519–520CrossRefPubMedGoogle Scholar
  7. 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 4Google Scholar
  8. Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65:505–530CrossRefPubMedGoogle Scholar
  9. Berger GL, Liu S, Hall MD, Brooks WS, Chao S, Muehlbauer GJ, Baik B-K, Steffenson B, Griffey CA (2013) Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor Appl Genet 126:693–710CrossRefPubMedGoogle Scholar
  10. Bernardo R (2017) Prospective targeted recombination and genetic gains for quantitative traits in maize. Plant Genome 10Google Scholar
  11. Bockelman HE, Valkoun J (2010) Barley germplasm conservation and resources. Barley: improvement, production, and uses. Wiley-Blackwell, Oxford, UK, pp 144–159Google Scholar
  12. Cantalapiedra CP, Contreras-Moreira B, Silvar C, Perovic D, Ordon F, Gracia MP, Igartua E, Casas AM (2016) A cluster of nucleotide-binding site–leucine-rich repeat genes resides in a barley powdery mildew resistance quantitative trait loci on 7HL. Plant Genome 9Google Scholar
  13. Carvalho CM, Lupski JR (2016) Mechanisms underlying structural variant formation in genomic disorders. Nat Rev Genet 17:224CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chaisson MJ, Huddleston J, Dennis MY, Sudmant PH, Malig M, Hormozdiari F, Antonacci F, Surti U, Sandstrom R, Boitano M (2015) Resolving the complexity of the human genome using single-molecule sequencing. Nature 517:608–611CrossRefPubMedGoogle Scholar
  15. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303PubMedPubMedCentralGoogle Scholar
  16. Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szucs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, Deyoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cockram J, Jones H, Leigh FJ, O’Sullivan D, Powell W, Laurie DA, Greenland AJ (2007) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J Exp Bot 58:1231–1244CrossRefPubMedGoogle Scholar
  18. 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 44:1388–1392CrossRefPubMedGoogle Scholar
  19. Dahleen LS, Bregitzer P, Mornhinweg D, Klos KE (2015) Genetic diversity for Russian wheat aphid resistance as determined by genome-wide association mapping and inheritance in progeny. Crop Sci 55:1925–1933CrossRefGoogle Scholar
  20. Dempewolf H, Baute G, Anderson J, Kilian B, Smith C, Guarino L (2017) Past and future of wild relatives in crop breeding. Crop Sci 57:1070–1082CrossRefGoogle Scholar
  21. Fang Z, Gonzales AM, Clegg MT, Smith KP, Muehlbauer GJ, Steffenson BJ, Morrell PL (2014) Two genomic regions contribute disproportionately to geographic differentiation in wild barley. G3-Genes Genom Genet 4:1193–1203Google Scholar
  22. Filler Hayut S, Melamed Bessudo C, Levy AA (2017) Targeted recombination between homologous chromosomes for precise breeding in tomato. Nat Commun 8:15605CrossRefPubMedPubMedCentralGoogle Scholar
  23. Francia E, Rizza F, Cattivelli L, Stanca A, Galiba G, Toth B, Hayes P, Skinner J, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680CrossRefPubMedGoogle Scholar
  24. Francia E, Morcia C, Pasquariello M, Mazzamurro V, Milc JA, Rizza F, Terzi V, Pecchioni N (2016) Copy number variation at the HvCBF4–HvCBF2 genomic segment is a major component of frost resistance in barley. Plant Mol Biol 92:161–175CrossRefPubMedGoogle Scholar
  25. Fu D, Szűcs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273:54–65CrossRefPubMedGoogle Scholar
  26. Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, Sato K, Nakazono M, Ma JF (2012) Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun 3:713CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gill KS, Gill BS, Endo TR, Taylor T (1996) Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144:1883–1891PubMedPubMedCentralGoogle Scholar
  28. Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH (2009) A first-generation haplotype map of maize. Science 326:1115–1117CrossRefPubMedPubMedCentralGoogle Scholar
  29. Graebner RC, Wise M, Cuesta-Marcos A, Geniza M, Blake T, Blake VC, Butler J, Chao S, Hole DJ, Horsley R (2015) Quantitative trait loci associated with the tocochromanol (vitamin E) pathway in barley. PLoS One 10:e0133767CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gutiérrez L, Cuesta-Marcos A, Castro AJ, von Zitzewitz J, Schmitt M, Hayes PM (2011) Association mapping of malting quality quantitative trait loci in winter barley: positive signals from small germplasm arrays. Plant Genome 4:256–272CrossRefGoogle Scholar
  31. Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10:551CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hodgkinson A, Eyre-Walker A (2011) Variation in the mutation rate across mammalian genomes. Nat Rev Genet 12:756CrossRefPubMedGoogle Scholar
  33. Hudson RR, Kaplan NL (1995) Deleterious background selection with recombination. Genetics 141:1605–1617PubMedPubMedCentralGoogle Scholar
  34. International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716CrossRefGoogle Scholar
  35. 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 6:685–702CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kidwell MG, Lisch D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94:7704–7711CrossRefPubMedGoogle Scholar
  37. 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 121:21–35CrossRefPubMedGoogle Scholar
  38. Konishi T, Linde-Laursen I (1988) Spontaneous chromosomal rearrangements in cultivated and wild barleys. Theor Appl Genet 75:237–243CrossRefGoogle Scholar
  39. Künzel G (1982) Differences between genetic and physical centromere distances in the case of two genes for male sterility in barley. Theor Appl Genet 64:25–29CrossRefPubMedGoogle Scholar
  40. Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412PubMedPubMedCentralGoogle Scholar
  41. 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 30:771–776CrossRefPubMedGoogle Scholar
  42. Lee S-I, Kim N-S (2014) Transposable elements and genome size gariations in plants. Genomics Inform 12:87–97CrossRefPubMedPubMedCentralGoogle Scholar
  43. Looseley ME, Bayer M, Bull H, Ramsay L, Thomas W, Booth A, De La Fuente Canto C, Morris J, Hedley PE, Russell J (2017) Association mapping of diastatic power in UK winter and spring barley by exome sequencing of phenotypically contrasting variety sets. Front Plant Sci 8Google Scholar
  44. Loscos J, Igartua E, Contreras-Moreira B, Gracia MP, Casas AM (2014) HvFT1 polymorphism and effect—survey of barley germplasm and expression analysis. Front Plant Sci 5:251CrossRefPubMedPubMedCentralGoogle Scholar
  45. Marroni F, Pinosio S, Morgante M (2014) Structural variation and genome complexity: is dispensable really dispensable? Curr Opin Plant Biol 18:31–36CrossRefPubMedGoogle Scholar
  46. Mascher M, Muehlbauer GJ, Rokhsar DS, Chapman J, Schmutz J, Barry K, Muñoz-Amatriaín M, Close TJ, Wise RP, Schulman AH, Himmelbach A, Mayer KFX, Scholz U, Poland JA, Stein N, Waugh R (2013a) Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ). Plant J 76:718–727CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 KF, Flavell AJ, Muehlbauer GJ, Waugh R, Jeddeloh JA, Stein N (2013b) Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J 76:494–505CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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 544:427–433CrossRefPubMedGoogle Scholar
  49. Massman J, Cooper B, Horsley R, Neate S, Dill-Macky R, Chao S, Dong Y, Schwarz P, Muehlbauer G, Smith K (2011) Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol Breed 27:439–454CrossRefGoogle Scholar
  50. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23:23–35CrossRefGoogle Scholar
  51. 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 159:1295–1308CrossRefPubMedPubMedCentralGoogle Scholar
  52. Morgante M, De Paoli M, Slobodanka R (2007) Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10:149–155CrossRefPubMedGoogle Scholar
  53. 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:R58CrossRefPubMedPubMedCentralGoogle Scholar
  54. Muñoz-Amatriaín M, Cuesta-Marcos A, Endelman JB, Comadran J, Bonman JM, Bockelman HE, Chao S, Russell J, Waugh R, Hayes PM (2014a) The USDA barley core collection: genetic diversity, population structure, and potential for genome-wide association studies. PLoS One 9:e94688CrossRefPubMedPubMedCentralGoogle Scholar
  55. Muñoz-Amatriaín M, Cuesta-Marcos A, Hayes PM, Muehlbauer GJ (2014b) Barley genetic variation: implications for crop improvement. Brief Funct Genomics 13:341–350CrossRefPubMedGoogle Scholar
  56. Muñoz-Amatriaín M, Lonardi S, Luo M, Madishetty K, Svensson JT, Moscou MJ, Wanamaker S, Jiang T, Kleinhofs A, Muehlbauer GJ, Wise RP, Stein N, Ma Y, Rodriguez E, Kudrna D, Bhat PR, Chao S, Condamine P, Heinen S, Resnik J, Wing R, Witt HN, Alpert M, Beccuti M, Bozdag S, Cordero F, Mirebrahim H, Ounit R, Wu Y, You F, Zheng J, Šimková H, Doležel J, Grimwood J, Schmutz J, Duma D, Altschmied L, Blake T, Bregitzer P, Cooper L, Dilbirligi M, Falk A, Feiz L, Graner A, Gustafson P, Hayes PM, Lemaux P, Mammadov J, Close TJ (2015) Sequencing of 15 622 gene-bearing BACs clarifies the gene-dense regions of the barley genome. Plant J 84:216–227CrossRefPubMedPubMedCentralGoogle Scholar
  57. Neumann K, Zhao Y, Chu J, Keilwagen J, Reif JC, Kilian B, Graner A (2017) Genetic architecture and temporal patterns of biomass accumulation in spring barley revealed by image analysis. BMC Plant Biol 17:137CrossRefPubMedPubMedCentralGoogle Scholar
  58. Neupane A, Tamang P, Brueggeman R, Friesen T (2015) Evaluation of a barley core collection for spot form net blotch reaction reveals distinct genotype-specific pathogen virulence and host susceptibility. Phytopathology 105:509–517CrossRefPubMedGoogle Scholar
  59. Nice LM, Steffenson BJ, Blake TK, Horsley RD, Smith KP, Muehlbauer GJ (2017) Mapping agronomic traits in a wild barley advanced backcross–nested association mapping population. Crop SciGoogle Scholar
  60. Nielsen R, Paul JS, Albrechtsen A, Song YS (2011) Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet 12:443–451CrossRefPubMedPubMedCentralGoogle Scholar
  61. Nitcher R, Distelfeld A, Tan C, Yan L, Dubcovsky J (2013) Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley. Mol Genet Genomics 288:261–275CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA, Haseneyer G, Kilian B, Graner A (2012) Genome-wide association studies for agronomical traits in a world wide spring barley collection. BMC Plant Biol 12:16CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pasquariello M, Barabaschi D, Himmelbach A, Steuernagel B, Ariyadasa R, Stein N, Gandolfi F, Tenedini E, Bernardis I, Tagliafico E (2014) The barley Frost resistance-H2 locus. Funct Integr Genomics 14:85–100CrossRefPubMedGoogle Scholar
  64. Pinosio S, Giacomello S, Faivre-Rampant P, Taylor G, Jorge V, le Paslier MC, Zaina G, Bastien C, Cattonaro F, Marroni F, Morgante M (2016) Characterization of the poplar pan-genome by genome-wide identification of structural variation. Mol Biol Evol 33:2706–2719CrossRefPubMedPubMedCentralGoogle Scholar
  65. 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:e32253CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 162:527–539CrossRefPubMedGoogle Scholar
  67. Ramage R, Burnham C, Hagberg A (1961) A summary of translocation studies in barley. Crop Sci 1:277–279CrossRefGoogle Scholar
  68. Rey M-D, Calderón MC, Prieto P (2015) The use of the ph1b mutant to induce recombination between the chromosomes of wheat and barley. Front Plant Sci 6:160CrossRefPubMedPubMedCentralGoogle Scholar
  69. Richards JK, Friesen TL, Brueggeman RS (2017) Association mapping utilizing diverse barley lines reveals net form net blotch seedling resistance/susceptibility loci. Theor Appl Genet 130:915–927CrossRefPubMedGoogle Scholar
  70. Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ (2010) Association mapping of spot blotch resistance in wild barley. Mol Breed 26:243–256CrossRefPubMedPubMedCentralGoogle Scholar
  71. 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 191:564–578CrossRefPubMedGoogle Scholar
  72. 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 48:1024–1030CrossRefPubMedGoogle Scholar
  73. Sadhu MJ, Bloom JS, Day L, Kruglyak L (2016) CRISPR-directed mitotic recombination enables genetic mapping without crosses. Science 352:1113–1116CrossRefPubMedPubMedCentralGoogle Scholar
  74. Scherrer B, Isidore E, Klein P, Kim JS, Bellec A, Chalhoub B, Keller B, Feuillet C (2005) Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell 17:361–374CrossRefPubMedPubMedCentralGoogle Scholar
  75. Springer NM, Ying K, Fu Y, Ji T, Yeh C-T, Jia Y, Wu W, Richmond T, Kitzman J, Rosenbaum H (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5:e1000734CrossRefPubMedPubMedCentralGoogle Scholar
  76. Steffenson BJ, Olivera P, Roy JK, Jin Y, Smith KP, Muehlbauer GJ (2007) A walk on the wild side: mining wild wheat and barley collections for rust resistance genes. Crop Pasture Sci 58:532–544CrossRefGoogle Scholar
  77. Stein N, Steuernagel B (2014) Advances in sequencing the barley genome. In: Genomics of plant genetic resources. SpringerGoogle Scholar
  78. Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51:308–321CrossRefPubMedGoogle Scholar
  79. 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 318:1446–1449CrossRefPubMedGoogle Scholar
  80. Szűcs P, Skinner JS, Karsai I, Cuesta-Marcos A, Haggard KG, Corey AE, Chen TH, Hayes PM (2007) Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity. Mol Genet Genomics 277:249–261CrossRefPubMedGoogle Scholar
  81. Taketa S, Amano S, Tsujino Y, Sato T, Saisho D, Kakeda K, Nomura M, Suzuki T, Matsumoto T, Sato K, Kanamori H, Kawasaki S, Takeda K (2008) Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc Natl Acad Sci USA 105:4062–4067CrossRefPubMedGoogle Scholar
  82. Tamang P, Neupane A, Mamidi S, Friesen T, Brueggeman R (2015) Association mapping of seedling resistance to spot form net blotch in a worldwide collection of barley. Phytopathology 105:500–508CrossRefPubMedGoogle Scholar
  83. Tang H, Lyons E, Town CD (2015) Optical mapping in plant comparative genomics. GigaScience 4:3CrossRefPubMedPubMedCentralGoogle Scholar
  84. Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066CrossRefPubMedGoogle Scholar
  85. Tondelli A, Xu X, Moragues M, Sharma R, Schnaithmann F, Ingvardsen C, Manninen O, Comadran J, Russell J, Waugh R, Schulman AH, Pillen K, Rasmussen SK, Kilian B, Cattivelli L, Thomas WTB, Flavell AJ (2013) Structural and temporal variation in genetic diversity of European spring two-row barley cultivars and association mapping of quantitative traits. Plant Genome 6Google Scholar
  86. Visioni A, Tondelli A, Francia E, Pswarayi A, Malosetti M, Russell J, Thomas W, Waugh R, Pecchioni N, Romagosa I, Comadran J (2013) Genome-wide association mapping of frost tolerance in barley (Hordeum vulgare L.). BMC Genomics 14:424CrossRefPubMedPubMedCentralGoogle Scholar
  87. von Zitzewitz J, Szűcs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen TH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59:449–467CrossRefGoogle Scholar
  88. von Zitzewitz J, Cuesta-Marcos A, Condon F, Castro AJ, Chao S, Corey A, Filichkin T, Fisk SP, Gutierrez L, Haggard K (2011) The genetics of winterhardiness in barley: perspectives from genome-wide association mapping. Plant Genome 4:76–91CrossRefGoogle Scholar
  89. Wang Q, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci USA 103:17644–17649CrossRefPubMedGoogle Scholar
  90. Wang C, Hu S, Gardner C, Lubberstedt T (2017a) Emerging avenues for utilization of exotic germplasm. Trends Plant Sci 22:624–637CrossRefPubMedGoogle Scholar
  91. Wang R, Leng Y, Ali S, Wang M, Zhong S (2017b) Genome-wide association mapping of spot blotch resistance to three different pathotypes of Cochliobolus sativus in the USDA barley core collection. Mol Breed 37:44CrossRefGoogle Scholar
  92. Weischenfeldt J, Symmons O, Spitz F, Korbel JO (2013) Phenotypic impact of genomic structural variation: insights from and for human disease. Nat Rev Genet 14:125–138CrossRefPubMedGoogle Scholar
  93. Woodhouse MR, Schnable JC, Pedersen BS, Lyons E, Lisch D, Subramaniam S, Freeling M (2010) Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homeologs. PLoS Biol 8:e1000409CrossRefPubMedPubMedCentralGoogle Scholar
  94. Yamasaki M, Tenaillon MI, Bi IV, Schroeder SG, Sanchez-Villeda H, Doebley JF, Gaut BS, McMullen MD (2005) A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17:2859–2872CrossRefPubMedPubMedCentralGoogle Scholar
  95. Yu P, Wang C, Xu Q, Feng Y, Yuan X, Yu H, Wang Y, Tang S (2011) Detection of copy number variations in rice using array-based comparative genomic hybridization. BMC Genomics 12:372CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Botany and Plant SciencesUniversity of California RiversideRiversideUSA
  2. 2.Leibniz Institute of Plant Genetic and Crop Plant Research (IPK) GaterslebenSeelandGermany
  3. 3.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany

Personalised recommendations