Skip to main content
SpringerLink
Log in

Allelic genome structural variations in maize detected by array comparative genome hybridization

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

DNA polymorphisms such as insertion/deletions and duplications affecting genome segments larger than 1 kb are known as copy-number variations (CNVs) or structural variations (SVs). They have been recently studied in animals and humans by using array-comparative genome hybridization (aCGH), and have been associated with several human diseases. Their presence and phenotypic effects in plants have not been investigated on a genomic scale, although individual structural variations affecting traits have been described. We used aCGH to investigate the presence of CNVs in maize by comparing the genome of 13 maize inbred lines to B73. Analysis of hybridization signal ratios of 60,472 60-mer oligonucleotide probes between inbreds in relation to their location in the reference genome (B73) allowed us to identify clusters of probes that deviated from the ratio expected for equal copy-numbers. We found CNVs distributed along the maize genome in all chromosome arms. They occur with appreciable frequency in different germplasm subgroups, suggesting ancient origin. Validation of several CNV regions showed both insertion/deletions and copy-number differences. The nature of CNVs detected suggests CNVs might have a considerable impact on plant phenotypes, including disease response and heterosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aitman TJ, Dong R, Vyse TJ, Norsworthy PJ, Johnson MD, Smith J, Mangion J, Roberton-Lowe C, Marshall AJ, Petretto E, Hodges MD, Bhangal G, Patel SG, Sheehan-Rooney K, Duda M, Cook PR, Evans DJ, Domin J, Flint J, Boyle JJ, Pusey CD, Cook HT (2006) Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439:851–855

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Auer H, Newsom DL, Nowak NJ, McHugh KM, Singh S, Yu C, Yang Y, Wenger GD, Gastier-Foster JM, Kornacker K (2007) Gene-resolution analysis of DNA copy number variation using oligonucleotide expression microarrays. BMC Genomics 8:111

    Article  PubMed  Google Scholar 

  • Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, Linhart D, Vivanco I, Lee JC, Huang JH, Alexander S, Du J, Kau T, Thomas RK, Shah K, Soto H, Perner S, Prensner J, Debiasi RM, Demichelis F, Hatton C, Rubin MA, Garraway LA, Nelson SF, Liau L, Mischel PS, Cloughesy TF, Meyerson M, Golub TA, Lander ES, Mellinghoff IK, Sellers WR (2007) Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci USA 104:20007–20012

    Article  CAS  PubMed  Google Scholar 

  • Borevitz JO, Liang D, Plouffe D, Chang H, Zhu T, Weigel D, Berry CC, Winzeler E, Chory J (2003) Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res 13:513–523

    Article  CAS  PubMed  Google Scholar 

  • Bruce M, Hess A, Bai J, Mauleon R, Diaz MG, Sugiyama N, Bordeos A, Wang GL, Leung H, Leach J (2009) Detection of genomic deletions in rice using oligonucleotide microarrays. BMC Genomics 10:129

    Article  PubMed  Google Scholar 

  • Bruder CEG, Piotrowski A, Gijsbers AACJ, Andersson R, Erickson S, de Stahl TD, Menzel U, Sandgren J, von Tell D, Poplawski A, Crowley M, Crasto C, Partridge EC, Tiwari H, Allison DB, Komorowski J, van Ommen GB, Boomsma DI, Pedersen NL, den Dunnen JT, Wirdefeldt K, Dumanski JP (2008) Phenotypically concordant and discordant monozygotic twins display different DNA copy-number-variation profiles. Am J Hum Genet 82:763–771

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Campbell PJ, Stephens PJ, Pleasance ED, O’Meara S, Li H, Santarius T, Stebbings LA, Leroy C, Edkins S, Hardy C, Teague JW, Menzies A, Goodhead I, Turner DJ, Clee CM, Quail MA, Cox A, Brown C, Durbin R, Hurles ME, Edwards PAW, Bignell GR, Stratton MR, Futreal PA (2008) Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 40:722–729

    Article  CAS  PubMed  Google Scholar 

  • 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 18:1143–1149

    Article  CAS  PubMed  Google Scholar 

  • 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 40:800–804

    Article  CAS  PubMed  Google Scholar 

  • Dooner HK, Martínez-Férez IM (1997) Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. Plant Cell 9:1633–1646

    Article  CAS  PubMed  Google Scholar 

  • Emerson JJ, Cardoso-Moreira M, Borevitz JO, Long M (2008) Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320:1629–1631

    Article  CAS  PubMed  Google Scholar 

  • Fanciulli M, Norsworthy PJ, Petretto E, Dong R, Harper L, Kamesh L, Heward JM, Gough SCL, de Smith A, Blakemore AIF, Froguel P, Owen CJ, Pearce SHS, Teixeira L, Guillevin L, Graham DSC, Pusey CD, Cook HT, Vyse TJ, Aitman TJ (2007) FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat Genet 39:721–723

    Article  CAS  PubMed  Google Scholar 

  • Fengler K, Allen SM, Li B, Rafalski A (2007) Distribution of genes, recombination, and repetitive elements in the maize genome. Crop Sci 47:S83–S95

    Google Scholar 

  • Feuk L, Carson AR, Scherer SW (2006) Structural variation in the human genome. Nat Rev Genet 7:85–97

    Article  CAS  PubMed  Google Scholar 

  • Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99:9573–9578

    CAS  PubMed  Google Scholar 

  • Fu H, Zheng Z, Dooner HK (2002) Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc Natl Acad Sci USA 99:1082–1087

    CAS  PubMed  Google Scholar 

  • Fu Y, Wen T, Ronin YI, Chen HD, Guo L, Mester DI, Yang Y, Lee M, Korol AB, Ashlock DA, Schnable PS (2006) Genetic dissection of intermated recombinant inbred lines using a new genetic map of maize. Genetics 174:1671–1683

    Article  CAS  PubMed  Google Scholar 

  • Garcia AAF, Wang S, Melchinger AE, Zeng Z (2008) QTL mapping and the genetic basis of heterosis in maize and rice. Genetics 180:1707–1724

    Article  PubMed  Google Scholar 

  • Geschwind DH, Gregg J, Boone K, Karrim J, Pawlikowska-Haddal A, Rao E, Ellison J, Ciccodicola A, D’Urso M, Woods R, Rappold GA, Swerdloff R, Nelson SF (1998) Klinefelter’s syndrome as a model of anomalous cerebral laterality: testing gene dosage in the X chromosome pseudoautosomal region using a DNA microarray. Dev Genet 23:215–229

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, Catano G, Nibbs RJ, Freedman BI, Quinones MP, Bamshad MJ, Murthy KK, Rovin BH, Bradley W, Clark RA, Anderson SA, O’connell RJ, Agan BK, Ahuja SS, Bologna R, Sen L, Dolan MJ, Ahuja SK (2005) The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307:1434–1440

    Article  CAS  PubMed  Google Scholar 

  • Grant M, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes R, Dangl J (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846

    Article  CAS  PubMed  Google Scholar 

  • Grant M, McDowell J, Sharpe A, de Torres Zabala M, Lydiate D, Dangl J (1998) Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci USA 95:15843–15848

    Article  CAS  PubMed  Google Scholar 

  • Gresham D, Dunham MJ, Botstein D (2008) Comparing whole genomes using DNA microarrays. Nat Rev Genet 9:291–302

    Article  CAS  PubMed  Google Scholar 

  • Guryev V, Saar K, Adamovic T, Verheul M, van Heesch SAAC, Cook S, Pravenec M, Aitman T, Jacob H, Shull JD, Hubner N, Cuppen E (2008) Distribution and functional impact of DNA copy number variation in the rat. Nat Genet 40:538–545

    Article  CAS  PubMed  Google Scholar 

  • Hittinger CT, Carroll SB (2007) Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449:677–681

    Article  CAS  PubMed  Google Scholar 

  • Huang JT, Dooner HK (2008) Macrotransposition and other complex chromosomal restructuring in maize by closely linked transposons in direct orientation. Plant Cell 20:2019–2032

    Article  CAS  PubMed  Google Scholar 

  • Hughes TR, Mao M, Jones AR, Burchard J, Marton MJ, Shannon KW, Lefkowitz SM, Ziman M, Schelter JM, Meyer MR, Kobayashi S, Davis C, Dai H, He YD, Stephaniants SB, Cavet G, Walker WL, West A, Coffey E, Shoemaker DD, Stoughton R, Blanchard AP, Friend SH, Linsley PS (2001) Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol 19:342–347

    Article  CAS  PubMed  Google Scholar 

  • Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, Qi Y, Scherer SW, Lee C (2004) Detection of large-scale variation in the human genome. Nat Genet 36:949–951

    Article  CAS  PubMed  Google Scholar 

  • Infante JJ, Dombek KM, Rebordinos L, Cantoral JM, Young ET (2003) Genome-wide amplifications caused by chromosomal rearrangements play a major role in the adaptive evolution of natural yeast. Genetics 165:1745–1759

    CAS  PubMed  Google Scholar 

  • Kallioniemi A (2008) CGH microarrays and cancer. Curr Opin Biotechnol 19:36–40

    Article  CAS  PubMed  Google Scholar 

  • 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 258:818–821

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Qiu J, Joshi T, Valliyodan B, Xu D, Nguyen HT (2007) Single feature polymorphism discovery in rice. PLoS One 2:e284

    Article  PubMed  Google Scholar 

  • Lakshmi B, Hall IM, Egan C, Alexander J, Leotta A, Healy J, Zender L, Spector MS, Xue W, Lowe SW, Wigler M, Lucito R (2006) Mouse genomic representational oligonucleotide microarray analysis: detection of copy number variations in normal and tumor specimens. Proc Natl Acad Sci USA 103:11234–11239

    Article  CAS  PubMed  Google Scholar 

  • McCarroll SA, Kuruvilla FG, Korn JM, Cawley S, Nemesh J, Wysoker A, Shapero MH, de Bakker PIW, Maller JB, Kirby A, Elliott AL, Parkin M, Hubbell E, Webster T, Mei R, Veitch J, Collins PJ, Handsaker R, Lincoln S, Nizzari M, Blume J, Jones KW, Rava R, Daly MJ, Gabriel SB, Altshuler D (2008) Integrated detection and population-genetic analysis of SNPs and copy number variation. Nat Genet 40:1166–1174

    Article  CAS  PubMed  Google Scholar 

  • Olshen AB, Venkatraman ES, Lucito R, Wigler M (2004) Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 5:557–572

    Article  PubMed  Google Scholar 

  • Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, Carter NP, Lee C, Stone AC (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256–1260

    Article  CAS  PubMed  Google Scholar 

  • Perry GH, Yang F, Marques-Bonet T, Murphy C, Fitzgerald T, Lee AS, Hyland C, Stone AC, Hurles ME, Tyler-Smith C, Eichler EE, Carter NP, Lee C, Redon R (2008) Copy number variation and evolution in humans and chimpanzees. Genome Res 18:1689–1710

    Article  Google Scholar 

  • Pinkel D, Segraves R, Sudar D, Clark S, Poole I, Kowbel D, Collins C, Kuo WL, Chen C, Zhai Y, Dairkee SH, Ljung BM, Gray JW, Albertson DG (1998) High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 20:207–211

    Article  CAS  PubMed  Google Scholar 

  • Pollack JR, Perou CM, Alizadeh AA, Eisen MB, Pergamenschikov A, Williams CF, Jeffrey SS, Botstein D, Brown PO (1999) Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nat Genet 23:41–46

    Article  CAS  PubMed  Google Scholar 

  • Pollack JR, Sorlie T, Perou CM, Rees CA, Jeffrey SS, Lonning PE, Tibshirani R, Botstein D, Borresen-Dale A, Brown PO (2002) Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci USA 99:12963–12968

    Article  CAS  PubMed  Google Scholar 

  • Price TS, Regan R, Mott R, Hedman A, Honey B, Daniels RJ, Smith L, Greenfield A, Tiganescu A, Buckle V, Ventress N, Ayyub H, Salhan A, Pedraza-Diaz S, Broxholme J, Ragoussis J, Higgs DR, Flint J, Knight SJL (2005) SW-ARRAY: a dynamic programming solution for the identification of copy-number changes in genomic DNA using array comparative genome hybridization data. Nucleic Acids Res 33:3455–3464

    Article  CAS  PubMed  Google Scholar 

  • Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, Gonzalez JR, Gratacos M, Huang J, Kalaitzopoulos D, Komura D, MacDonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, Zhang J, Zerjal T, Zhang J, Armengol L, Conrad DF, Estivill X, Tyler-Smith C, Carter NP, Aburatani H, Lee C, Jones KW, Scherer SW, Hurles ME (2006) Global variation in copy number in the human genome. Nature 444:444–454

    Article  CAS  PubMed  Google Scholar 

  • Ríos G, Naranjo M, Iglesias D, Ruiz-Rivero O, Geraud M, Usach A, Talon M (2008) Characterization of hemizygous deletions in citrus using array-comparative genomic hybridization and microsynteny comparisons with the poplar genome. BMC Genomics 9:381

    Article  PubMed  Google Scholar 

  • Salathia N, Hana NL, Sangster TA, Morneau K, Landry CR, Schellenberg K, Behere AS et al (2007) Indel arrays: an affordable alternative for genotyping. Plant J 51:727–737

    Article  CAS  PubMed  Google Scholar 

  • Sebat J, Lakshmi B, Troge J, Alexander J, Young J, Lundin P, Maner S, Massa H, Walker M, Chi M, Navin N, Lucito R, Healy J, Hicks J, Ye K, Reiner A, Gilliam TC, Trask B, Patterson N, Zetterberg A, Wigler M (2004) Large-scale copy number polymorphism in the human genome. Science 305:525–528

    Article  CAS  PubMed  Google Scholar 

  • She X, Cheng Z, Zöllner S, Church DM, Eichler EE (2008) Mouse segmental duplication and copy number variation. Nat Genet 40:909–914

    Article  CAS  PubMed  Google Scholar 

  • Shlien A, Tabori U, Marshall CR, Pienkowska M, Feuk L, Novokmet A, Nanda S, Druker H, Scherer SW, Malkin D (2008) Excessive genomic DNA copy number variation in the Li-Fraumeni cancer predisposition syndrome. Proc Natl Acad Sci USA 105:11264–11269

    Article  CAS  PubMed  Google Scholar 

  • Skvortsov D, Abdueva D, Stitzer ME, Finkel SE, Tavaré S (2007) Using expression arrays for copy number detection: an example from E. coli. BMC Bioinformatics 8:203

    Article  PubMed  Google Scholar 

  • Solinas-Toldo S, Lampel S, Stilgenbauer S, Nickolenko J, Benner A, Döhner H, Cremer T, Lichter P (1997) Matrix-based comparative genomic hybridization: biochips to screen for genomic imbalances. Genes Chromosomes Cancer 20:399–407

    Article  CAS  PubMed  Google Scholar 

  • Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17:264–275

    Article  CAS  PubMed  Google Scholar 

  • Stranger BE, Forrest MS, Dunning M, Ingle CE, Beazley C, Thorne N, Redon R, Bird CP, de Grassi A, Lee C, Tyler-Smith C, Carter N, Scherer SW, Tavare S, Deloukas P, Hurles ME, Dermitzakis ET (2007) Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 315:848–853

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. http://www.R-project.org. Accessed 24 Mar 2009

  • Tian D, Wang Q, Zhang P, Araki H, Yang S, Kreitman M, Nagylaki T, Hudson R, Bergelson J, Chen J (2008) Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature 455:105–108

    Article  CAS  PubMed  Google Scholar 

  • Xu B, Roos JL, Levy S, van Rensburg EJ, Gogos JA, Karayiorgou M (2008) Strong association of de novo copy number mutations with sporadic schizophrenia. Nat Genet 40:880–885

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Li C, Paez JG, Chin K, Jänne PA, Chen T, Girard L, Minna J, Christiani D, Leo C, Gray JW, Sellers WR, Meyerson M (2004) An integrated view of copy number and allelic alterations in the cancer genome using single nucleotide polymorphism arrays. Cancer Res 64:3060–3071

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are thankful to Scott Tingey for frequent challenging discussions and to DuPont Crop Genetics for providing financial support.

Author information

Authors and Affiliations

  1. DuPont Crop Genetics, Route 141, Henry Clay Road, Wilmington, DE, 19803, USA

    André Beló, Kevin A. Fengler, Bailin Li & Antoni Rafalski

  2. Department of Plant and Soil Sciences, University of Delaware, 152 Townsend Hall, Newark, DE, 19716, USA

    André Beló & Antoni Rafalski

  3. Pioneer Hi-Bred International, 7300 NW 62nd Avenue, Johnston, IA, 50131, USA

    Mary K. Beatty & David Hondred

Authors
  1. André Beló
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mary K. Beatty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Hondred
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kevin A. Fengler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bailin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Antoni Rafalski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antoni Rafalski.

Additional information

Communicated by P. Heslop-Harrison.

Contribution to the special issue “Heterosis in Plants”.

Electronic supplementary material

Below is the link to the electronic supplementary material.

List of PCR primers used for CNV validation. The primers are listed in the 5′ to 3′ direction. (PDF 66 kb)

122_2009_1128_MOESM2_ESM.pdf

Result of aCGH between Mo17 and B73. Probes highlighted in green and red are those detecting a CNV region with more copies or presence in Mo17 and B73, respectively. Solid and dashed horizontal red lines correspond to one and two standard-deviations, respectively, calculated for all probes in the experiment. The blue curve is a loess function (R Development Core Team 2009) based on the aCGH ratio. Coordinates along the chromosomes are given as bands in a maize physical map (Fengler et al. 2007). (PDF 2,581 kb)

122_2009_1128_MOESM3_ESM.pdf

Result of aCGH experiment between two independent preparations of the inbred line PHP38. Solid and dashed horizontal red lines correspond to one and two standard-deviations, respectively, calculated for all probes in the experiment. The blue curve is a loess function (R Development Core Team 2009) based on the aCGH ratio. Coordinates along the chromosomes are given as bands in a maize physical map (Fengler et al. 2007). (PDF 2,497 kb)

122_2009_1128_MOESM4_ESM.png

PCR of a CNV region on chromosome five at 530 cM. A. aCGH results. B. Detailed view of CNV regions showing B73 BACs, microarray probes (number of matches to B73 genome in parentheses), and PCR results. Left lane: PCR from B73; right lane: PCR from Mo17. C. PCR of probe regions in other maize inbreds. (PNG 308 kb)

122_2009_1128_MOESM5_ESM.png

PCR of two CNV regions on chromosomes eight (206 cM) and nine (300.2 cM). A. aCGH results. B. Detailed view of CNV regions showing B73 BACs, microarray probes (number of matches to B73 genome in parentheses) and PCR results. Left lane: PCR from B73; right lane: PCR from Mo17. C. PCR of probe regions in other maize inbreds. (PNG 193 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Beló, A., Beatty, M.K., Hondred, D. et al. Allelic genome structural variations in maize detected by array comparative genome hybridization. Theor Appl Genet 120, 355–367 (2010). https://doi.org/10.1007/s00122-009-1128-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1128-9

Keywords

Search

Navigation