Tropical Plant Biology

, Volume 4, Issue 3–4, pp 217–227 | Cite as

Molecular and Cytological Characterization of Centromeric Retrotransposons in a Wild Relative of Rice, Oryza granulata

  • Dongying Gao
  • Zhiyun Gong
  • Rod A. Wing
  • Jiming Jiang
  • Scott A. JacksonEmail author


Centromeric retrotransposons (CRs) are important component of the functional centromeres of rice chromosomes. To track the evolution of the CR elements in genus Oryza, we sequenced the orthologous region of the rice centromere 8 (Cen8) in O. granulata and analyzed transposons in this region. A total of 12 bacterial artificial chromosomes (BACs) that span the centromeric region in O. granulata were sequenced. The O. granulate centromeric sequences are composed of as much as 85% of transposons, higher than any other reported eukaryotic centromeres. Ten novel LTR retrotransposon families were identified but a single retrotransposon, Gran3, constitutes nearly 43% of the centromeric sequences. Integration times of complete LTR retrotransposons indicate that the centromeric region had a massive insertion of LTR retrotransposons within 4.5 million year (Myr), which indicates a recent expansion of the centromere in O. granulata after the radiation of the Oryza genus. Two retrotransposon families, OGRetro7 and OGRetro9, show sequence similarity with the canonical CRs from rice and maize. Both OGRetro7 and OGRetro9 are highly concentrated in the centromeres of O. granulata chromosomes. Furthermore, strong hybridization signals were detected in all Oryza species but in O. brachyantha with the OGRetro7 and OGRetro9 probes. Characterization of the centromeric retrotransposons in O. granulata confirms the conservation of the CRs in the Oryza genus and provides a resource for comparative analysis of centromeres and centromere evolution among the Oryza genus and other genomes.


Centromere 8 Evolution Centromeric retrotransposon Oryza granulata Comparative genomics 



We thank Dr. Ning Jiang for providing us the unpublished rice transposon database. This research was founded by the National Science Foundation DBI 0603927 (JJ, SAJ and RAW) and 0424833 (SAJ).


  1. Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937PubMedCrossRefGoogle Scholar
  2. Ammiraju JS et al (2006) The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza. Genome Res 16(1):140–147PubMedCrossRefGoogle Scholar
  3. Ammiraju JS, Zuccolo A, Yu Y, Song X, Piegu B, Chevalier F, Walling JG, Ma J, Talag J, Brar DS, SanMiguel PJ, Jiang N, Jackson SA, Panaud O, Wing RA (2007) Evolutionary dynamics of an ancient retrotransposon family provides insights into evolution of genome size in the genus Oryza. Plant J 52:342–351PubMedCrossRefGoogle Scholar
  4. 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 20:3191–209PubMedCrossRefGoogle Scholar
  5. 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 Genomics 275:421–430PubMedCrossRefGoogle Scholar
  6. Boffelli D, McAuliffe J, Ovcharenko D, Lewis KD, Ovcharenko I, Pachter L, Rubin EM (2003) Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299:1391–1394PubMedCrossRefGoogle Scholar
  7. Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD, McCombie WR, Martienssen RA, Marra M, Preuss D (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468–2474PubMedCrossRefGoogle Scholar
  8. 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 14:1691–1704PubMedCrossRefGoogle Scholar
  9. Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002) Conservation of gene function in the solanaceae as revealed by comparative mapping of domestication traits in eggplant. Genetics 161:1713–1726PubMedGoogle Scholar
  10. 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 95:8135–8140PubMedCrossRefGoogle Scholar
  11. Dong F, Song J, Naess K, Helgeson JP, Gebhardt C, Jiang JM (2000) Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor Appl Genet 101:1001–1007CrossRefGoogle Scholar
  12. 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 60:820–831PubMedCrossRefGoogle Scholar
  13. Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28CrossRefGoogle Scholar
  14. 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 96:14400–14405Google Scholar
  15. Goff SA, Ricke D, Lan TH, Presting G, Wang R et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  16. Fransz PF, Armstrong S, de Jong JH, Parnell LD, van Drunen C, Dean C, Zabel P, Bisseling T, Jones GH (2000) Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100:367–376PubMedCrossRefGoogle Scholar
  17. Hall AE, Keith KC, Hall SE, Copenhaver GP, Preuss D (2004) The rapidly evolving field of plant centromeres. Curr Opin Plant Biol 7:108–114PubMedCrossRefGoogle Scholar
  18. Hass-Jacobus BL et al (2006) Integration of hybridization-based markers (overgos) into physical maps for comparative and evolutionary explorations in the genus Oryza and in Sorghum. BMC Genomics 7:199PubMedCrossRefGoogle Scholar
  19. Jiang J, Birchler JA, Parrott WA, Daw RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575PubMedCrossRefGoogle Scholar
  20. Kalendar R, Vicient CM, Peleg O, Anamthawat-Jonsson K, Bolshoy A, Schulman AH (2004) Large retrotransposon derivatives: abundant, conserved but nonautonomous retroelements of barley and related genomes. Genetics 166:1437–1450PubMedCrossRefGoogle Scholar
  21. Kim H, Hurwitz B, Yu Y, Collura K, Gill N, SanMiguel P, Mullikin JC, Maher C, Nelson W, Wissotski M, Braidotti M, Kudrna D, Goicoechea JL, Stein L, Ware D, Jackson SA, Soderlund C, Wing RA (2008) Construction, alignment and analysis of twelve framework physical maps that represent the ten genome types of the genus Oryza. Genome Biol 9:R45PubMedCrossRefGoogle Scholar
  22. Kumekawa N, Ohmido N, Fukui K, Ohtsubo E, Ohtsubo H (2001) A new gypsy-type retrotransposon, RIRE7: preferential insertion into the tandem repeat sequence TrsD in pericentromeric heterochromatin regions of rice chromosomes. Mol Genet Genomics 265:480–488PubMedCrossRefGoogle Scholar
  23. Langdon T, Seago C, Mende M, Leggett M, Thomas H, Forster JW, Jones RN, Jenkins G (2000) Retrotransposon evolution in diverse plant genomes. Genetics 156:313–325PubMedGoogle Scholar
  24. 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 USA 102:11793–11798PubMedCrossRefGoogle Scholar
  25. Liu Z, Yue W, Li D, Wang RR, Kong X, Lu K, Wang G, Dong Y, Jin W, Zhang X (2008) Structure and dynamics of retrotransposons at wheat centromeres and pericentromeres. Chromosoma 117:445–456PubMedCrossRefGoogle Scholar
  26. 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 106:2071–2076PubMedCrossRefGoogle Scholar
  27. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci SA 101:12404–12410CrossRefGoogle Scholar
  28. Miller JT, Dong F, Jackson SA, Song J, Jiang J (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150:1615–1623PubMedGoogle Scholar
  29. 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 36:138–145PubMedCrossRefGoogle Scholar
  30. 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 22:845–855PubMedCrossRefGoogle Scholar
  31. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269PubMedCrossRefGoogle Scholar
  32. 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 16:721–728PubMedCrossRefGoogle Scholar
  33. Qian W, Ge S, Hong DY (2001) Genetic variation within and among populations of a wild rice Oryza granulate. Theor Appl Genet 102:440–449CrossRefGoogle Scholar
  34. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45PubMedCrossRefGoogle Scholar
  35. Sanyal A, Ammiraju JS, Lu F, Yu Y, Rambo T, Currie J, Kollura K, Kim HR, Chen J, Ma J, San Miguel P, Mingsheng C, Wing RA, Jackson SA (2010) Orthologous comparisons of the Hd1 region across genera reveal Hd1 gene lability within diploid Oryza species and disruptions to microsynteny in Sorghum. Mol Biol Evol 27:2487–2506PubMedCrossRefGoogle Scholar
  36. Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115PubMedCrossRefGoogle Scholar
  37. Spence JM, Critcher R, Ebersole TA, Valdivia MM, Earnshaw WC, Fukagawa T, Farr CJ (2002) Co-localization of centromere activity, proteins and topoisomerase II within a subdomain of the major human X alpha-satellite array. EMBO J 21:5269–5280PubMedCrossRefGoogle Scholar
  38. Vaughan DA, Morishima H (2003) Kadowaki K (2003) Diversity in the Oryza genus. Curr Opin Plant Biol 6:139–146PubMedCrossRefGoogle Scholar
  39. Vaughan DA, Kadowaki K, Kaga A, Tommoka N (2005) On the phylogeny biogeographyof the genus Oryza. Breeding Science 55:113–122CrossRefGoogle Scholar
  40. Vitte C, Panaud O, Quesneville H (2007) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8:218–232PubMedCrossRefGoogle Scholar
  41. Wu J et al (2004) Composition and structure of the centromeric region of rice chromosome 8. Plant Cell 16:967–976PubMedCrossRefGoogle Scholar
  42. Wu J et al (2009) Comparative analysis of complete orthologous centromeres from two subspecies of rice reveals rapid variation of centromere organization and structure. Plant J 60:805–819PubMedCrossRefGoogle Scholar
  43. Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265–268PubMedCrossRefGoogle Scholar
  44. Yan H, Ito H, Nobuta K, Ouyang S, Jin W, Tian S, Lu C, Venu RC, Wang GL, Green PJ, Wing RA, Buell CR, Meyers BC (2006) Jiang J (2006) Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere. Plant Cell 18:2123–33PubMedCrossRefGoogle Scholar
  45. Yu J, Hu S, Wang J, Wong GK, Li S et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92PubMedCrossRefGoogle Scholar
  46. 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 14:2825–2836PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Dongying Gao
    • 1
  • Zhiyun Gong
    • 2
  • Rod A. Wing
    • 3
  • Jiming Jiang
    • 2
  • Scott A. Jackson
    • 1
    Email author
  1. 1.Center for Applied Genetic Technologies and Institute for Plant Breeding Genetics and GenomicsUniversity of GeorgiaAthensUSA
  2. 2.Department of HorticultureUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Arizona Genome Institute, Department of Plant SciencesUniversity of ArizonaTucsonUSA

Personalised recommendations