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Identification and diversity of functional centromere satellites in the wild rice species Oryza brachyantha

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Abstract

The centromere is a key chromosomal component for sister chromatid cohesion and is the site for kinetochore assembly and spindle fiber attachment, allowing each sister chromatid to faithfully segregate to each daughter cell during cell division. It is not clear what types of sequences act as functional centromeres and how centromere sequences are organized in Oryza brachyantha, an FF genome species. In this study, we found that the three classes of centromere-specific CentO-F satellites (CentO-F1, CentO-F2, and CentO-F3) in O. brachyantha share no homology with the CentO satellites in Oryza sativa. The three classes of CentO-F satellites are all located within the chromosomal regions to which the spindle fibers attach and are characterized by megabase tandem arrays that are flanked by centromere-specific retrotransposons, CRR-F, in the O. brachyantha centromeres. Although these CentO-F satellites are quantitatively variable among 12 O. brachyantha centromeres, immunostaining with an antibody specific to CENH3 indicates that they are colocated with CENH3 in functional centromere regions. Our results demonstrate that the three classes of CentO-F satellites may be the major components of functional centromeres in O. brachyantha.

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Abbreviations

BAC:

bacterial artificial chromosome

CentO-F:

centromere-specific satellite repeat of FF genome

CRR-F:

centromere-specific retrotransposon of FF genome

FISH:

fluorescence in-situ hybridization

CEN:

centromere of chromosome

References

  • Aggarwal RK, Brar DS, Khush GS (1997) Two new genomes in the Oryza complex identified on the basis of molecular divergence analysis using total genomic DNA hybridization. Mol Gen Genet 254:1–12

    Article  CAS  PubMed  Google Scholar 

  • Alfenito MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589–597

    CAS  PubMed  Google Scholar 

  • Ammiraju JS, Lu F, Sanyal A, Yu Y, Song X, Jiang N, Pontaroli AC, Rambo T, Currie J, Collura K, Talag J, Fan C, Goicoechea JL, Zuccolo A, Chen J, Bennetzen JL, Chen M, Jackson S, Wing RA (2008) Dynamic evolution of oryza genomes is revealed by comparative genomic analysis of a genus-wide vertical data set. Plant Cell 20:3191–3209

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Amor DJ, Kalitsis P, Sumer H, Choo KH (2004) Building the centromere: from foundation proteins to 3D organization. Trends Cell Biol 14:359–368

    Article  CAS  PubMed  Google Scholar 

  • Bao W, Zhang W, Yang Q, Zhang Y, Han B, Gu M, Xue Y, Cheng Z (2006) Diversity of centromeric repeats in two closely related wild rice species, Oryza officinalis and Oryza rhizomatis. Mol Genet Genom 275:421–430

    Article  CAS  Google Scholar 

  • Bennetzen JL (2007) Patterns in grass genome evolution. Curr Opin Plant Biol 10:176–181

    Article  CAS  PubMed  Google Scholar 

  • Brandes A, Thompson H, Dean C, Heslop-Harrison JS (1997) Multiple repetitive DNA sequences in the paracentromeric regions of Arabidopsis thaliana L. Chromosom Res 5:238–246

    Article  CAS  Google Scholar 

  • Brar DS, Khush GS (1997) Alien introgression in rice. Plant Mol Biol 35:35–47

    Google Scholar 

  • Cheng Z, Buell CR, Wing RA, Jiang J (2002a) Resolution of fluorescence in-situ hybridization mapping on rice mitotic prometaphase chromosomes, meiotic pachytene chromosomes and extended DNA fibers. Chromosom Res 10:379–387

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choo KH, Vissel B, Nagy A, Earle E, Kalitsis P (1991) A survey of the genomic distribution of alpha satellite DNA on all the human chromosomes, and derivation of a new consensus sequence. Nucleic Acids Res 19:1179–1182

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clarke L (1990) Centromeres of budding and fission yeasts. Trends Genet 6:150–154

    Article  CAS  PubMed  Google Scholar 

  • Clarke L (1998) Centromeres: proteins, protein complexes, and repeated domains at centromeres of simple eukaryotes. Curr Opin Genet Dev 8:212–218

    Article  CAS  PubMed  Google Scholar 

  • Devos KM, Gale MD (1997) Comparative genetics in the grasses. Plant Mol Biol 35:3–15

    Article  CAS  PubMed  Google Scholar 

  • Dong F, Miller JT, Jackson SA, Wang GL, Ronald PC, Jiang J (1998) Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc Natl Acad Sci U S A 95:8135–8140

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gao D, Gill N, Kim HR, Walling JG, Zhang W, Fan C, Yu Y, Ma J, SanMiguel P, Jiang N, Cheng Z, Wing RA, Jiang J, Jackson SA (2009) A lineage-specific centromere retrotransposon in Oryza brachyantha. Plant J 60:820–831

    Article  CAS  PubMed  Google Scholar 

  • Ge S, Sang T, Lu BR, Hong DY (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci U S A 96:14400–14405

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hall AE, Keith KC, Hall SE, Copenhaver GP, Preuss D (2004) The rapidly evolving field of plant centromeres. Curr Opin Plant Biol 7:108–114

    Article  CAS  PubMed  Google Scholar 

  • Hall SE, Kettler G, Preuss D (2003) Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res 13:195–205

    Article  CAS  PubMed  Google Scholar 

  • Harrington JJ, Van Bokkelen G, Mays RW, Gustashaw K, Willard HF (1997) Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet 15:345–355

    Article  CAS  PubMed  Google Scholar 

  • Harrison GE, Heslop-Harrison JS (1995) Centromeric repetitive DNA sequences in the genus Brassica. Theor Appl Genet 90:157–165

    Article  CAS  PubMed  Google Scholar 

  • Hass BL, Pires JC, Porter R, Phillips RL, Jackson SA (2003) Comparative genetics at the gene and chromosome levels between rice ( Oryza sativa) and wildrice ( Zizania palustris). Theor Appl Genet 107:773–782

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  CAS  PubMed  Google Scholar 

  • Jackson SA, Wang ML, Goodman HM, Jiang J (1998) Application of fiber-FISH in physical mapping of Arabidopsis thaliana. Genome 41:566–572

    CAS  PubMed  Google Scholar 

  • Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, 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 U S A 92:4487–4491

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kang TJ, Yang MS (2004) Rapid and reliable extraction of genomic DNA from various wild-type and transgenic plants. BMC Biotechnol 4:20

    Article  PubMed Central  PubMed  Google Scholar 

  • Le MH, Duricka D, Karpen GH (1995) Islands of complex DNA are widespread in Drosophila centric heterochromatin. Genetics 141:283–303

    CAS  PubMed  Google Scholar 

  • Lee HR, Zhang W, Langdon T, Jin W, Yan H, Cheng Z, Jiang J (2005) Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc Natl Acad Sci U S A 102:11793–11798

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu F, Ammiraju JS, Sanyal A, Zhang S, Song R, Chen J, Li G, Sui Y, Song X, Cheng Z, de Oliveira AC, Bennetzen JL, Jackson SA, Wing RA, Chen M (2009) Comparative sequence analysis of MONOCULM1-orthologous regions in 14 Oryza genomes. Proc Natl Acad Sci U S A 106:2071–2076

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martinez-Zapater JM, Estelle MA, Somerville CR (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204:417–423

    Article  CAS  Google Scholar 

  • Murata M (2002) Telomeres and Centromeres in Plants. Current Genom 3:527–538

    Article  CAS  Google Scholar 

  • Murphy TD, Karpen GH (1995) Localization of centromere function in a Drosophila minichromosome. Cell 82:599–609

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Song J, Stupar RM, Parokonny AS, Yuan Q, Ouyang S, Liu J, Hsiao J, Jones KM, Dawe RK, Buell CR, Jiang J (2003) Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics 163:759–770

    CAS  PubMed  Google Scholar 

  • Palmer D, Kevany M, Mackworth-Young C, Batchelor R, Lombardi G, Lechler R (1991) Generation and characterization of an HLA-DR alpha-specific monoclonal antibody using L-cell transfectants expressing human and mouse class II major histocompatibility dimers. Immunogenetics 33:12–17

    Article  CAS  PubMed  Google Scholar 

  • Peterson, D.G., Tomkins, J.P., Frisch, D.A., Wing, R.A., and Paterson, A.H. (2000). Construction of plant bacterial artificial chromosome (BAC) libraries: An illustrated guide. Journal of Agricultural Genomics 5:www.ncgr.org/research/jag

  • Round EK, Flowers SK, Richards EJ (1997) Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res 7:1045–1053

    CAS  PubMed  Google Scholar 

  • Singer MF (1982) Highly repeated sequences in mammalian genomes. Int Rev Cytol 76:67–112

    CAS  PubMed  Google Scholar 

  • Sullivan KF, Hechenberger M, Masri K (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127:581–592

    Article  CAS  PubMed  Google Scholar 

  • Talbert PB, Bryson TD, Henikoff S (2004) Adaptive evolution of centromere proteins in plants and animals. J Biol 3:18

    Article  PubMed Central  PubMed  Google Scholar 

  • Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–1066

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488

    Article  CAS  PubMed  Google Scholar 

  • Tyler-Smith C, Oakey RJ, Larin Z, Fisher RB, Crocker M, Affara NA, Ferguson-Smith MA, Muenke M, Zuffardi O, Jobling MA (1993) Localization of DNA sequences required for human centromere function through an analysis of rearranged Y chromosomes. Nat Genet 5:368–375

    Article  CAS  PubMed  Google Scholar 

  • Vafa O, Sullivan KF (1997) Chromatin containing CENP-A and alpha-satellite DNA is a major component of the inner kinetochore plate. Curr Biol 7:897–900

    Article  CAS  PubMed  Google Scholar 

  • Vaughan DA, Morishima H, Kadowaki K (2003) Diversity in the Oryza genus. Curr Opin Plant Biol 6:139–146

    Article  CAS  PubMed  Google Scholar 

  • Warburton PE, Cooke CA, Bourassa S, Vafa O, Sullivan BA, Stetten G, Gimelli G, Warburton D, Tyler-Smith C, Sullivan KF, Poirier GG, Earnshaw WC (1997) Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol 7:901–904

    Article  CAS  PubMed  Google Scholar 

  • Willard HF, Waye JS (1987) Chromosome-specific subsets of human alpha satellite DNA: analysis of sequence divergence within and between chromosomal subsets and evidence for an ancestral pentameric repeat. J Mol Evol 25:207–214

    Article  CAS  PubMed  Google Scholar 

  • Wolfgruber TK, Sharma A, Schneider KL, Albert PS, Koo DH, Shi J, Gao Z, Han F, Lee H, Xu R, Allison J, Birchler JA, Jiang J, 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:e1000743

    Article  PubMed Central  PubMed  Google Scholar 

  • Yi CD, Gong ZY, Liang GH, Wang FH, Tang SZ, Gu MH (2007) Isolation and characterization of the centromeric BAC clones from differnet genomes in genus Oryza. HEREDITAS (Beijing) 29:851–858

    Article  CAS  Google Scholar 

  • Zhang D, Yang Q, Bao W, Zhang Y, Han B, Xue Y, Cheng Z (2005a) Molecular cytogenetic characterization of the Antirrhinum majus genome. Genetics 169:325–335

    Article  CAS  PubMed  Google Scholar 

  • Zhang, W. (2005). Functional Analysis of Centromeric Elements of Two Diploid Genomes BB and FF in Oryza Genus. [D].Beijing:Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

  • Zhang W, Yi C, Bao W, Liu B, Cui J, Yu H, Cao X, Gu M, Liu M, Cheng Z (2005b) The transcribed 165-bp CentO satellite is the major functional centromeric element in the wild rice species Oryza punctata. Plant Physiol 139:306–315

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang J, Dawe RK (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Basic Research Program of China (“973” Program, 2010CB125904, 2013CBA01405), the National Natural Science Foundation of China (31071382, 30771210) and the Priority Academic Program Development of Jiangsu Higher Education Institutions(PAPD).

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Correspondence to Chuandeng Yi or Minghong Gu.

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Responsible Editor: Hans de Jong.

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KF293389-KF293391)

Chuandeng Yi and Wenli Zhang contributed equally to this work.

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Yi, C., Zhang, W., Dai, X. et al. Identification and diversity of functional centromere satellites in the wild rice species Oryza brachyantha. Chromosome Res 21, 725–737 (2013). https://doi.org/10.1007/s10577-013-9374-8

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