Abstract
Brachypodium distachyon is a wild annual grass belonging to the Pooideae, more closely related to wheat, barley, and forage grasses than rice and maize. As an experimental model, the completed genome sequence of B. distachyon provides a unique opportunity to study centromere evolution during the speciation of grasses. Centromeric satellite sequences have been identified in B. distachyon, but little is known about centromeric retrotransposons in this species. In the present study, bacterial artificial chromosome (BAC)-fluorescence in situ hybridization was conducted in maize, rice, barley, wheat, and rye using B. distachyon (Bd) centromere-specific BAC clones. Eight Bd centromeric BAC clones gave no detectable fluorescence in situ hybridization (FISH) signals on the chromosomes of rice and maize, and three of them also did not yield any FISH signals in barley, wheat, and rye. In addition, four of five Triticeae centromeric BAC clones did not hybridize to the B. distachyon centromeres, implying certain unique features of Brachypodium centromeres. Analysis of Brachypodium centromeric BAC sequences identified a long terminal repeat (LTR)-centromere retrotransposon of B. distachyon (CRBd1). This element was found in high copy number accounting for 1.6 % of the B. distachyon genome, and is enriched in Brachypodium centromeric regions. CRBd1 accumulated in active centromeres, but was lost from inactive ones. The LTR of CRBd1 appears to be specific to B. distachyon centromeres. These results reveal different evolutionary events of this retrotransposon family across grass species.
Similar content being viewed by others
Abbreviations
- BAC:
-
Bacterial artificial chromosome
- Bd_CENT:
-
Brachypodium distachyon centromeric repeat
- CCD:
-
Charge-coupled device
- CENH3:
-
Centromere-specific histone H3
- CR:
-
Centromeric retrotransposon
- CRBd:
-
Centromeric retrotransposon of B. distachyon
- CRM:
-
Centromeric retrotransposon of maize
- CRR:
-
Centromeric retrotransposon of rice
- CRW:
-
Centromeric retrotransposon of wheat
- EST:
-
Expressed sequence tag
- FISH:
-
Fluorescence in situ hybridization
- LTR:
-
Long terminal repeat
- MYA:
-
Million years ago
- PBS:
-
Primer-binding site
- PPT:
-
Polypurine tract
- REBd:
-
Retrotransposon element of B. distachyon
- TSD:
-
Target site duplication
- TREP:
-
Triticeae Repeat Sequence Database
References
Abbo S, Dunford RP, Foote T, Reader SM, Flavell RB, Moore G (1995) Organization of retroelement and stem-loop repeat families in the genomes and nuclei of cereals. Chromosome Res 3:5–15
Ananiev EV, Phillips RL, Rines HW (1998) Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA 95:13073–13078
Aragón-Alcaide L, Miller T, Schwatzacher T, Reader S, Moore G (1996) A cereal centromeric sequence. Chromosoma 105:261–268
Bolot S, Abrouk M, Masood-Quraishi U, Stein N, Messing J, Feuillet C, Salse J (2009) The ‘inner circle’ of the cereal genomes. Curr Opin Plant Bio 12:119–125
Buchmann JP, Matsumoto T, Stein N, Keller B, Wicker T (2012) Inter-species sequence comparison of Brachypodium reveals how transposon activity corrodes genome colinearity. Plant J 71:550–556
Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR, Gu MH, Blattner FR, Jiang J (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704
Choulet F, Wicker T, Rustenholz C et al (2010) Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:1686–1701
Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S et al (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468–2474
Dong F, Miller T, Jacson SA, Wang GL, Ronald PC, Jinag J (1998) Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc Natl Acad Sci USA 95:8135–8140
Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, Shoemaker RC, Ma J (2010) Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J 63:584–598
Francki MG (2001) Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.). Genome 44:266–274
Gao D, Gill N, Kim HR, Walling JG, Zhang W, Fan C, Yu Y, Ma J, SanMigue P, Jiang N et al (2009) A lineage-specific centromere retrotransposon in Oryza brachyantha. Plant J 60:820–831
Hall SE, Kettler G, Preuss D (2003) Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res 13:195–205
Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 203:1098–1102
Hudakova S, Michalek W, Presting GG, Ten Hoopen R, Dos Santos K, Jasencakova Z, Schubert I (2001) Sequence organization of barley centromeres. Nucleic Acids Res 29:5029–5035
Huo N, Gu YQ, Lazo GR, Vogel JP, Coleman-Derr D, Luo MC, Thilmony R, Garvin DF, Anderson OD (2006) Construction and characterization of two BAC libraries from Brachypodium distachyon, a new model for grass genomics. Genome 49:1099–1108
Jiang J, Nasuda S, Dong F, Scherrer CW, Woo SS, Wing RA, Gill BS, Ward DC (1996) A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci USA 93:14210–14213
Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575
Jin WW, Melo JR, Nagaki K, Talbert PB, Henikoff S, Dawe RK, Jiang J (2004) Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16:571–581
Jin WW, Lamb JC, Vega JM, Dawe RK, Birchler JA, Jiang J (2005) Molecular and functional dissection of the maize B chromosome centromere. Plant Cell 17:1412–1423
Kulikova O, Geurts R, Lamine M et al (2004) Satellite repeats in the functional centromere and pericentromeric heterochromatin of Medicago truncatula. Chromosoma 113:276–283
Kumekawa N, Ohtsubo E, Ohtsubo H (1999) Identification and phylogenetic analysis of gypsy-type retrotransposons in the plant kingdom. Genes Genet Syst 74:299–307
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
Lamb JC, Yu W, Han F, Birchler JA (2008) Plant centromeres. Genome Dyn 4:95–107
Lee HR, Zhang W, Langdon T, Jin WW, 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
Li B, Choulet F, Heng Y et al (2013) Wheat centromeric retrotransposons: the new ones take a major role in centromeric structure. Plant J 73:952–965
Lim K-B, Yang T-J, Hwang Y-J et al (2007) Characterization of the centromere and peri-centromere retrotransposons in Brassica rapa and their distribution in related Brassica species. Plant J 49:173–183
Liu Z, Yue W, Li D et al (2008) Structure and dynamics of retrotransposons at wheat centromeres and pericentromeres. Chromosoma 117:445–456
Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410
Ma J, Wing R, Bennetzen JL, Jackson SA (2007) Evolutionary history and positional shift of a rice centromere. Genetics 177:1217–1220
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
Nagaki K, Song J, Stupar RM et al (2003a) Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics 163:759–770
Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J (2003b) Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163:1221–1225
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
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
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
Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21(Suppl 1):i351–i358
Qi LL, Friebe B, Zhang P, Gill BS (2009) A molecular-cytogenetic method for locating genes to pericentromeric regions facilitates a genome-wide comparison of synteny between the centromeric regions of wheat and rice. Genetics 183:1235–1247
Qi LL, Friebe B, Wu J, Gu Y, Qian C, Gill BS (2010) The compact Brachypodium genome conserves centromeric regions of a common ancestor with wheat and rice. Funct Integr Genomics 10:477–492
Round EK, Flowers SK, Richards EJ (1997) Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res 91:1007–1019
Šafář J, Bartoš J, Janda J et al (2004) Dissecting large and complex genomes: flow sorting and BAC cloning of individual chromosomes from bread wheat. Plant J 39:960–968
Sharma A, Presting GG (2008) Centromeric retrotransposon lineages predate the maize/rice divergence and differ in abundance and activity. Mol Genet Genomics 279:133–147
Tek AL, Kashihara K, Murata M, Nagaki K (2010) Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon. Chromosome Res 18:337–347
The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nuture 463:763–768
Weber B, Schmidt T (2009) Nested Ty3-gypsy retrotransposons of a single Betaprocumbens centromere contain a putative chromodomain. Chromsome Res 17:379–396
Wen R, Moore G, Shaw PJ (2012) Centromeres cluster de novo at the beginning of meiosis in Brachypodium distachyon. PLoS One 7:e44681
Wu J, Fujisawa M, Tian Z 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
Zhang P, Li WL, Fellers J, Friebe B, Gill BS (2004a) BAC-FISH in wheat identifies chromosome landmarks consisting of different types of transposable elements. Chromosoma 112:288–299
Zhang Y, Huang Y, Zhang L et al (2004b) Structural features of the rice chromosome 4 centromere. Nucleic Acids Res 32:2023–2030
Zhao X, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35(Web Server issue):W265–W268
Zhong CX, Marshall JB, Topp C et al (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836
Acknowledgments
We thank Drs Zhao Liu and Gerald Seiler for critical review of the manuscript. This research was supported by a special USDA-NIFA grant to the Wheat Genetic Resources Center, Kansas State University, USA, and fund for excellent young scholar of Shandong Province of China (BS2011SW027).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Hans de Jong
L.L. Qi and J.J Wu contributed equally to this work
Rights and permissions
About this article
Cite this article
Qi, L.L., Wu, J.J., Friebe, B. et al. Sequence organization and evolutionary dynamics of Brachypodium-specific centromere retrotransposons. Chromosome Res 21, 507–521 (2013). https://doi.org/10.1007/s10577-013-9378-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-013-9378-4