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Chromosome Research

, Volume 25, Issue 3–4, pp 299–311 | Cite as

Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3

  • Hainan Zhao
  • Zixian Zeng
  • Dal-Hoe Koo
  • Bikram S. Gill
  • James A. Birchler
  • Jiming Jiang
Original Article

Abstract

Centromeres can arise de novo from non-centromeric regions, which are often called “neocentromeres.” Neocentromere formation provides the best evidence for the concept that centromere function is not determined by the underlying DNA sequences, but controlled by poorly understood epigenetic mechanisms. Numerous neocentromeres have been reported in several plant and animal species. However, it has been elusive how and why a specific chromosomal region is chosen to be a new centromere during the neocentromere activation events. We report recurrent establishment of neocentromeres in a pericentromeric region of chromosome 3 in maize (Zea mays). This latent region is located in the short arm and is only 2 Mb away from the centromere (Cen3) of chromosome 3. At least three independent neocentromere activation events, which were likely induced by different mechanisms, occurred within this latent region. We mapped the binding domains of CENH3, the centromere-specific H3 histone variant, of the three neocentromeres and analyzed the genomic and epigenomic features associated with Cen3, the de novo centromeres and an inactivated centromere derived from an ancestral chromosome. Our results indicate that lack of genes and transcription and a relatively high level of DNA methylation in this pericentromeric region may provide a favorable chromatin environment for neocentromere activation.

Keywords

Centromere CENH3 neocentromere centromeric genes centromeric chromatin 

Abbreviations

ChIP

Chromatin immunoprecipitation

DAPI

4′,6-diamidino-2-phenylindole

FISH

Flourescence in situ hybridization

OMA

Oat-maize chromosome addition

SNP

Single nucleotide polymorphism

Notes

Acknowledgements

We thank Dr. Patrick Schnable for providing the seeds of maize line ax-3 and Drs. Kelly Dawe and Jonathan Gent for valuable comments on the manuscript. This work was supported by the National Science Foundation (NSF) grant 1338897 to B.S.G. and NSF grant IOS-1444514 to J.A.B. and J.J.

Author contributions

H.Z and J.J. designed the research, Z.Z. and D.H.K. performed experiments, H.Z., J.A.B., and J.J. analyzed data, and H.Z., B.S.G., J.A.B., and J.J. wrote the article.

Supplementary material

10577_2017_9564_MOESM1_ESM.pdf (226 kb)
Figure S1 (PDF 225 kb)
10577_2017_9564_MOESM2_ESM.pdf (260 kb)
Figure S2 (PDF 259 kb)
10577_2017_9564_MOESM3_ESM.pdf (124 kb)
Figure S3 (PDF 123 kb)
10577_2017_9564_MOESM4_ESM.pdf (49 kb)
Table S1 (PDF 48 kb)

References

  1. Ananiev EV, Phillips RL, Rines HW (1998) Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci U S A 95:13073–13078CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anderson LK, Doyle GG, Brigham B, Carter J, Hooker KD, Lai A, Rice M, Stack SM (2003) High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics 165:849–865PubMedPubMedCentralGoogle Scholar
  3. Baldini A, Ried T, Shridhar V, Ogura K, Daiuto L, Rocchi M, Ward DC (1993) An alphoid DNA sequence conserved in all human and great ape chromosomes—evidence for ancient centromeric sequences at human chromosomal regions 2q21 and 9q13. Hum Genet 90:577–583CrossRefPubMedGoogle Scholar
  4. Capozzi O, Purgato S, D'Addabbo P, Archidiacono N, Battaglia P, Baroncini A, Capucci A, Stanyon R, Della Valle G, Rocchi M (2009) Evolutionary descent of a human chromosome 6 neocentromere: a jump back to 17 million years ago. Genome Res 19:778–784CrossRefPubMedPubMedCentralGoogle Scholar
  5. Fu SL, Lv ZL, Gao Z, Wu HJ, Pang JL, Zhang B, Dong QH, Guo X, Wang XJ, Birchler JA, Han FP (2013) De novo centromere formation on a chromosome fragment in maize. Proc Natl Acad Sci U S A 110:6033–6036CrossRefPubMedPubMedCentralGoogle Scholar
  6. Gong ZY, Wu YF, Koblizkova A, Torres GA, Wang K, Iovene M, Neumann P, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24:3559–3574CrossRefPubMedPubMedCentralGoogle Scholar
  7. Gong ZY, Yu HX, Huang J, Yi CD, Gu MH (2009) Unstable transmission of rice chromosomes without functional centromeric repeats in asexual propagation. Chromosom Res 17:863–872CrossRefGoogle Scholar
  8. Guo X, Su HD, Shi QH, Fu SL, Wang J, Zhang XQ, Hu ZM, Han FP (2016) De novo centromere formation and centromeric sequence expansion in wheat and its wide hybrids. PLoS Genet 12:e1005997CrossRefPubMedPubMedCentralGoogle Scholar
  9. Haas BJ, Delcher AL, Wortman JR, Salzberg SL (2004) DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20:3643–3646CrossRefPubMedGoogle Scholar
  10. Han YH, Zhang ZH, Liu CX, Liu JH, Huang SW, Jiang JM, Jin WW (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci U S A 106:14937–14941CrossRefPubMedPubMedCentralGoogle Scholar
  11. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102CrossRefPubMedGoogle Scholar
  12. Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, Kakuma T, Hiraoka Y, Takahashi K (2008) Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321:1088–1091CrossRefPubMedGoogle Scholar
  13. Jiang JM, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575CrossRefPubMedGoogle Scholar
  14. Jiao YP, Peluso P, Shi JH, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei XH, Chin CS, Guill K, Regulski M, Kumari S, Olson A, Gent J, Schneider KL, Wolfgruber TK, May MR, Springer NM, Antoniou E, McCombie WR, Presting GG, McMullen M, Ross-Ibarra J, Dawe RK, Hastie A, Rank DR, Ware D (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527PubMedGoogle Scholar
  15. Jin WW, Melo JR, Nagaki K, Talbert PB, Henikoff S, Dawe RK, Jiang JM (2004) Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16:571–581CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kalitsis P, Choo KHA (2012) The evolutionary life cycle of the resilient centromere. Chromosoma 121:327–340CrossRefPubMedGoogle Scholar
  17. Ketel C, Wang HSW, McClellan M, Bouchonville K, Selmecki A, Lahav T, Gerami-Nejad M, Berman J (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5:e1000400CrossRefPubMedPubMedCentralGoogle Scholar
  18. Koo DH, Han FP, Birchler JA, Jiang JM (2011) Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res 21:908–914CrossRefPubMedPubMedCentralGoogle Scholar
  19. Krueger F, Andrews SR (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27:1571–1572CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kynast RG, Riera-Lizarazu O, Vales MI, Okagaki RJ, Maquieira SB, Chen G, Ananiev EV, Odland WE, Russell CD, Stec AO, Livingston SM, Zaia HA, Rines HW, Phillips RL (2001) A complete set of maize individual chromosome additions to the oat genome. Plant Physiol 125:1216–1227CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lamb JC, Meyer JM, Birchler JA (2007) A hemicentric inversion in the maize line knobless Tama flint created two sites of centromeric elements and moved the kinetochore-forming region. Chromosoma 116:237–247CrossRefPubMedGoogle Scholar
  22. Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM http://arxiv.org/abs/1303.3997
  23. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079CrossRefPubMedPubMedCentralGoogle Scholar
  24. Li Q, Song J, West PT, Zynda G, Eichten SR, Vaughn MW, Springer NM (2015) Examining the causes and consequences of context-specific differential DNA methylation in maize. Plant Physiol 168:1262–1274CrossRefPubMedPubMedCentralGoogle Scholar
  25. Liu YL, Su HD, Pang JL, Goo Z, Wang XJ, Birchler JA, Han FP (2015) Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize. Proc Natl Acad Sci U S A 112:E1263–E1271CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lyons E, Pedersen B, Kane J, Freeling M (2008) The value of nonmodel genomes and an example using SynMap within CoGe to dissect the hexaploidy that predates the rosids. Trop Plant Biol 1:181–190CrossRefGoogle Scholar
  27. Marshall OJ, Chueh AC, Wong LH, Choo KHA (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Human Genet 82:261–282CrossRefGoogle Scholar
  28. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal 17:10–12CrossRefGoogle Scholar
  29. Nagaki K, Cheng ZK, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang JM (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145CrossRefPubMedGoogle Scholar
  30. Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang JM (2003) Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163:1221–1225PubMedPubMedCentralGoogle Scholar
  31. Nasuda S, Hudakova S, Schubert I, Houben A, Endo TR (2005) Stable barley chromosomes without centromeric repeats. Proc Natl Acad Sci U S A 102:9842–9847CrossRefPubMedPubMedCentralGoogle Scholar
  32. Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101:9903–9908CrossRefPubMedPubMedCentralGoogle Scholar
  33. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108:59–67CrossRefPubMedGoogle Scholar
  34. Saffery R, Irvine DV, Griffiths B, Kalitsis P, Wordeman L, Choo KHA (2000) Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins. Hum Mol Genet 9:175–185CrossRefPubMedGoogle Scholar
  35. Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci U S A 108:4069–4074CrossRefPubMedPubMedCentralGoogle Scholar
  36. Schnable PS, Ware D, Fulton RS, Stein JC, Wei FS, Pasternak S, Liang CZ, Zhang JW, Fulton L, Graves TA et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefPubMedGoogle Scholar
  37. Schneider KL, Xie ZD, Wolfgruber TK, Presting GG (2016) Inbreeding drives maize centromere evolution. Proc Natl Acad Sci U S A 113:E987–E996CrossRefPubMedPubMedCentralGoogle Scholar
  38. Scott KC, Sullivan BA (2014) Neocentromeres: a place for everything and everything in its place. Trends Genet 30:66–74CrossRefPubMedGoogle Scholar
  39. Shang WH, Hori T, Martins NMC, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A, Kimura H, Earnshaw WC, Fukagawa T (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24:635–648CrossRefPubMedPubMedCentralGoogle Scholar
  40. Stadler LJ, Roman H (1948) The effect of X-rays upon mutation of the gene A in maize. Genetics 33:273–303PubMedPubMedCentralGoogle Scholar
  41. Sullivan BA, Schwartz S (1995) Identification of centromeric antigens in dicentric robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Human Mol Genet 4:2189–2197CrossRefGoogle Scholar
  42. Swigonova Z, Lai JS, Ma JX, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923CrossRefPubMedPubMedCentralGoogle Scholar
  43. Thakur J, Sanyal K (2013) Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res 23:638–652CrossRefPubMedPubMedCentralGoogle Scholar
  44. Tolomeo D, Capozzi O, Stanyon RR, Archidiacono N, D'Addabbo P, Catacchio CR, Purgato S, Perini G, Schempp W, Huddleston J, Malig M, Eichler EE, Rocchi M (2017) Epigenetic origin of evolutionary novel centromeres. Sci Rep-Uk 7:41980CrossRefGoogle Scholar
  45. Topp CN, Okagaki RJ, Melo JR, Kynast RG, Phillips RL, Dawe RK (2009) Identification of a maize neocentromere in an oat-maize addition line. Cytogenet Genome Res 124:228–238CrossRefPubMedPubMedCentralGoogle Scholar
  46. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111CrossRefPubMedPubMedCentralGoogle Scholar
  47. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ventura M, Mudge JM, Palumbo V, Burn S, Blennow E, Pierluigi M, Giorda R, Zuffardi O, Archidiacono N, Jackson MS, Rocchi M (2003) Neocentromeres in 15q24-26 map to duplicons which flanked an ancestral centromere in 15q25. Genome Res 13:2059–2068CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ventura M, Weigl S, Carbone L, Cardone MF, Misceo D, Teti M, D'Addabbo P, Wandall A, Bjorck E, de Jong PJ, She XW, Eichler EE, Archidiacono N, Rocchi M (2004) Recurrent sites for new centromere seeding. Genome Res 14:1696–1703CrossRefPubMedPubMedCentralGoogle Scholar
  50. Voullaire LE, Slater HR, Petrovic V, Choo KHA (1993) A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: activation of a latent centromere? Am J Hum Genet 52:1153–1163PubMedPubMedCentralGoogle Scholar
  51. Wang H, Bennetzen JL (2012) Centromere retention and loss during the descent of maize from a tetraploid ancestor. Proc Natl Acad Sci U S A 109:21004–21009CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wang K, Wu YF, Zhang WL, Dawe RK, Jiang JM (2014) Maize centromeres expand and adopt a uniform size in the genetic background of oat. Genome Res 24:107–116CrossRefPubMedPubMedCentralGoogle Scholar
  53. Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S, Fuks G, Sanchez-Villeda H, Schroeder S, Fang Z, McMullen M, Davis G, Bowers JE, Paterson AH, Schaeffer M, Gardiner J, Cone K, Messing J, Soderlund C, Wing RA (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3:1254–1263CrossRefGoogle Scholar
  54. Wolfgruber TK, Sharma A, Schneider KL, Albert PS, Koo DH, Shi JH, Gao Z, Han FP, Lee H, Xu RH, Allison J, Birchler JA, Jiang JM, Dawe RK, Presting GG (2009) Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic loci shaped primarily by retrotransposons. PLoS Genet 5:e1000743CrossRefPubMedPubMedCentralGoogle Scholar
  55. Yunis JJ, Prakash O (1982) The origin of man—a chromosomal pictorial legacy. Science 215:1525–1530CrossRefPubMedGoogle Scholar
  56. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W (2009) A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952–1958CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zhang B, Lv ZL, Pang JL, Liu YL, Guo X, Fu SL, Li J, Dong QH, Wu HJ, Gao Z, Wang XJ, Han FP (2013) Formation of a functional maize centromere after loss of centromeric sequences and gain of ectopic sequences. Plant Cell 25:1979–1989CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zhang HQ, Koblizkova A, Wang K, Gong ZY, Oliveira L, Torres GA, Wu YF, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2014) Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26:1436–1447CrossRefPubMedPubMedCentralGoogle Scholar
  59. Zhao HN, Zhu XB, Wang K, Gent JI, Zhang WL, Dawe RK, Jiang JM (2016) Gene expression and chromatin modifications associated with maize centromeres. G3 6:183-192Google Scholar
  60. Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang JM, Dawe RK (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of HorticultureUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Wheat Genetics Resource Center, Department of Plant PathologyKansas State UniversityManhattanUSA
  3. 3.Division of Biological SciencesUniversity of MissouriColumbiaUSA

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