Molecular Genetics and Genomics

, Volume 279, Issue 2, pp 133–147 | Cite as

Centromeric retrotransposon lineages predate the maize/rice divergence and differ in abundance and activity

Original Paper

Abstract

Centromeric retrotransposons (CR) are located almost exclusively at the centromeres of plant chromosomes. Analysis of the emerging Zea mays inbred B73 genome sequence revealed two novel subfamilies of CR elements of maize (CRM), bringing the total number of known CRM subfamilies to four. Orthologous subfamilies of each of these CRM subfamilies were discovered in the rice lineage, and the orthologous relationships were demonstrated with extensive phylogenetic analyses. The much higher number of CRs in maize versus Oryza sativa is due primarily to the recent expansion of the CRM1 subfamily in maize. At least one incomplete copy of a CRM1 homolog was found in O. sativa ssp. indica and O. officinalis, but no member of this subfamily could be detected in the finished O. sativa ssp. japonica genome, implying loss of this prolific subfamily in that subspecies. CRM2 and CRM3, as well as the corresponding rice subfamilies, have been recently active but are present in low numbers. CRM3 is a full-length element related to the non-autonomous CentA, which is the first described CRM. The oldest subfamily (CRM4), as well as its rice counterpart, appears to contain only inactive members that are not located in currently active centromeres. The abundance of active CR elements is correlated with chromosome size in the three plant genomes for which high quality genomic sequence is available, and the emerging picture of CR elements is one in which different subfamilies are active at different evolutionary times. We propose a model by which CR elements might influence chromosome and genome size.

Keywords

CentA Centromere Genome expansion 

Abbreviations

CR

Centromeric retrotransposon

LTR

Long terminal repeat

FISH

Fluorescent in situ hybridization

MSA

Multiple sequence alignment

nt

Nucleotide

RT

Reverse transcriptase

TSD

Target site duplication

UTR

Untranslated region

Supplementary material

438_2007_302_MOESM1_ESM.doc (235 kb)
(DOC 235 kb)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedCrossRefGoogle Scholar
  2. Ananiev EV, Phillips RL, Rines HW (1998) Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA 95:13073–13078PubMedCrossRefGoogle Scholar
  3. Aragón-Alcaide L, Miller T, Schwarzacher T, Reader S, Moore G (1996) A cereal centromeric sequence. Chromosoma 105:261–268PubMedGoogle Scholar
  4. 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
  5. Bremer K (2002) Godwanan evolution of the grass alliance of families (Poales). Evolution 56:1374–1387PubMedGoogle Scholar
  6. Buzdin AA (2004) Retroelements and formation of chimeric retrogenes. Cell Mol Life Sci 61:2046–2059PubMedCrossRefGoogle Scholar
  7. 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
  8. Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079PubMedCrossRefGoogle Scholar
  9. Dimmic MW, Rest JS, Mindell DP, Goldstein RA (2002) rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J Mol Evol 55:65–73PubMedCrossRefGoogle Scholar
  10. Felsenstein J (1989) PHYLIP—phylogeny inference package (Version 3.2). Cladistics 5:164–166Google Scholar
  11. Felsenstein J (2005) PHYLIP—Phylogeny Inference Package (Version 3.6). Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  12. Fleischer B, Gindullis F, Dechyeva D, Schmidt T (2002) Beetle1, a Ty3-gypsy-retrotransposon highly amplified at centromeres of Beta procumbens chromosomes. Plant & Animal Genome X, San Diego, USAGoogle Scholar
  13. Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279PubMedCrossRefGoogle Scholar
  14. Gorinsek B, Gubensek F, Kordis D (2004) Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol 21:781–798PubMedCrossRefGoogle Scholar
  15. Gorinsek B, Gubensek F, Kordis D (2005) Phylogenomic analysis of chromoviruses. Cytogenet Genome Res 110:543–552PubMedCrossRefGoogle Scholar
  16. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucl Acids Res 33:W557–W559PubMedCrossRefGoogle Scholar
  17. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  18. 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 93:14210–14213PubMedCrossRefGoogle Scholar
  19. Jin WW, Melo JR, Nagaki K, Talbert PB, Henikoff S, Dawe RK, Jiang JM (2004) Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16:571–581PubMedCrossRefGoogle Scholar
  20. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  21. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532PubMedCrossRefGoogle Scholar
  22. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle 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 H, 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. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659PubMedCrossRefGoogle Scholar
  26. Lim KB, Yang TJ, Hwang YJ, Kim JS, Park JY, Kwon SJ, Kim J, Choi BS, Lim MH, Jin M, Kim HI, de Jong H, Bancroft I, Lim Y, Park BS (2007) Characterization of the centromere and peri-centromere retrotransposons in Brassica rapa and their distribution in related Brassica species. Plant J 49:173–183PubMedCrossRefGoogle Scholar
  27. Luce AC, Sharma A, Mollere OS, Wolfgruber TK, Nagaki K, Jiang J, Presting GG, Dawe RK (2006) Precise centromere mapping using a combination of repeat junction markers and ChIP-PCR. Genetics 174:1057–1061PubMedCrossRefGoogle Scholar
  28. Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869PubMedCrossRefGoogle Scholar
  29. Ma J, Jackson SA (2006) Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. Genome Res 16:251–259PubMedCrossRefGoogle Scholar
  30. Malik HS, Eickbush TH (1999) Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol 73:5186–5190PubMedGoogle Scholar
  31. Malik HS, Eickbush TH (2001) Phylogenetic analysis of riobnuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res 11:1187–1197PubMedCrossRefGoogle Scholar
  32. Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32(W):327–331CrossRefGoogle Scholar
  33. Marin I, Llorens C (2000) Ty3/Gypsy retrotransposons: description of new Arabidopsis thaliana elements and evolutionary perspectives derived from comparative genomic data. Mol Biol Evol 17:1040–1049PubMedGoogle Scholar
  34. May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1:e79PubMedCrossRefGoogle Scholar
  35. McClure MA, Johnson MS, Feng D-F, Doolittle RF (1988) Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci USA 85:2469–2473PubMedCrossRefGoogle Scholar
  36. 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
  37. 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
  38. Nagaki K, Song J, Stupar RM, Parokonny AS, Yuan Q, Ouyang S, Liu J, Hsiao J, Jones KM, Dawe RK, Buell CR, Jiang J (2003a) Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics 163:759–770PubMedGoogle Scholar
  39. 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 163:1221–1225PubMedGoogle Scholar
  40. Nix DA, Eisen MB (2005) GATA: a graphic alignment tool for comparative sequence analysis. BMC Bioinformatics [electronic resource] 6:9CrossRefGoogle Scholar
  41. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  42. Pelissier T, Tutois S, Deragon JM, Tourmente S, Genestier S, Picard G (1995) Athila, a new retroelement from Arabidopsis thaliana. Plant Mol Biol 29:441–452PubMedCrossRefGoogle Scholar
  43. Pelissier T, Tutois S, Tourmente S, Deragon JM, Picard G (1996) DNA regions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences. Genetica 97:141–151PubMedCrossRefGoogle Scholar
  44. 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
  45. 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
  46. Sabot F, Schulman AH (2007) Template switching can create complex LTR retrotransposon insertions in the Triticeae genomes. BMC Genomics 8:247 doi:10.1186/1471–2164/8/247 PubMedCrossRefGoogle Scholar
  47. SanMiguel P, Gaut B, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45PubMedCrossRefGoogle Scholar
  48. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  49. Topp CN, Zhong CX, Dawe RK (2004) Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci USA 101:15986–15991PubMedCrossRefGoogle Scholar
  50. Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:1769–1784PubMedCrossRefGoogle Scholar
  51. Vicient CM, Kalendar R, Schulman AH (2005) Variability, recombination, and mosaic evolution of the barley BARE-1 retrotransposon. J Mol Evol 61:275–91PubMedCrossRefGoogle Scholar
  52. Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotranpsosons in rice Oryza sativa L. Mol Biol Evol 20:528–540PubMedCrossRefGoogle Scholar
  53. Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond B 268:2211–2220CrossRefGoogle Scholar
  54. Wilson R, Wing R, McCombie WR, Martienssen R, Ware D, Stein L, Clifton S, Minx P, Robert F, Schnable P (2006) Sequencing the maize genome. 48th Annual Maize Genetics Conference, Asilomar Conference Grounds, Pacific Grove, California, USAGoogle Scholar
  55. 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
  56. Zmasek CM, Eddy SR (2001) ATV: display and manipulation of annotated phylogenetic trees. Bioinformatics 17:383–384PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Molecular Biosciences and BioengineeringUniversity of HawaiiHonoluluUSA

Personalised recommendations