Skip to main content
SpringerLink
Log in

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

  • Published:
Tropical Plant Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  • 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):140–147

    Article  PubMed  Google Scholar 

  • 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 52:342–351

    Article  PubMed  CAS  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 20:3191–209

    Article  PubMed  CAS  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 Genomics 275:421–430

    Article  PubMed  CAS  Google Scholar 

  • 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 299:1391–1394

    Article  PubMed  CAS  Google Scholar 

  • 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 286:2468–2474

    Article  PubMed  CAS  Google Scholar 

  • 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 14:1691–1704

    Article  PubMed  CAS  Google Scholar 

  • 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 161:1713–1726

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • 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 101:1001–1007

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28

    Article  CAS  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

    Google Scholar 

  • 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 296:92–100

    Article  PubMed  CAS  Google Scholar 

  • 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 100:367–376

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • 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 7:199

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 166:1437–1450

    Article  PubMed  CAS  Google Scholar 

  • 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:R45

    Article  PubMed  Google Scholar 

  • 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 265:480–488

    Article  PubMed  CAS  Google Scholar 

  • Langdon T, Seago C, Mende M, Leggett M, Thomas H, Forster JW, Jones RN, Jenkins G (2000) Retrotransposon evolution in diverse plant genomes. Genetics 156:313–325

    PubMed  CAS  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 USA 102:11793–11798

    Article  PubMed  CAS  Google Scholar 

  • 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 117:445–456

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci SA 101:12404–12410

    Article  CAS  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

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • 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 22:845–855

    Article  PubMed  CAS  Google Scholar 

  • 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 16:1262–1269

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Qian W, Ge S, Hong DY (2001) Genetic variation within and among populations of a wild rice Oryza granulate. Theor Appl Genet 102:440–449

    Article  CAS  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  PubMed  CAS  Google Scholar 

  • 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 27:2487–2506

    Article  PubMed  CAS  Google Scholar 

  • Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115

    Article  PubMed  CAS  Google Scholar 

  • 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 21:5269–5280

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vaughan DA, Kadowaki K, Kaga A, Tommoka N (2005) On the phylogeny biogeographyof the genus Oryza. Breeding Science 55:113–122

    Article  CAS  Google Scholar 

  • Vitte C, Panaud O, Quesneville H (2007) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8:218–232

    Article  PubMed  Google Scholar 

  • Wu J et al (2004) Composition and structure of the centromeric region of rice chromosome 8. Plant Cell 16:967–976

    Article  PubMed  CAS  Google Scholar 

  • 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 60:805–819

    Article  PubMed  CAS  Google Scholar 

  • Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265–268

    Article  PubMed  Google Scholar 

  • 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 18:2123–33

    Article  PubMed  CAS  Google Scholar 

  • 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 296:79–92

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. Center for Applied Genetic Technologies and Institute for Plant Breeding Genetics and Genomics, University of Georgia, 111 Riverbend Rd., Athens, GA, 30602, USA

    Dongying Gao & Scott A. Jackson

  2. Department of Horticulture, University of Wisconsin-Madison, 1575 Linden Drive, Madison, WI, 53706, USA

    Zhiyun Gong & Jiming Jiang

  3. Arizona Genome Institute, Department of Plant Sciences, University of Arizona, 1657 E. Helen Street, Tucson, AZ, 85721, USA

    Rod A. Wing

Authors
  1. Dongying Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhiyun Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rod A. Wing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiming Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Scott A. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott A. Jackson.

Additional information

Communicated by James Birchler

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gao, D., Gong, Z., Wing, R.A. et al. Molecular and Cytological Characterization of Centromeric Retrotransposons in a Wild Relative of Rice, Oryza granulata . Tropical Plant Biol. 4, 217–227 (2011). https://doi.org/10.1007/s12042-011-9083-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-011-9083-4

Keywords

Search

Navigation