Composition and Structure of Rice Centromeres and Telomeres

  • Hiroshi Mizuno
  • Takashi Matsumoto
  • Jianzhong Wu


Complete or partial sequences of centromeres and telomeres of a number of rice chromosomes are now publicly available. In this chapter, we summarize the current findings on the DNA content and structure of these special regions. Core regions of rice centromeres consist of the satellite repeat CentO organized in tandem arrays and copies of the Ty3/gypsy-type retrotransposon CRR physically associated with the CentO arrays. The physical size of CentO arrays differs considerably among individual chromosomes. Unexpectedly, rice centromeres also contain active genes. Telomere satellite repeat arrays are highly conserved within the plant kingdom, but their length varies considerably among species and even among rice chromosomes. Frequent nucleotide substitutions and rearrangements of the satellite repeat sequences are detected mainly within the proximal telomere regions in rice. Subtelomere-associated repeats appear to be species-specific; at least 14 of its 24 chromosomal ends in the rice cultivar Nipponbare contain no TrsA sequences, that is, the telomere arrays are directly attached to gene-containing regions. Despite the conservation of functions, both centromeres and telomeres in rice reveal a considerable size variation and sequence divergence, thereby providing insights into the structural and evolutionary dynamics of these highly heterochromatic regions.


Rice Centromere Telomere Satellite repeat array Retrotransposon 



We thank the editors of this book for their valuable comments and suggestions, all the former members of the Rice Genome Research Program for their scientific contributions, and the Ministry of Agriculture, Forestry and Fisheries of Japan for its financial supporting on the above works.


  1. Ammiraju JSS, Yu Y, Luo M, Kudrna D, Kim H, Goicoechea JL, Katayose Y, Matsumoto T, Wu J, Sasaki T, Wing RA (2005) Random sheared fosmid library as a new genomic tool to accelerate complete finishing of rice (Oryza sativa spp. Nipponbare) genome sequence: sequencing of gap-specific fosmid clones uncovers new euchromatic portions of the genome. Theor Appl Genet 111:1596–1607CrossRefPubMedGoogle Scholar
  2. Baur JA, Zou Y, Shay JW, Wright WE (2001) Telomere position effect in human cells. Science 292:2075–2077CrossRefPubMedGoogle Scholar
  3. Burr B, Burr FA, Matz EC, Romero-Severson J (1992) Pinning down loose ends: mapping telomeres and factors affecting their length. Plant Cell 4:953–960CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chen M, Presting G, Barbazuk WB, Goicoechea JL, Blackmon B, Fang G, Kim H, Frisch D, Yu Y, Sun S et al (2002) An integrated physical and genetic map of the rice genome. Plant Cell 14:537–545CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR, Gu M, Blattner FR, Jiang J (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cheng C-H, Chung M-C, Liu S-M, Chen S-K, Kao F-Y, Lin S-J, Hsiao S-H, Tseng I-C, Hsing Y-IC, Wu H-P et al (2005) A fine physical map of the rice chromosome 5. Mol Gen Genomics 274:337–345CrossRefGoogle Scholar
  7. Copenhaver GP, Nickel K, Kuromori T, Benito M-I, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD et al (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468–2474CrossRefPubMedGoogle Scholar
  8. Dong F, Miller JT, Jackson SA, Wang G-L, Ronald RC (1998) Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc Natl Acad Sci U S A 95:8135–8140CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fajkus J, Kovarik A, Kralovics R, Bezdek M (1995a) Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet 247:633–638CrossRefPubMedGoogle Scholar
  10. Fajkus J, Kralovics R, Kovarik A, Fajkusova L (1995b) The telomeric sequence is directly attached to the HRS60 subtelomeric tandem repeat in tobacco chromosomes. FEBS Lett 364:33–35CrossRefPubMedGoogle Scholar
  11. Fan C, Walling JG, Zhang J, Hirsch CD, Jiang J, Wing RA (2011) Conservation and purifying selection of transcribed gene located in a rice centromere. Plant Cell 23:2821–2830CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fujisawa M, Yamagata H, Kamiya K, Nakamura M, Saji S, Kanamori H, Wu J, Matsumoto T, Sasaki T (2006) Sequence comparison of distal and proximal ribosomal DNA arrays in rice (Oryza sativa L.) chromosome 9S and analysis of their flanking regions. Theor Appl Genet 113(3):419–428CrossRefPubMedGoogle Scholar
  13. Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3:87–94CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hall AE, Keith KC, Hall SE, Copenhaver GP, Preuss D (2004) The rapidly evolving field of plant centromeres. Curr Opin Plant Biol 7:108–114CrossRefPubMedGoogle Scholar
  15. Han B, Xue YB, Jia L, Deng X-W, Zhang Q (2007) Rice functional genomics research in China. Philos Trans R Soc B 362:1009–1021CrossRefGoogle Scholar
  16. Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin S-Y, Antonio BA, Parco A et al (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148:479–494PubMedPubMedCentralGoogle Scholar
  17. Heslop-Harrison JS, Murata M, Ogura Y, Schwarzacher, Motoyoshi F (1999) Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11:31–42CrossRefPubMedPubMedCentralGoogle Scholar
  18. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  19. Jiang J (2013) Rice centromeres. In: Jiang J, Birchler JA (eds) Plant centromere biology. Wiley-Blackwell, Oxford. CrossRefGoogle Scholar
  20. Jiang J, Nasuda S, Dong F, Scherrer CW, Woo S-S, Wing RA, Gill BS, Ward DC (1996) A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci U S A 93:14210–14213CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S et al (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4CrossRefPubMedPubMedCentralGoogle Scholar
  22. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34CrossRefPubMedGoogle Scholar
  23. Kilian A, Kleinhofs A (1992) Cloning and mapping of telomere-associated sequences from Hordeum vulgare L. Mol Gen Genet 235:153–156CrossRefPubMedGoogle Scholar
  24. Kilian A, Stiff C, Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci U S A 92:9555–9559CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ko S, Yu EY, Shin J, Yoo HH, Tanaka T, Kim WT, Cho H-S, Lee W, Chung IK (2009) Solution structure of the DNA binding domain of rice telomere binding protein RTBP1. Biochemistry 48(5):827–838CrossRefPubMedGoogle Scholar
  26. Kotani H, Hosouchi T, Tsuruoka H (1999) Structural analysis and complete physical map of Arabidopsis thaliana chromosome 5 including centromeric and telomeric regions. DNA Res 6:381–386CrossRefPubMedGoogle Scholar
  27. Lamb JC, Birchler JA (2003) The role of DNA sequence in centromere formation. Genome Biol 4:214CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lamb JC, Theuri J, Birchler JA (2004) What’s in a centromere? Genome Biol 5:239CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lamb JC, Yu W, Han F, Birchler JA (2007) Plant chromosomes from end to end: telomeres, heterochromatin and centromeres. Curr Opin Plant Biol 10:116–122CrossRefPubMedGoogle Scholar
  30. Langdon T, Seago C, Mende M, Leggett M, Thomas H, Forster JW, Thomas H, Jones RN, Jenkins G (2000) Retrotransposon evolution in diverse plant genomes. Genetics 156:313–325PubMedPubMedCentralGoogle Scholar
  31. Li B, Lustig AJ (1996) A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev 10:1310–1326CrossRefPubMedGoogle Scholar
  32. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404–12410CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ma J, Wing RA, Bennetzen JL, Jackson SA (2007a) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 23(3):134–139CrossRefPubMedGoogle Scholar
  34. Ma J, Wing RA, Bennetzen JL, Jackson SA (2007b) Evolutionary history and positional shift of a rice centromere. Genetics 177:1217–1220CrossRefPubMedPubMedCentralGoogle Scholar
  35. Macas J, Neumann P, Novak P, Jiang J (2010) Global sequence characterization of rice centromeric satellite based on oligomer frequency analysis in large-scale sequencing data. Bioinformatics 26(17):2101–2108CrossRefPubMedGoogle Scholar
  36. Majerova E, Mandakova T, Vu GTH, Fajkus J, Lysak MA, Fojtova M (2014) Chromatin features of plant telomeric sequences at terminal vs. internal positions. Front Plant Sci 5:593CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mao L, Devos KM, Zhu L, Gale MD (1997) Cloning and genetic mapping of wheat telomere-associated sequences. Mol Gen Genet 254:584–591CrossRefPubMedGoogle Scholar
  38. Matsumoto T, Wu J, Itoh T, Numa H, Antonio B, Sasaki T (2016) The Nipponbare genome and the next-generation of rice genomics research in Japan. Rice 9:33CrossRefPubMedPubMedCentralGoogle Scholar
  39. Miller JT, Dong F, Jackson SA, Song J, Jiang J (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150:1615–1623PubMedPubMedCentralGoogle Scholar
  40. Mizuno H, Wu J, Kanamori H, Fujisawa M, Namiki N, Saji S, Katagiri S, Katayose Y, Sasaki T, Matsumoto T (2006) Sequencing and characterization of telomere and subtelomere regions on rice chromosomes 1S, 2S, 2L, 6L, 7S, 7L and 8S. Plant J 46:206–217CrossRefPubMedGoogle Scholar
  41. Mizuno H, Wu J, Katayose Y, Kanamori H, Sasaki T, Matsumoto T (2008a) Chromosome-specific distribution of nucleotide substitutions in telomeric repeats of rice (Oryza sativa L.) Mol Biol Evol 25:62–68CrossRefPubMedGoogle Scholar
  42. Mizuno H, Wu J, Katayose Y, Kanamori H, Sasaki T, Matsumoto T (2008b) Characterization of chromosome ends on the basis of the structure of TrsA subtelomeric repeats in rice (Oryza sativa L.) Mol Gen Genomics 280:19–24CrossRefGoogle Scholar
  43. Mizuno H, Kawahara Y, Wu J, Katayose Y, Kanamori H, Ikawa H, Itoh T, Sasaki T, Matsumoto T (2011) Asymmetric distribution of gene expression in the centromeric region of rice chromosome 5. Front Plant Sci 2:16CrossRefPubMedPubMedCentralGoogle Scholar
  44. Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53CrossRefPubMedGoogle Scholar
  45. Nagaki K (2009) Components and structures of plant centromeres. Chromosome Sci 12:5–11Google Scholar
  46. 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 163:759–770PubMedPubMedCentralGoogle Scholar
  47. 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(2):138–145CrossRefPubMedGoogle Scholar
  48. Nagaki K, Neumann P, Zhang D, Ouyang S, Buell CR, Cheng Z, Jiang J (2005) Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. Mol Biol Evol 22(4):845–855CrossRefPubMedGoogle Scholar
  49. Nonomura K-I, Kurata N (1999) Organization of the 1.9-kb repeat unit RCE1 in the centromeric region of rice chromosomes. Mol Gen Genet 261:1–10CrossRefPubMedGoogle Scholar
  50. Nonomura K-I, Kurata N (2001) The centromere composition of multiple repetitive sequences on rice chromosome 5. Chromosoma 110:284–291CrossRefPubMedGoogle Scholar
  51. Ohtsubo H, Ohtsubo E (1994) Involvement of transposition in dispersion of tandem repeat sequences (TrsA) in rice genomes. Mol Gen Genet 245:449–455. 254CrossRefPubMedGoogle Scholar
  52. Ohtsubo H, Umeda M, Ohtsubo E (1991) Organization of DNA sequences highly repeated in tandem in rice genomes. Jpn J Genet 66:241CrossRefPubMedGoogle Scholar
  53. Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53:127–136CrossRefPubMedGoogle Scholar
  54. Richards EJ, Dawe RK (1998) Plant centromeres: structure and control. Curr Opin Plant Biol 1:130–135CrossRefPubMedGoogle Scholar
  55. Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698CrossRefPubMedPubMedCentralGoogle Scholar
  56. Roder MS, Lapitan NL, Sorrells ME, Tanksley SD (1993) Genetic and physical mapping of barley telomeres. Mol Gen Genet 238:294–303PubMedGoogle Scholar
  57. Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115CrossRefPubMedGoogle Scholar
  58. Sykorova E, Lim KY, Kunicka Z, Chase MW, Bennett MD, Fajkus J, Leitch AR (2003) Telomere variability in the monocotyledonous plant order Asparagales. Proc R Soc Lond B 270:1893–1904CrossRefGoogle Scholar
  59. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–781CrossRefGoogle Scholar
  60. Vaquero-Sedas MI, Vega-Palas MA (2014) Determination of Arabidopsis thaliana telomere length by PCR. Sci Rep 4:5540CrossRefPubMedPubMedCentralGoogle Scholar
  61. Watson J, Shippen DE (2007) Telomere rapid deletion regulates telomere length in Arabidopsis thaliana. Mol Cell Biol 27:1706–1715CrossRefPubMedGoogle Scholar
  62. Wu K-S, Tanksley SD (1993) Genetic and physical mapping of telomeres and macrosatellites of rice. Plant Mol Biol 22:861–872CrossRefPubMedGoogle Scholar
  63. Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J et al (2002) A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14:525–535CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wu J, Mizuno H, Hayashi-Tsugane M, Ito Y, Chidem Y, Fujisawa M, Katagiri S, Saji S, Yoshiki S, Karasawa W et al (2003) Physical maps and recombination frequency of 6 rice chromosomes. Plant J 36:720–730CrossRefPubMedGoogle Scholar
  65. Wu J, Yamagata H, Hayashi-Tsugane M, Hijishita S, Fujisawa M, Shibata M, Ito Y, Nakamura M, Sakaguchi M, Yoshihara R et al (2004) Composition and structure of the centromeric region of rice chromosome 8. Plant Cell 16:967–976CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wu J, Mizuno H, Sasaki T, Matsumoto T (2008) Comparative analysis of rice genome sequence to understand the molecular basis of genome evolution. Rice 1(2):119–126CrossRefGoogle Scholar
  67. Wu J, Fujisawa M, Tian Z, Yamagata H, Kamiya K, Shibata M, Hosokawa S, Ito Y, Hamada M, Katagiri S et al (2009) Comparative analysis of complete orthologous centromeres from two subspecies of rice reveals rapid variation of centromere organization and structure. Plant J 60(5):805–819CrossRefPubMedGoogle Scholar
  68. Yan H, Jiang J (2007) Rice as a model for centromere and heterochromatin research. Chromosom Res 15:77–84CrossRefGoogle Scholar
  69. Yan H, Ito H, Nobuta K, Ouyang S, Jin W, Tian S, Lu C, Venu RC, Wang G-L, Green PJ et al (2006) Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere. Plant Cell 18:2123–2133CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yan H, Talbert PB, Lee H-R, Jett J, Henikoff S, Chen F, Jiang J (2008) Intergenic locations of rice centromeric chromatin. PLoS Biol 6(11):e286. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yan H, Kikuchi S, Neumann P, Zhang W, Wu Y, Chen F, Jiang J (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63:353–365CrossRefPubMedGoogle Scholar
  72. Yang T-J, Yu Y, Chang S-B, de Jong H, Oh C-S, Ahn S-N, Fang E, Wing RA (2005) Toward closing rice telomere gaps: mapping and sequence characterization of rice subtelomere regions. Theor Appl Genet 111:467–478CrossRefPubMedGoogle Scholar
  73. Yi C, Zhang W, Dai X, Li X, Gong Z, Zhou Y, Liang G, Gu M (2013) Identification and diversity of functional centromere satellites in the wild rice species Oryza brachyantha. Chromosom Res 21:725–737CrossRefGoogle Scholar
  74. Zhang Y, Huang Y, Zhang L, Li Y, Lu T, Lu Y, Feng Q, Zhao Q, Cheng Z, Xue Y, Wing RA, Han B (2004) Structural features of the rice chromosome 4 centromere. Nucleic Acids Res 32(6):2023–2030CrossRefPubMedPubMedCentralGoogle Scholar
  75. Zhang W, Yi C, Bao W, Liu B, Cui J, Yu H, Cao X, Gu M, Liu M, Cheng Z (2005) The transcribed 165-bp CentO satellite is the major functional centromeric element in the wild rice species Oryza punctata. Plant Physiol 139:306–315CrossRefPubMedPubMedCentralGoogle Scholar
  76. Zhong XB, Fransz PF, Wennekes-Eden J, Ramanna MS, van Kammen A, Zabel P, Hans de Jong J (1998) FISH studies reveal the molecular and chromosomal organization of individual telomere domains in tomato. Plant J 13:507–517CrossRefPubMedGoogle Scholar
  77. Zuo J, Li J (2013) Molecular dissection of complex agronomic traits of rice: a team effort by Chinese scientists in recent years. Natl Sci Rev 1(2):253–276CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Hiroshi Mizuno
    • 1
  • Takashi Matsumoto
    • 1
    • 2
  • Jianzhong Wu
    • 1
  1. 1.Institute of Crop ScienceNational Agriculture and Food Research OrganizationTsukubaJapan
  2. 2.Department of BioscienceTokyo University of AgricultureTokyoJapan

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