Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3
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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.
KeywordsCentromere CENH3 neocentromere centromeric genes centromeric chromatin
Flourescence in situ hybridization
Oat-maize chromosome addition
Single nucleotide polymorphism
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.
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.
- 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
- 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
- Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM http://arxiv.org/abs/1303.3997
- 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
- 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
- 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
- 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
- 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