Advertisement

Theoretical and Applied Genetics

, Volume 130, Issue 12, pp 2479–2490 | Cite as

Copy number variation and disease resistance in plants

  • Aria Dolatabadian
  • Dhwani Apurva Patel
  • David Edwards
  • Jacqueline BatleyEmail author
Review

Abstract

Plant genome diversity varies from single nucleotide polymorphisms to large-scale deletions, insertions, duplications, or re-arrangements. These re-arrangements of sequences resulting from duplication, gains or losses of DNA segments are termed copy number variations (CNVs). During the last decade, numerous studies have emphasized the importance of CNVs as a factor affecting human phenotype; in particular, CNVs have been associated with risks for several severe diseases. In plants, the exploration of the extent and role of CNVs in resistance against pathogens and pests is just beginning. Since CNVs are likely to be associated with disease resistance in plants, an understanding of the distribution of CNVs could assist in the identification of novel plant disease-resistance genes. In this paper, we review existing information about CNVs; their importance, role and function, as well as their association with disease resistance in plants.

Notes

Acknowledgements

The authors thank the Australian Research Council Projects FT130100604, DP1601004497, LP140100537, LP160100030 and LP130100925.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

References

  1. Abel HJ, Duncavage EJ (2013) Detection of structural DNA variation from next generation sequencing data: a review of informatic approaches. Cancer Genet 206:432–440PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alkan C, Coe BP, Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12:363–376PubMedPubMedCentralCrossRefGoogle Scholar
  3. Armour JA, Sismani C, Patsalis PC, Cross G (2000) Measurement of locus copy number by hybridisation with amplifiable probes. Nucleic Acids Res 28:605–609PubMedPubMedCentralCrossRefGoogle Scholar
  4. Armour JA, Palla R, Zeeuwen PL, den Heijer M, Schalkwijk J, Hollox EJ (2007) Accurate, high-throughput typing of copy number variation using paralogue ratios from dispersed repeats. Nucleic Acids Res 35:1–8CrossRefGoogle Scholar
  5. Bai H, Cao Y, Quan J et al (2013) Identifying the genome-wide sequence variations and developing new molecular markers for genetics research by re-sequencing a landrace cultivar of foxtail millet. PLoS One 8:e73514PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bai Z, Chen J, Liao Y, Wang M, Liu R, Ge S et al (2016) The impact and origin of copy number variations in the Oryza species. BMC Genom 17:261CrossRefGoogle Scholar
  7. Bayer PE, Ruperao P, Mason AS, Stiller J, Chan CKK, Hayashi S, Long Y, Meng J, Sutton T, Visendi P, Varshney RK, Batley J, Edwards D (2015) High resolution skim genotyping by sequencing reveals the distribution of crossovers and gene conversions in Cicer arietinum and Brassica napus. Theor Appl Genet 128:1039–1047PubMedCrossRefGoogle Scholar
  8. Belo A, Beatty MK, Hondred D et al (2010) Allelic genome structural variations in maize detected by array comparative genome hybridization. Theor Appl Genet 120:355–367PubMedCrossRefGoogle Scholar
  9. Berglund J, Nevalainen EM, Molin A-M, Perloski M, The Lupa Consortium, Andre C, Zody MC, Sharpe T, Hitte C, Lindblad-Toh K, Lohi H, Webster MT (2012) Novel origins of copy number variation in the dog genome. Genome Biol 13:R73PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bertioli DJ, Leal-Bertioli SCM, Lion MB, Santos VL, Pappas G Jr, Cannon SB, Guimaraes PM (2003) A large scale analysis of resistance gene homologues in Arachis. Mol Gen Genom 270:34–45CrossRefGoogle Scholar
  11. Bickhart DM, Hou Y, Schroeder SG, Alkan C, Cardone MF, Matukumalli LK, Song J, Schnabel RD, Ventura M, Taylor JF et al (2012) Copy number variation of individual cattle genomes using next-generation sequencing. Genome Res 22:778–790PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bignell GR, Santarius T, Pole JCM et al (2007) Architectures of somatic genomic rearrangement in human cancer amplicons at sequence-level resolution. Genome Res 17:1296–1303PubMedPubMedCentralCrossRefGoogle Scholar
  13. Boocock J, Chagné D, Merriman TR, Black MA (2015) The distribution and impact of common copy-number variation in the genome of the domesticated apple, Malus × domestica Borkh. BMC Genom 16:848CrossRefGoogle Scholar
  14. Bradeen JM, Iorizzo M, Mollov DS, Raasch J, Kramer LC, Millett BP, Austin-Phillips S, Jiang J, Carputo D (2009) Higher copy numbers of the potato RB transgene correspond to enhanced transcript and late blight resistance levels. Mol Plant Microbe Interact 22:437–446PubMedCrossRefGoogle Scholar
  15. Campbell PC, Stephens PJ, Pleasance ED et al (2008) Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 40:722–729PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, Wang X, Ott F, Müller J, Alonso-Blanco C, Borgwardt K, Schmid KJ, Weigel D (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43:956–963PubMedCrossRefGoogle Scholar
  17. Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953PubMedCrossRefGoogle Scholar
  18. Chen K, Wallis JW, Mclellan MD, Larson DE, Kalicki JM, Pohl CS et al (2009) Break dancer: an algorithm for high-resolution mapping of genomic structural variation. Nat Methods 6:677–681PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chia JM, 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 44:803–807PubMedCrossRefGoogle Scholar
  20. Cong B, Barrero LS, Tanksley SD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804PubMedCrossRefGoogle Scholar
  21. Conrad DF, Andrews TD, Carter NP, Hurles ME, Pritchard JKA (2006) High-resolution survey of deletion polymorphism in the human genome. Nat Genet 38:75–81PubMedCrossRefGoogle Scholar
  22. Cook DE, Lee TG, Guo X et al (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209PubMedCrossRefGoogle Scholar
  23. Dalton-Morgan J, Hayward A, Alamery S, Tollenaere R, Mason AS, Campbell E, Patel D, Lorenc MT, Yi B, Long Y, Meng J, Raman R, Raman H, Lawley C, Edwards D, Batley J (2014) A high-throughput SNP array in the amphidiploid species Brassica napus shows diversity in resistance genes. Funct Integr Genom 14:643–655CrossRefGoogle Scholar
  24. David P, Chen NWG, Pedrosa-Harand A, Thareau V, Sévignac M, Cannon SB, Debouck D, Langin T, Geffroy V (2009) A nomadic subtelomeric disease resistance gene cluster in common bean. Plant Physiol 151:1048–1065PubMedPubMedCentralCrossRefGoogle Scholar
  25. DeBolt S (2010) Copy number variation shapes genome diversity in Arabidopsis over immediate family generational scales. Genome Biol Evol 2:441–453PubMedPubMedCentralCrossRefGoogle Scholar
  26. Diaz 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:e33234PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JDG (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915–1925PubMedPubMedCentralCrossRefGoogle Scholar
  28. Douchkov D, Lück S, Johrde A, Nowara D, Himmelbach A, Rajaraman J, Stein N, Sharma R, Kilian B, Schweizer P (2014) Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi. Genome Biol 15:518PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fadista J, Thomsen B, Holm LE, Bendixen C (2010) Copy number variation in the bovine genome. BMC Genom 11:284CrossRefGoogle Scholar
  30. Feuk L, Marshall CR, Wintle RF et al (2006) Structural variants: changing the landscape of chromosomes and design of disease studies. Hum Mol Genet 15:R57–R66PubMedCrossRefGoogle Scholar
  31. Flagel LE, Willis J, Vision TJ (2013) The standing pool of genomic structural variation in a natural population of Mimulus guttatus. Genome Biol Evol 6:53–64PubMedCentralCrossRefGoogle Scholar
  32. Freeman JL, Perry GH, Feuk L, Redon R, McCarroll SA, Altshuler DM, Aburatani H, Jones KW, Tyler-Smith C, Hurles ME, Carter NP, Scherer SW, Lee C (2006) Copy number variation: new insights in genome diversity. Genome Res 16:949–961PubMedCrossRefGoogle Scholar
  33. Gaines TA, Zhang W, Wang D, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS, Grey TL, Webster TM, Vencill WK, Sammons RD, Jiang J, Preston C, Leach JE, Westra P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA 107:1029–1034PubMedCrossRefGoogle Scholar
  34. Gaines TA, Shaner DL, Ward SM, Leach JE, Preston C, Westra P (2011) Mechanism of resistance of evolved glyphosate-resistant Amaranthus palmeri. J Agric Food Chem 59:5886–5889PubMedCrossRefGoogle Scholar
  35. Gazave E, Darré F, Morcillo-Suarez C, Petit-Marty N, Carreño A, Marigorta UM, Ryder OA, Blancher A, Rocchi M, Bosch E, Baker C, Marquès-Bonet T, Eichler EE, Navarro A (2011) Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. Genome Res 21:1626–1639PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gillet-Markowska A, Richard H, Fischer G, Lafontaine I (2014) Ulysses: accurate detection of low-frequency structural variations in large insert-size sequencing libraries. Bioinformatics 31:801–808PubMedCrossRefGoogle Scholar
  37. Girirajan S, Campbell CD, Eichler EE (2011) Human copy number variation and complex genetic disease. Annu Rev Genet 45:203–226PubMedCrossRefGoogle Scholar
  38. Golicz AA, Schliep M, Lee HT, Larkum AWD, Dolferus R, Batley J, Chan CKK, Sablok G, Ralph PJ, Edwards D (2015) Genome-wide survey of the seagrass Zostera muelleri suggests modification of the ethylene signalling network. J Exp Bot 6:1–10Google Scholar
  39. Golicz AA, Batley J, Edwards D (2016a) Towards plant pangenomics. Plant Biotechnol J 14:1099–1105PubMedCrossRefGoogle Scholar
  40. Golicz AA, Bayer PE, Barker GC, Edger PP, Kim HR, Martinez PA, Chan CKC, 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 7:13390PubMedPubMedCentralCrossRefGoogle Scholar
  41. Guo YL, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D et al (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 157:757–769PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65CrossRefGoogle Scholar
  43. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395PubMedCrossRefGoogle Scholar
  44. Hanikenne M, Kroymann J, Trampczynska A, Bernal M, Motte P, Clemens S, Krämer U (2013) Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet 9:e1003707PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hardigan MA, Crisovan E, Hamilton JP, Kim J, Laimbeer P, Leisner CP, Manrique-Carpintero NC, Newton L, Pham GM, Vaillancourt B, Xueming Y, Zeng Z, Douches DS, Jiang J, Veilleux RE, Buell CB (2016) Genome reduction uncovers a large dispensable genome and adaptive role for copy number variation in asexually propagated Solanum tuberosum. Plant Cell 28:388–405PubMedPubMedCentralCrossRefGoogle Scholar
  46. Horiguchi G, Gonzalez N, Beemster GT, Inzé D, Tsukaya H (2009) Impact of segmental chromosomal duplications on leaf size in the grandifolia-D mutants of Arabidopsis thaliana. Plant J 60:122–133PubMedCrossRefGoogle Scholar
  47. Hurgobin B, Edwards D (2017) SNP discovery using a pangenome: has the single reference approach become obsolete? Biology 6(1):21PubMedCentralCrossRefGoogle Scholar
  48. Iwakami S, Shimono Y, Manabe Y, Endo M, Shibaike H, Uchino A, Tominaga T (2017) Copy number variation in acetolactate synthase genes of thifensulfuron-methyl resistant Alopecurus aequalis (Short-awn Foxtail) accessions in Japan. Front Plant Sci 8:254PubMedPubMedCentralCrossRefGoogle Scholar
  49. Jamann TM, Poland JA, Kolkman JM, Smith LG, Nelson RJ (2014) Unraveling genomic complexity at a quantitative disease resistance locus in maize. Genetics 198:333–344PubMedPubMedCentralCrossRefGoogle Scholar
  50. Jiang Y, Wang Y, Brudno M (2012) PRISM: pair-read informed split- read mapping for base-pair level detection of insertion, deletion and structural variants. Bioinformatics 28:2576–2583PubMedCrossRefGoogle Scholar
  51. Katoh H, Inoue H, Iwanami T (2015) Changes in variable number of tandem repeats in ‘Candidatus Liberibacter asiaticus’ through insect transmission. PLoS One 10(9):e0138699PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kidd JM, Cooper GM, Donahue WF et al (2008) Mapping and sequencing of structural variation from eight human genomes. Nature 453:56–64PubMedPubMedCentralCrossRefGoogle Scholar
  53. Klambauer G, Schwarzbauer K, Mayr A, Clevert DA, Mitterecker A, Bodenhofer U et al (2012) cn.MOPS: mixture of Poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res 40:e69PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kolomietz E, Meyn MS, Pandita A et al (2002) The role of Alu repeat clusters as mediators of recurrent chromosomal aberrations in tumours. Genes Chromosomes Cancer 35:97–112PubMedCrossRefGoogle Scholar
  55. Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci 279:5048–5057PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lam HY, Mu XJ, Stütz AM, Tanzer A, Cayting PD, Snyder M, Kim PM, Korbel JO, Gerstein MB (2009) Nucleotide-resolution analysis of structural variants using BreakSeq and a breakpoint library. Nat Biotechnol 28:47–55PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lam HYK, Clark MJ, Chen R, Chen R, Natsoulis G, O’Huallachain M, Dewey FE, Habegger L, Ashley EA, Gerstein MB, Butte AJ, Ji HP, Snyder M (2012) Performance comparison of whole-genome sequencing platforms. Nat Biotechnol 30:78–82CrossRefGoogle Scholar
  58. Layer RM, Chiang C, Quinlan AR, Hall IM (2014) LUMPY: a probabilistic frame work for structural variant discovery. Genome Biol 15:R84PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lee OG, Kumar I, Diers BW, Hudson ME (2015) Evolution and selection of Rhg1, a copy-number variant nematode-resistance locus. Mol Ecol 24:1774–1791PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 USA 95:370–375PubMedCrossRefGoogle Scholar
  61. Li W, Olivier M (2013) Current analysis platforms and methods for detecting copy number variation. Physiol Genom 45:1–16CrossRefGoogle Scholar
  62. 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 196:282–291PubMedCrossRefGoogle Scholar
  63. 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, Hong 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 32:1045–1054PubMedCrossRefGoogle Scholar
  64. Lin X, Zhang Y, Kuang H, Chen J (2013) Frequent loss of lineages and deficient duplications accounted for low copy number of disease resistance genes in Cucurbitaceae. BMC Genom 14:335CrossRefGoogle Scholar
  65. 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 rapa genomes: a turnip, a rapid cycling and a Chinese cabbage. BMC Genom 15:250CrossRefGoogle Scholar
  66. Liu GE, Hou Y, Zhu B, Cardone MF, Jiang L, Cellamare A, Mitra A, Alexander LJ, Coutinho LL, Dell’Aquila ME, Gasbarre LC, Lacalandra G, Li RW, Matukumalli LK, Nonneman D, Regitano LCA, Smith TPL, Song J, Sonstegard TS, Van Tassell CP, Ventura M, Eichler EE, McDaneld TG, Keele JW (2010) Analysis of copy number variations among diverse cattle breeds. Genome Res 20:693–703PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lu P, Han X, Qi J et al (2012) Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by re-sequencing Landsberg erecta and all four products of a single meiosis. Genome Res 22:508–518PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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. Plant Biol 14:253Google Scholar
  69. Marcinkowska-Swojak M, Uszczynska B, Figlerowicz M, Kozlowski P (2013) An MLPA-based strategy for discrete CNV genotyping: CNV-miRNAs as an example. Hum Mutat 34:763–773PubMedCrossRefGoogle Scholar
  70. Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D et al (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci 110:5241–5246PubMedCrossRefGoogle Scholar
  71. Marschall T, Hajirasouliha I, Schonhuth A (2013) MATE-CLEVER: mendelian-inheritance-aware discovery and genotyping of midsize and long indels. Bioinformatics 29:3143–3150PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mason AM, Zhang J, Tollenaere R, Vasquez Teuber P, Dalton-Morgan J, Hu L, Yan G, Edwards D, Redden R, Batley J (2015) High-throughput genotyping for species identification and diversity assessment in germplasm collections. Mol Ecol Resour 15:1091–1101PubMedCrossRefGoogle Scholar
  73. 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 159:1295–1308PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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:R58PubMedPubMedCentralCrossRefGoogle Scholar
  75. Muñoz-Amatriaín M, Lonardi S, Luo MC et al (2015) Sequencing of 15 622 gene-bearing BACs clarifies the gene-dense regions of the barley genome. Plant J 84:216–227PubMedPubMedCentralCrossRefGoogle Scholar
  76. Nguyen HT, Merriman TR, Black MA (2014) The CNVrd2 package: measurement of copy number at complex loci using high-throughput sequencing data. Front Genet 5:248PubMedPubMedCentralCrossRefGoogle Scholar
  77. Nicholas TJ, Baker C, Eichler EE, Akey JM (2011) A high-resolution integrated map of copy number polymorphisms within and between breeds of the modern domesticated dog. BMC Genom 12:414CrossRefGoogle Scholar
  78. Nijkamp JF, Van Den Broek MA, Geertman JM, Reinders MJ, Daran JM, De Ridder D (2012) De novo detection of copy number variation by co-assembly. Bioinformatics 28:3195–3202PubMedCrossRefGoogle Scholar
  79. Nishida H, Yoshida T, Kawakami K et al (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 Breed 31:27–37CrossRefGoogle Scholar
  80. O’Rawe J, Jiang T, Sun G, Wu Y, Wang W, Hu J, Bodily P, Tian L, Hakonarson H, Johnson WE, Wei Z, Wang Kai, Lyon GJ (2013) Low concordance of multiple variant-calling pipelines: practical implications for exome and genome sequencing. Genome Med 5:28PubMedPubMedCentralCrossRefGoogle Scholar
  81. Orozco LD, Cokus SJ, Ghazalpour A, Ingram-Drake L, Wang S, Van Nas A, Che N, Araujo JA, Pellegrini M, Lusis AJ (2009) Copy number variation influences gene expression and metabolic traits in mice. Hum Mol Genet 18:4118–4129PubMedPubMedCentralCrossRefGoogle Scholar
  82. Ortiz-Estevez M, De Las Rivas J, Fontanillo C, Rubio A (2011) Segmentation of genomic and transcriptomic microarrays data reveals major correlation between DNA copy number aberrations and gene-loci expression. Genomics 97:86–93PubMedCrossRefGoogle Scholar
  83. 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 33:2706–2719PubMedPubMedCentralCrossRefGoogle Scholar
  84. Pirooznia M, Goes FS, Zandi PP (2015) Whole-genome CNV analysis: advances in computational approaches. Front Genet 6:138PubMedPubMedCentralCrossRefGoogle Scholar
  85. Redon R, Ishikawa S, Fitch KR et al (2006) Global variation in copy number in the human genome. Nature 444:444–454PubMedPubMedCentralCrossRefGoogle Scholar
  86. Samelak-Czajka A, Marszalek-Zenczak M, Marcinkowska-Swojak M, Kozlowski P, Figlerowicz M, Zmienko A (2017) MLPA-based analysis of copy number variation in plant populations. Front Plant Sci 8:222PubMedPubMedCentralCrossRefGoogle Scholar
  87. Sammons RD, Gaines TA (2014) Glyphosate resistance: state of knowledge. Pest Manag Sci 70:1367–1377PubMedPubMedCentralCrossRefGoogle Scholar
  88. Saxena RK, Edwards D, Varshney RK (2014) Structural variations in plant genomes. Brief Funct Genom 13:296–307CrossRefGoogle Scholar
  89. Scherer SW, Lee C, Birney E, Altshuler DM, Eichler EE, Carter NP, Hurles ME, Feuk L (2007) Challenges and standards in integrating surveys of structural variation. Nat Genet 39:S7–S15PubMedPubMedCentralCrossRefGoogle Scholar
  90. Schiessl S, Huettel B, Kuehn D, Reinhardt R, Snowdon R (2017) Post-polyploidisation morphotype diversification associates with gene copy number variation. Nat/Sci Rep 7:41845Google Scholar
  91. Sebat J, Lakshmi B, Troge J, Alexander J, Young J, Lundin P, Maner S, Massa H, Walker M, Chi M et al (2004) Large-scalecopy number polymorphism in the human genome. Science 305:525–528PubMedCrossRefGoogle Scholar
  92. Sieber AN, 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 129:1087–1097PubMedCrossRefGoogle Scholar
  93. Šķipars V, Krivmane B, Ruņģis D (2011) Thaumatin-like protein gene copy number variation in Scots pine (Pinus sylvestris). Environ Exp Biol 9:75–81Google Scholar
  94. Slabaugh MB, Yu JK, Tang S, Heesacker A, Hu X, Lu G, Han F, Bidney D, Knapp SJ (2003) Haplotyping and mapping a large cluster of resistance gene candidates in sunflower using multilocus intron fragment length polymorphisms. Plant Biotechnol J 1:167–185PubMedCrossRefGoogle Scholar
  95. Springer NM, Ying K, Fu Y et al (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5:e1000734PubMedPubMedCentralCrossRefGoogle Scholar
  96. Stankiewicz P, Lupski JR (2010) Structural variation in the human genome and its role in disease. Annu Rev Med 61:437–455PubMedCrossRefGoogle Scholar
  97. Sutton T, Baumann U, Hayes J, Collins NC, Shi BJ, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M et al (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449PubMedCrossRefGoogle Scholar
  98. 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 20:1689–1699PubMedPubMedCentralCrossRefGoogle Scholar
  99. Teo SM, Pawitan Y, Ku CS, Chia KS, Salim A (2012) Statisticalchal lenges associated with detecting copy number variations with next-generation sequencing. Bioinformatics 28:2711–2718PubMedCrossRefGoogle Scholar
  100. Trappe K, Emde AK, Ehrlich HC, Reinert K (2014) Gustaf: detecting and correctly classifying SVs in the NGS twilight zone. Bioinformatics 30:3484–3490PubMedCrossRefGoogle Scholar
  101. Trębicki P, Nancarrow N, Cole E, Bosque-Pérez NA, Constable FE, Freeman AJ, Rodoni B, Yen AL, Luck JE, Fitzgerald GJ (2015) Virus disease in wheat predicted to increase with a changing climate. Glob Change Biol 21:3511–3519CrossRefGoogle Scholar
  102. Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV (2010) Population re-sequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–263PubMedCrossRefGoogle Scholar
  103. Vallejos CE, Astua-Monge G, Jones V, Plyler TR, Sakiyama NS, Mackenzie SA (2006) Genetic and molecular characterization of the I locus of Phaseolus vulgaris. Genetics 172:1229–1242PubMedPubMedCentralCrossRefGoogle Scholar
  104. Veltman JA, Brunner HG (2012) De novo mutations in human genetic disease. Nat Rev Genet 18(13):565–575CrossRefGoogle Scholar
  105. Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:e123PubMedPubMedCentralCrossRefGoogle Scholar
  106. Wang H, Nettleton D, Ying K (2014) Copy number variation detection using next generation sequencing read counts. BMC Bioinform 15:109CrossRefGoogle Scholar
  107. 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 47:944–949PubMedCrossRefGoogle Scholar
  108. Weaver S, Dube S, Mir A, Qin J, Sun G, Ramakrishnan R, Jones RC, Li-vak KJ (2010) Taking qPCR to a higher level: analysis of CNV reveals the power of high throughput qPCR to enhance quantitative resolution. Methods 50:271–276PubMedCrossRefGoogle Scholar
  109. Wei C, Chen J, Kuang H (2016) Dramatic number variation of R genes in Solanaceae species accounted for by a few R gene subfamilies. PLoS One 11:e0148708PubMedPubMedCentralCrossRefGoogle Scholar
  110. Würschum T, Boeven PHG, Langer SM, Longin CFH, Wl Leiser (2015) Multiply to conquer: copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat. BMC Genet 16:96PubMedPubMedCentralCrossRefGoogle Scholar
  111. Würschum T, Longin CFH, Hahn V, Tucker MR, Leiser WL (2017) Copy number variations of CBF genes at the Fr-A2 locus are essential components of winter hardiness in wheat. Plant J 89:764–773PubMedCrossRefGoogle Scholar
  112. Xi R, Lee S, Park PJ (2012) A survey of copy-number variation detection tools based on high-throughput sequencing data, chapter 7. Curr Protoc Hum Genet (Unit 7–19). doi: 10.1002/0471142905.hg0719s75
  113. Xiao H, Jiang N, Schaffner E, Stockinger EJ, Vander Knaap E (2008) Retro-transposon-mediated gene duplication under lies morphological variation of tomato fruit. Science 319:1527–1530PubMedCrossRefGoogle Scholar
  114. Xu X, Liu X, Ge S et al (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111CrossRefGoogle Scholar
  115. Yang S, Lia J, Zhanga X, Zhangb Q, Huanga J, Chena JQ, Hartlc DL, Tian D (2013) Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease. Proc Natl Acad Sci 110:18572–18577PubMedCrossRefGoogle Scholar
  116. 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 16:1–20CrossRefGoogle Scholar
  117. 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 Genom 12:372CrossRefGoogle Scholar
  118. Yu P, Wang CH, Xu Q, Feng Y, Yuan XP, Yu HY, Wang YP, Tang SX, Wei XH (2013) Genome-wide copy number variations in Oryza sativa L. BMC Genom 14:649CrossRefGoogle Scholar
  119. Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553PubMedPubMedCentralCrossRefGoogle Scholar
  120. Zhang F, Gu W, Hurles ME, Lupski JR (2009) Copy number variation in human health, disease, and evolution. Annu Rev Genom Hum Genet 10:451–481CrossRefGoogle Scholar
  121. Zhang R, Murat F, Pont C, Langin T, Salse J (2014) Paleo-evolutionary plasticity of plant disease resistance genes. BMC Genom 15:187CrossRefGoogle Scholar
  122. Zhao M, Wang Q, Wang Q, Jia P, Zhao Z (2013) Computational tools for copy number variation (CNV) detection using next-generation sequencing data: features and perspectives. BMC Bioinform 14(Suppl 11):S1CrossRefGoogle Scholar
  123. Zheng LY, Guo XS, He B, Sun LJ, Peng Y, Dong SS, Liu TF, Jiang S, Ramachandran S, Liu CM, Jing HC (2011) Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol 12:1–14CrossRefGoogle Scholar
  124. 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 Genom 18:261CrossRefGoogle Scholar
  125. Zhu M, Need AC, Han Y, Ge D, Maia JM, Zhu Q et al (2012) Using ERDS to infer copy number variants in high-coverage genomes. Am J Hum Genet 91:408–421PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zmienko A, Samelak-Czajka A, Kozlowski P, Szymanska M, Figlerowicz M (2016) Arabidopsis thaliana population analysis reveals high plasticity of the genomic region spanning MSH2 AT3G18530 and AT3G18535 genes and provides evidence for NAHR-driven recurrent CNV events occurring in this location. BMC Genom 17:893CrossRefGoogle Scholar
  127. Żmieńko A, Samelak A, Kozłowski P, Figlerowicz M (2014) Copy number polymorphism in plant genomes. Theor Appl Genet 127:1–18PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.School of Biological Sciences and Institute of AgricultureUniversity of Western AustraliaCrawleyAustralia

Personalised recommendations