Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor

Genome Research

Volumn 20, Issue 12, 2010, Pages 1689-1699

  Swanson Wagner, Ruth A ^a   Eichten, Steven R ^a   Kumari, Sunita ^b   Tiffin, Peter ^a   Stein, Joshua C ^b   Ware, Doreen ^b,c   Springer, Nathan M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Simons Center for Quantitative Biology   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; GENE CONTENT VARIATION; GENE DOSAGE; GENETIC VARIABILITY; GENOTYPE; MAIZE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

CHROMOSOME MAPPING; COMPARATIVE GENOMIC HYBRIDIZATION; GENE DOSAGE; GENES, PLANT; GENETIC VARIATION; GENOTYPE; RECOMBINATION, GENETIC; SPECIES SPECIFICITY; ZEA MAYS;

ZEA MAYS;

EID: 78549273825     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.109165.110     Document Type: Article

References (86)

1. Beckmann JS, Estivill X, Antonarakis SE. 2007. Copy number variants and genetic traits: Closer to the resolution of phenotypic to genotypic variability. Nat Rev Genet 8: 639-646.
2. Belo 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: 355-367.
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300.
4. Bennetzen J. 2005. Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15: 621-627.
5. Bennetzen JL. 2007. Patterns in grass genome evolution. Curr Opin Plant Biol 10: 176-181.
6. Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W. 2004. Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7: 732-736. (Pubitemid 39379517)
7. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, et al. 2010. The landscape of somatic copy-number alteration across human cancers. Nature 463: 899-905.
8. Birchler J, Auger D, Riddle N. 2003. In search of the molecular basis of heterosis. Plant Cell 15: 2236-2239.
9. Blanc G, Hokamp K, Wolfe KH. 2003. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13: 137-144. (Pubitemid 36575763)
10. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A. 2005. Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17: 343-360. (Pubitemid 41672960)
11. Bucan M, Abrahams BS, Wang K, Glessner JT, Herman EI, Sonnenblick LI, Alvarez Retuerto AI, Imielinski M, Hadley D, Bradfield JP, et al. 2009. Genome-wide analyses of exonic copy number variants in a family-based study point to novel autism susceptibility genes. PLoS Genet 5: e1000536. doi: 10.1371/journal.pgen.1000536.
12. Buckler E, Gaut B, McMullen M. 2006. Molecular and functional diversity of maize. Curr Opin Plant Biol 9: 172-176.
13. Chen WK, Swartz JD, Rush LJ, Alvarez CE. 2009. Mapping DNA structural variation in dogs. Genome Res 19: 500-509.
14. Chopra S, Athma P, Li XG, Peterson T. 1998. A maize Myb homolog is encoded by a multicopy gene complex. Mol Gen Genet 260: 372-380. (Pubitemid 28552174)
15. Conrad DF, Andrews TD, Carter NP, Hurles ME, Pritchard JK. 2006. A high-resolution survey of deletion polymorphism in the human genome. Nat Genet 38: 75-81. (Pubitemid 43011885)
16. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, et al. 2010. Origins and functional impact of copy number variation in the human genome. Nature 464: 704-712.
17. Cooper GM, Nickerson DA, Eichler EE. 2007. Mutational and selective effects on copy-number variants in the human genome. Nat Genet 39: S22-S29.
18. Emrich SJ, Barbazuk WB, Li L, Schnable PS. 2007. Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Res 17: 69-73. (Pubitemid 46041667)
19. Feuk L, Carson AR, Scherer SW. 2006. Structural variation in the human genome. Nat Rev Genet 7: 85-97.
20. Foster T, Yamaguchi J, Wong BC, Veit B, Hake S. 1999. Gnarley1 is a dominant mutation in the knox4 homeobox gene affecting cell shape and identity. Plant Cell 11: 1239-1252.
21. Freeling M. 2009. Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60: 433-453.
22. Fu H, Dooner HK. 2002. Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci 99: 9573-9578.
23. Fu Y, Wen TJ, Ronin YI, Chen HD, Guo L, Mester DI, Yang Y, Lee M, Korol AB, Ashlock DA, et al. 2006. Genetic dissection of intermated recombinant inbred lines using a new genetic map of maize. Genetics 174: 1671-1683.
24. Gaut BS, Doebley JF. 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci 94: 6809-6814.
25. Goettel W, Messing J. 2009. Change of gene structure and function by non-homologous end-joining, homologous recombination, and transposition of DNA. PLoS Genet 5: e1000516. doi: 10.1371/journal.pgen.1000516.
26. Graubert TA, Cahan P, Edwin D, Selzer RR, Richmond TA, Eis PS, Shannon WD, Li X, McLeod HL, Cheverud JM, et al. 2007. A high-resolution map of segmental DNA copy number variation in the mouse genome. PLoS Genet 3: e3. doi: 10.1371/journal.pgen.0030003.
27. Guryev V, Saar K, Adamovic T, Verheul M, van Heesch SA, Cook S, Pravenec M, Aitman T, Jacob H, Shull JD, et al. 2008. Distribution and functional impact of DNA copy number variation in the rat. Nat Genet 40: 538-545.
28. Hansey CN, Johnson JM, Sekhon RS, Kaeppler SM, de Leon N. 2010. Genetic diversity of a maize association population with restricted phenology. Crop Sci (in press). doi: 10.2135/cropsci2010.03.0178.
29. Haun WJ, Springer NM. 2008. Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J 56: 903-912.
30. Hurles ME, Dermitzakis ET, Tyler-Smith C. 2008. The functional impact of structural variation in humans. Trends Genet 24: 238-245.
31. Innan H, Kondrashov F. 2010. The evolution of gene duplications: Classifying and distinguishing between models. Nat Rev Genet 11: 97-108.
32. Kato A, Lamb JC, Birchler JA. 2004. Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci 101: 13554-13559.
33. Kidd JM, Cooper GM, Donahue WF, Hayden HS, Sampas N, Graves T, Hansen N, Teague B, Alkan C, Antonacci F, et al. 2008. Mapping and sequencing of structural variation from eight human genomes. Nature 453: 56-64.
34. Lai J, Li Y, Messing J, Dooner HK. 2005. Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci 102: 9068-9073.
35. Lee AS, Gutierrez-Arcelus M, Perry GH, Vallender EJ, Johnson WE, Miller GM, Korbel JO, Lee C. 2008. Analysis of copy number variation in the rhesus macaque genome identifies candidate loci for evolutionary and human disease studies. Hum Mol Genet 17: 1127-1136.
36. Liu S, Yeh CT, Ji T, Ying K, Wu H, Tang HM, Fu Y, Nettleton D, Schnable PS. 2009. Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet 5: e1000733. doi: 10.137l/journal.pgen.1000733.
37. Lough AN, Roark LM, Kato A, Ream TS, Lamb JC, Birchler JA, Newton KJ. 2008. Mitochondrial DNA transfer to the nucleus generates extensive insertion site variation in maize. Genetics 178: 47-55.
38. Maere S, Heymans K, Kuiper M. 2005. BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449. (Pubitemid 41222459)
39. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. 2009. Finding the missing heritability of complex diseases. Nature 461: 747-753.
40. Maydan JS, Lorch A, Edgley ML, Flibotte S, Moerman DG. 2010. Copy number variation in the genomes of twelve natural isolates of Caenorhabditis elegans. BMC Genomics 11: 62. doi: 10.1186/1471-2164-11-62.
41. McCarroll SA, Altshuler DM. 2007. Copy-number variation and association studies of human disease. Nat Genet 39: S37-S42. (Pubitemid 47014474)
42. McClintock B, Yamakake TAK, Blumenschein A. 1981. Chromosome constitution of races of maize. Its significance in the interpretation of relationships between races and varieties in the Americas. Colegio de Postgraduados, Chapingo, Mexico.
43. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, et al. 2009. Genetic properties of the maize nested association mapping population. Science 325: 737-740.
44. Merikangas AK, Corvin AP, Gallagher L. 2009. Copy-number variants in neurodevelopmental disorders: Promises and challenges. Trends Genet 25: 536-544.
45. Messing J, Dooner H. 2006. Organization and variability of the maize genome. Curr Opin Plant Biol 9: 157-163.
46. Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF, et al. 2004. Sequence composition and genome organization of maize. Proc Natl Acad Sci 101: 14349-14354.
47. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A. 2005. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37: 997-1002.
48. Morgante M, De Paoli E, Radovic S. 2007. Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10: 149-155.
49. Paterson AH, Chapman BA, Kissinger JC, Bowers JE, Feltus FA, Estill JC. 2006. Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet 22: 597-602.
50. Penning BW, Hunter CT III, Tayengwa R, Eveland AL, Dugard CK, Olek AT, Vermerris W, Koch KE, McCarty DR, Davis MF, et al. 2009. Genetic resources for maize cell wall biology. Plant Physiol 151: 1703-1728.
51. Perry GH, Yang F, Marques-Bonet T, Murphy C, Fitzgerald T, Lee AS, Hyland C, Stone AC, Hurles ME, Tyler-Smith C, et al. 2008. Copy number variation and evolution in humans and chimpanzees. Genome Res 18: 1698-1710.
52. Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R. 2009. Starch grain and phytolith evidence for early ninth millennium B.P. maize from the Central Balsas River Valley, Mexico. Proc Natl Acad Sci 106: 5019-5024.
53. Pysh LD, Schmidt RJ. 1996. Characterization of the maize OHP1 gene: Evidence of gene copy variability among inbreds. Gene 177: 203-208.
54. Ranere AJ, Piperno DR, Holst I, Dickau R, Iriarte J. 2009. The cultural and chronological context of early Holocene maize and squash domestication in the Central Balsas River Valley, Mexico. Proc Natl Acad Sci 106: 5014-5018.
55. Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, et al. 2006. Global variation in copy number in the human genome. Nature 444: 444-454. (Pubitemid 44809057)
56. Rizzon C, Ponger L, Gaut BS. 2006. Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol 2: e115. doi: 10.1371/journal.pcbi.0020115.
57. Robbins TP, Walker EL, Kermicle JL, Alleman M, Dellaporta SL. 1991. Meiotic instability of the R-r complex arising from displaced intragenic exchange and intrachromosomal rearrangement. Genetics 129: 271-283.
58. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW. 1984. Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci 81: 8014-8018.
59. Santuari L, Pradervand S, Amiguet-Vercher AM, Thomas J, Dorcey E, Harshman K, Xenarios I, Juenger TE, Hardtke CS. 2010. Substantial deletion overlap among divergent Arabidopsis genomes revealed by intersection of short reads and tiling arrays. Genome Biol 11: R4. doi: 10.1186/gb-2010-11-1-r4.
60. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, et al. 2009. The B73 maize genome: Complexity, diversity, and dynamics. Science 326: 1112-1115.
61. Sebat J. 2007. Major changes in our DNA lead to major changes in our thinking. Nat Genet 39: S3-S5.
62. Sebat J, Lakshmi B, Troge J, Alexander J, Young J, Lundin P, Maner S, Massa H, Walker M, Chi M, et al. 2004. Large-scale copy number polymorphism in the human genome. Science 305: 525-528.
63. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
64. Sharp AJ, Locke DP, McGrath SD, Cheng Z, Bailey JA, Vallente RU, Pertz LM, Clark RA, Schwartz S, Segraves R, et al. 2005. Segmental duplications and copy-number variation in the human genome. Am J Hum Genet 77: 78-88. (Pubitemid 40848038)
65. Sharp AJ, Hansen S, Selzer RR, Cheng Z, Regan R, Hurst JA, Stewart H, Price SM, Blair E, Hennekam RC, et al. 2006. Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat Genet 38: 1038-1042.
66. Shomura A, Izawa T, Ebana K, Ebitani T, Kanegae H, Konishi S, Yano M. 2008. Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet 40: 1023-1028.
67. 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.
68. Springer NM, Ying K, Fu Y, Ji T, Yeh CT, Jia Y, Wu W, Richmond T, Kitzman J, Rosenbaum H, et al. 2009. Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5: e1000734. doi: 10.1371/journal.pgen.1000734.
69. Stankiewicz P, Lupski JR. 2010. Structural variation in the human genome and its role in disease. Annu Rev Med 61: 437-455.
70. Stupar RM, Springer NM. 2006. Cis-transcriptional variation inmaize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173: 2199-2210.
71. Stupar RM, Gardiner JM, Oldre AG, Haun WJ, Chandler VL, Springer NM. 2008. Gene expression analyses inmaize inbreds and hybrids with varying levels of heterosis. BMC Plant Biol 8: 33. doi: 10.1186/1471-2229-8-33.
72. Swigonova Z, Bennetzen JL, Messing J. 2005. Structure and evolution of the r/b chromosomal regions in rice, maize and sorghum. Genetics 169: 891-906.
73. Tuzun E, Sharp AJ, Bailey JA, Kaul R, Morrison VA, Pertz LM, Haugen E, Hayden H, Albertson D, Pinkel D, et al. 2005. Fine-scale structural variation of the human genome. Nat Genet 37: 727-732.
74. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. 2009. EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335.
75. Wang Q, Dooner HK. 2006. Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci 103: 17644-17649. (Pubitemid 44852214)
76. Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S, et al. 2007. Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3: e123. doi: 10.1371/journal.pgen.0030123.
77. Wellcome Trust Case Control Consortium. 2010. Genome-wide association study of CNVs in 16,000 cases of eight common diseases and 3,000 shared controls. Nature 464: 713-720.
78. Wong KK, deLeeuw RJ, Dosanjh NS, Kimm LR, Cheng Z, Horsman DE, MacAulay C, Ng RT, Brown CJ, Eichler EE, et al. 2007. A comprehensive analysis of common copy-number variations in the human genome.Am J Hum Genet 80: 91-104.
79. 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 homologs. PLoS Biol 8: e1000409. doi: 10.1371/journal.pbio.1000409.
80. Yandeau-Nelson MD, Xia Y, Li J, Neuffer MG, Schnable PS. 2006. Unequal sister chromatid and homolog recombination at a tandem duplication of the a1 locus in maize. Genetics 173: 2211-2226.
81. Yang L, Bennetzen JL. 2009. Distribution, diversity, evolution and survival of Helitrons in the maize genome. Proc Natl Acad Sci 106: 19922-19927.
82. Yao H, Zhou Q, Li J, Smith H, Yandeau M, Nikolau BJ, Schnable PS. 2002. Molecular characterization of meiotic recombination across the 140- kb multigenic a1-sh2 interval of maize. Proc Natl Acad Sci 99: 6157-6162.
83. Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, et al. 2005. The Genomes of Oryza sativa: A history of duplications. PLoS Biol 3: e38. doi: 10.1371/journal.pbio.0030038.
84. Zhang F, Peterson T. 2005. Comparisons of maize pericarp color1 alleles reveal paralogous gene recombination and an organ-specific enhancer region. Plant Cell 17: 903-914.
85. Zhang F, Gu W, Hurles ME, Lupski JR. 2009. Copy number variation in human health, disease, and evolution. Annu Rev Genomics Hum Genet 10: 451-481.
86. Zhou Y, Zhu J, Li Z, Yi C, Liu J, Zhang H, Tang S, Gu M, Liang G. 2009. Deletion in a quantitative trait gene qPE9-1 associated with panicle erectness improves plant architecture during rice domestication. Genetics 183: 315-324.