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Centromere inactivation and epigenetic modifications of a plant chromosome with three functional centromeres

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Abstract

A chromosome with two functional centromeres is cytologically unstable and can only be stabilized when one of the two centromeres becomes inactivated via poorly understood mechanisms. Here, we report a transmissible chromosome with multiple centromeres in wheat. This chromosome encompassed one large and two small domains containing the centromeric histone CENH3. The two small centromeres are in a close vicinity and often fused as a single centromere on metaphase chromosomes. This fused centromere contained approximately 30% of the CENH3 compared to the large centromere. An intact tricentric chromosome was transmitted to about 70% of the progenies, which was likely a consequence of the dominating pulling capacity of the large centromere during anaphases of meiosis. The tricentric chromosome showed characteristics typical to dicentric chromosomes, including chromosome breaks and centromere inactivation. Remarkably, inactivation was always associated with the small centromeres, indicating that small centromeres are less likely to survive than large ones in dicentric chromosomes. The inactivation of the small centromeres also coincided with changes of specific histone modifications, including H3K27me2 and H3K27me3, of the pericentromeric chromatin.

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References

  • Agudo M, Abad JP, Molina I, Losada A, Ripoll P, Villasante A (2000) A dicentric chromosome of Drosophila melanogaster showing alternate centromere inactivation. Chromosoma 109:190–196

    Article  CAS  PubMed  Google Scholar 

  • Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937

    Article  CAS  PubMed  Google Scholar 

  • Alonso A, Mahmood R, Li SL, Cheung F, Yoda K, Warburton PE (2003) Genomic microarray analysis reveals distinct locations for the CENP-A binding domains in three human chromosome 13q32 neocentromeres. Hum Mol Genet 12:2711–2721

    Article  CAS  PubMed  Google Scholar 

  • Amor DJ, Bentley K, Ryan J, Perry J, Wong L, Slater H, Choo KHA (2004) Human centromere repositioning “in progress”. Proc Nat Acad Sci USA 101:6542–6547

    Article  CAS  PubMed  Google Scholar 

  • 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 19:778–784

    Article  CAS  PubMed  Google Scholar 

  • Cardone MF, Alonso A, Pazienza M, Ventura M, Montemurro G, Carbone L, de Jong PJ, Stanyon R, D'Addabbo P, Archidiacono N, She XW, Eichler EE, Warburton PE, Rocchi M (2006) Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. Genome Biol 7:R91

    Article  PubMed  Google Scholar 

  • Cheng ZK, Dong F, Langdon T, Ouyang S, Buell CB, Gu MH, Blattner FR, Jiang JM (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704

    Article  CAS  PubMed  Google Scholar 

  • Earnshaw WC, Migeon BR (1985) Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92:290–296

    Article  CAS  PubMed  Google Scholar 

  • Ferreri GC, Liscinsky DM, Mack JA, Eldridge MDB, O'Neill RJ (2005) Retention of latent centromeres in the mammalian genome. J Hered 96:217–224

    Article  CAS  PubMed  Google Scholar 

  • Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci 11:199–208

    Article  CAS  PubMed  Google Scholar 

  • Gill BS, Friebe B, Endo TR (1991) Standard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34:830–839

    Google Scholar 

  • Gross M, Starke H, Trifonov V, Claussen U, Liehr T, Weise A (2006) A molecular cytogenetic study of chromosome evolution in chimpanzee. Cytogenet Genome Res 112:67–75

    Article  CAS  PubMed  Google Scholar 

  • Han FP, Lamb JC, Birchler JA (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc Nat Acad Sci USA 103:3238–3243

    Article  CAS  PubMed  Google Scholar 

  • Han FP, Gao Z, Birchler JA (2009a) Reactivation of an inactive centromere reveals epigenetic and structural components for centromere specification in maize. Plant Cell 21:1929–1939

    Article  CAS  PubMed  Google Scholar 

  • Han YH, Zhang ZH, Liu CX, Liu JH, Huang SW, Jiang JM, Jin WW (2009b) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Nat Acad Sci USA 106:14937–14941

    Article  CAS  PubMed  Google Scholar 

  • Houben A, Wako T, Furushima-Shimogawara R, Presting G, Kunzel G, Schubert I, Fukui K (1999) The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J 18:675–679

    Article  CAS  PubMed  Google Scholar 

  • Irvine DV, Amor DJ, Perry J, Sirvent N, Pedeutour F, Choo KHA, Saffery R (2004) Chromosome size and origin as determinants of the level of CENP-A incorporation into human centromeres. Chromosome Res 12:805–815

    Article  CAS  PubMed  Google Scholar 

  • Jiang JM, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491

    Article  CAS  PubMed  Google Scholar 

  • Kaszas E, Cande WZ (2000) Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J Cell Sci 113:3217–3226

    CAS  PubMed  Google Scholar 

  • Koo DH, Jiang JM (2009) Super-stretched pachytene chromosomes for fluorescence in situ hybridization mapping and immunodetection of DNA methylation. Plant J 59:509–516

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Yue W, Li DY, Wang RRC, Kong XY, Lu K, Wang GX, Dong YS, Jin WW, Zhang XY (2008) Structure and dynamics of retrotransposons at wheat centromeres and pericentromeres. Chromosoma 117:445–456

    Article  CAS  PubMed  Google Scholar 

  • Lo AW, Craig JM, Saffery R, Kalitsis P, Irvine DV, Earle E, Magliano DJ, Choo KH (2001a) A 330 kb CENP-A binding domain and altered replication timing at a human neocentromere. EMBO J 20:2087–2096

    Article  CAS  PubMed  Google Scholar 

  • Lo AWI, Magliano DJ, Sibson MC, Kalitsis P, Craig JM, Choo KHA (2001b) A novel chromatin immunoprecipitation and array (CIA) analysis identifies a 460-kb CENP-A-binding neocentromere DNA. Genome Res 11:448–457

    Article  CAS  PubMed  Google Scholar 

  • Manzanero S, Arana P, Puertas MJ, Houben A (2000) The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109:308–317

    Article  CAS  PubMed  Google Scholar 

  • Marshall OJ, Chueh AC, Wong LH, Choo KHA (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282

    Article  CAS  PubMed  Google Scholar 

  • Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6:838–849

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1939) The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc Natl Acad Sci USA 25:405–416

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1941) The stability of broken ends of chromosomes in Zea mays. Genetics 26:234–282

    CAS  PubMed  Google Scholar 

  • Miller JT, Dong F, Jackson SA, Song J, Jiang J (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150:1615–1623

    CAS  PubMed  Google Scholar 

  • Montefalcone G, Tempesta S, Rocchi M, Archidiacono N (1999) Centromere repositioning. Genome Res 9:1184–1188

    Article  CAS  PubMed  Google Scholar 

  • 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 36:138–145

    Article  CAS  PubMed  Google Scholar 

  • Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, Larionov V, Earnshaw WC, Masumoto H (2008) Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 14:507–522

    Article  CAS  PubMed  Google Scholar 

  • Nasuda S, Hudakova S, Schubert I, Houben A, Endo TR (2005) Stable barley chromosomes without centromeric repeats. Proc Natl Acad Sci USA 102:9842–9847

    Article  CAS  PubMed  Google Scholar 

  • Nath J, Tucker JD, Hando JC (1995) Y chromosome aneuploidy, micronuclei, kinetochores and aging in men. Chromosoma 103:725–731

    Article  CAS  PubMed  Google Scholar 

  • Naumann K, Fischer A, Hofmann I, Krauss V, Phalke S, Irmler K, Hause G, Aurich AC, Dorn R, Jenuwein T, Reuter G (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24:1418–1429

    Article  CAS  PubMed  Google Scholar 

  • Presting GG, Malysheva L, Fuchs J, Schubert I (1998) A Ty3/gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J 16:721–728

    Article  CAS  PubMed  Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma XF, Miftahudin GJP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16, 000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  CAS  PubMed  Google Scholar 

  • Sears ER, Camara A (1952) A transmissible discentric chromosome. Genetics 37:125–135

    CAS  PubMed  Google Scholar 

  • Stanyon R, Rocchi M, Capozzi O, Roberto R, Misceo D, Ventura M, Cardone MF, Bigoni F, Archidiacono N (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosome Res 16:17–39

    Article  CAS  PubMed  Google Scholar 

  • Sullivan BA, Karpen GH (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11:1076–1083

    Article  CAS  PubMed  Google Scholar 

  • Sullivan BA, Schwartz S (1995) Identification of centromeric antigens in dicentric robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum Mol Genet 4:2189–2197

    Article  CAS  PubMed  Google Scholar 

  • Sullivan BA, Willard HF (1998) Stable dicentric X chromosomes with two functional centromeres. Nat Genet 20:227–228

    Article  CAS  PubMed  Google Scholar 

  • 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 124:228–238

    Article  CAS  PubMed  Google Scholar 

  • Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:855–866

    Article  CAS  Google Scholar 

  • Ventura M, Archidiacono N, Rocchi M (2001) Centromere emergence in evolution. Genome Res 11:595–599

    Article  CAS  PubMed  Google Scholar 

  • Ventura M, Antonacci F, Cardone MF, Stanyon R, D'Addabbo P, Cellamare A, Sprague LJ, Eichler EE, Archidiacono N, Rocchi M (2007) Evolutionary formation of new centromeres in macaque. Science 316:243–246

    Article  CAS  PubMed  Google Scholar 

  • 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 52:1153–1163

    CAS  PubMed  Google Scholar 

  • Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD (1998) Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Nat Acad Sci USA 95:7480–7484

    Article  CAS  PubMed  Google Scholar 

  • Williams BC, Murphy TD, Goldberg ML, Karpen GH (1998) Neocentromere activity of structurally acentric mini-chromosomes in Drosophila. Nat Genet 18:30–37

    Article  CAS  PubMed  Google Scholar 

  • Wong NC, Wong LH, Quach JM, Canham P, Craig JM, Song JZ, Clark SJ, Choo KHA (2006) Permissive transcriptional activity at the centromere through pockets of DNA hypomethylation. PLoS Genet 2:172–186

    Article  CAS  Google Scholar 

  • Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530

    Article  CAS  PubMed  Google Scholar 

  • Zhang XY, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5:1026–1035

    CAS  Google Scholar 

  • Zhang WL, Lee HR, Koo DH, Jiang JM (2008) Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20:25–34

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Yufeng Wu for statistical analysis of the data in Table 2 and Dr. Kelly Dawe for his comments on the manuscript. This research was partially supported by grants DBI-0603927 and DBI-0553417 from the National Science Foundation.

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Authors and Affiliations

  1. Department of Horticulture, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Wenli Zhang & Jiming Jiang

  2. Department of Plant Pathology, Wheat Genetic and Genomic Resources Center, Kansas State University, Manhattan, KS, 66506, USA

    Bernd Friebe & Bikram S. Gill

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  1. Wenli Zhang
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  2. Bernd Friebe
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Correspondence to Jiming Jiang.

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Communicated by I. Schubert

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Supplementary Fig. 1

Distribution of H3K27me3 on wheat chromosomes. a H3K27me3 immunofluorescence (red) pattern of a metaphase cell from a plant containing a single mi7BStri chromosome (arrow). b Sequential immunofluorescence assay using anti-CENH3 antibodies (green). The faint green signals at the distal ends of the chromosomes, an example pointed by the arrowhead, were derived from H3K27me3. The H3K27me3 signals were not completely washed off after the first round of immunofluorescence assay. Bar = 10 μm. (GIF 145 kb)

High-resolution image (TIFF 4543 kb)

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Zhang, W., Friebe, B., Gill, B.S. et al. Centromere inactivation and epigenetic modifications of a plant chromosome with three functional centromeres. Chromosoma 119, 553–563 (2010). https://doi.org/10.1007/s00412-010-0278-5

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