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Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution

Daniël P Melters, Keith R Bradnam, Hugh A Young and 14 more

Genome Biology · 2013

doi:10.1186/gb-2013-14-1-r10

Abstract

Background. Centromeres are essential for chromosome segregation, yet their DNA sequences evolve rapidly. In most animals and plants that have been studied, centromeres contain megabase-scale arrays of tandem repeats. Despite their importance, very little is known about the degree to which centromere tandem repeats share common properties between different species across different phyla. We used bioinformatic methods to identify high-copy tandem repeats from 282 species using publicly available genomic sequence and our own data.

Results. Our methods are compatible with all current sequencing technologies. Long Pacific Biosciences sequence reads allowed us to find tandem repeat monomers up to 1,419 bp. We assumed that the most abundant tandem repeat is the centromere DNA, which was true for most species whose centromeres have been previously characterized, suggesting this is a general property of genomes. High-copy centromere tandem repeats were found in almost all animal and plant genomes, but repeat monomers were highly variable in sequence composition and length. Furthermore, phylogenetic analysis of sequence homology showed little evidence of sequence conservation beyond approximately 50 million years of divergence. We find that despite an overall lack of sequence conservation, centromere tandem repeats from diverse species showed similar modes of evolution.

Conclusions. While centromere position in most eukaryotes is epigenetically determined, our results indicate that tandem repeats are highly prevalent at centromeres of both animal and plant genomes. This suggests a functional role for such repeats, perhaps in promoting concerted evolution of centromere DNA across chromosomes.

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References 102

  1. 1.

    Stoler S Keith KC Curnick KE Fitzgerald-Hayes M A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis.Genes Dev1995 14573586

    Not in our library10.1101/gad.9.5.573

  2. 2.

    Shang WH Hori T Toyoda A Kato J Popendorf K Sakakibara Y Fujiyama A Fukagawa T Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences.Genome Res2010 1412191228

    Not in our library10.1101/gr.106245.110

  3. 3.
  4. 4.

    Henikoff S Ahmad K Malik HS The centromere paradox: stable inheritance with rapidly evolving DNA.Science2001 1410981102

    Not in our library10.1126/science.1062939

  5. 5.
  6. 6.

    McAinsh AD Tytell JD Sorger PK Structure, function, and regulation of budding yeast kinetochores.Annu Rev Cell Dev Biol2003 14519539

    Not in our library10.1146/annurev.cellbio.19.111301.155607

  7. 7.

    Birchler JA Gao Z Han F A tale of two centromeres--diversity of structure but conservation of function in plants and animals.Funct Integr Genomics2009 14713

    Not in our library10.1007/s10142-008-0104-9

  8. 8.

    Wang G Zhang X Jin W An overview of plant centromeres.J Genet Genomics2009 14529537

    Not in our library10.1016/s1673-8527(08)60144-7

  9. 9.

    Willard HF Centromeres of mammalian chromosomes.Trends Genet1990 14410416

    Not in our library10.1016/0168-9525(90)90302-m

  10. 10.

    Waye JS Durfy SJ Pinkel D Kenwrick S Patterson M Davies KE Willard HF Chromosome-specific alpha satellite DNA from human chromosome 1: hierarchical structure and genomic organization of a polymorphic domain spanning several hundred kilobase pairs of centromeric DNA.Genomics1987 144351

    Not in our library10.1016/0888-7543(87)90103-0

  11. 11.

    Rudd MK Wray GA Willard HF The evolutionary dynamics of alpha-satellite.Genome Res2006 148896

    Not in our library10.1101/gr.3810906

  12. 12.

    Amor DJ Choo KH Neocentromeres: role in human disease, evolution, and centromere study.Am J Hum Genet2002 14695714

    Not in our library10.1086/342730

  13. 13.

    Nasuda S Hudakova S Schubert I Houben A Endo TR Stable barley chromosomes without centromeric repeats.Proc Natl Acad Sci USA2005 1498429847

    Not in our library10.1073/pnas.0504235102

  14. 14.

    Lam AL Boivin CD Bonney CF Rudd MK Sullivan BA Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA.Proc Natl Acad Sci USA2006 1441864191

    Not in our library10.1073/pnas.0507947103

  15. 15.

    Wade CM Giulotto E Sigurdsson S Zoli M Gnerre S Imsland F Lear TL Adelson DL Bailey E Bellone RR Blocker H Distl O Edgar RC Garber M Leeb T Mauceli E MacLeod JN Penedo MC Raison JM Sharpe T Vogel J Andersson L Antczak DF Biagi T Binns MM Chowdhary BP Coleman SJ Della Valle G Fryc S Guerin G Genome sequence, comparative analysis, and population genetics of the domestic horse.Science2009 14865867

    Not in our library10.1126/science.1178158

  16. 16.

    Locke DP Hillier LW Warren WC Worley KC Nazareth LV Muzny DM Yang SP Wang Z Chinwalla AT Minx P Mitreva M Cook L Delehaunty KD Fronick C Schmidt H Fulton LA Fulton RS Nelson JO Magrini V Pohl C Graves TA Markovic C Cree A Dinh HH Hume J Kovar CL Fowler GR Lunter G Meader S Heger A Comparative and demographic analysis of orang-utan genomes.Nature2011 14529533

    Not in our library10.1038/nature09687

  17. 17.

    Marshall OJ Chueh AC Wong LH Choo KH Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution.Am J Hum Genet2008 14261282

    Not in our library10.1016/j.ajhg.2007.11.009

  18. 18.
  19. 19.

    Gong Z Wu Y Koblízková A Torres GA Wang K Iovene M Neumann P Zhang W Novák P Buell CR Macas J Jiang J Repeatless and repeat-based centromeres in potato: implications for centromere evolution.Plant Cell2012 1435593574

    Not in our library10.1105/tpc.112.100511

  20. 20.

    Dernburg AF Here, there, and everywhere: kinetochore function on holocentric chromosomes.J Cell Biol2001 14F33F38

    Not in our library10.1083/jcb.153.6.f33

  21. 21.

    Gassmann R Rechtsteiner A Yuen KW Muroyama A Egelhofer T Gaydos L Barron F Maddox P Essex A Monen J Ercan S Lieb JD Oegema K Strome S Desai A An inverse relationship to germline transcription defines centromeric chromatin in C. elegans.Nature2012 14534537

    Not in our library10.1038/nature10973

  22. 22.

    Elder JF Turner BJ Concerted evolution at the population level: pupfish HindIII satellite DNA sequences.Proc Natl Acad Sci USA1994 14994998

    Not in our library10.1073/pnas.91.3.994

  23. 23.

    Palomeque T Lorite P Satellite DNA in insects: a review.Heredity (Edinb)2008 14564573

    Not in our library10.1038/hdy.2008.24

  24. 24.

    Masumoto H Nakano M Ohzeki J The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres.Chromosome Res2004 14543556

    Not in our library10.1023/b:chro.0000036593.72788.99

  25. 25.

    Bensasson D Zarowiecki M Burt A Koufopanou V Rapid evolution of yeast centromeres in the absence of drive.Genetics2008 1421612167

    Not in our library10.1534/genetics.107.083980

  26. 26.
  27. 27.

    Plohl M Luchetti A Mestrović N Mantovani B Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin.Gene2008 147282

    Not in our library10.1016/j.gene.2007.11.013

  28. 28.

    Gaillard C Doly J Cortadas J Bernardi G The primary structure of bovine satellite 1.715.Nucleic Acids Res1981 1460696082

    Not in our library10.1093/nar/9.22.6069

  29. 29.

    Płucienniczak A Skowroński J Jaworski J Nucleotide sequence of bovine 1.715 satellite DNA and its relation to other bovine satellite sequences.J Mol Biol1982 14293304

    Not in our library10.1016/0022-2836(82)90434-x

  30. 30.

    Taparowsky EJ Gerbi SA Structure of 1.71 lb gm/cm(3) bovine satellite DNA: evolutionary relationship to satellite I.Nucleic Acids Res1982 1455035515

    Not in our library10.1093/nar/10.18.5503

  31. 31.

    Fishman L Saunders A Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers.Science2008 1415591562

    Not in our library10.1126/science.1161406

  32. 32.

    BLASTnhttp://blast.ncbi.nlm.nih.gov

    Not in our library

  33. 33.

    Alkan C Cardone MF Catacchio CR Antonacci F O'Brien SJ Ryder OA Purgato S Zoli M Della Valle G Eichler EE Ventura M Genome-wide characterization of centromeric satellites from multiple mammalian genomes.Genome Res2011 14137145

    Not in our library10.1101/gr.111278.110

  34. 34.
  35. 35.

    Schnable PS Ware D Fulton RS Stein JC Wei F Pasternak S Liang C Zhang J Fulton L Graves TA Minx P Reily AD Courtney L Kruchowski SS Tomlinson C Strong C Delehaunty K Fronick C Courtney B Rock SM Belter E Du F Kim K Abbott RM Cotton M Levy A Marchetto P Ochoa K Jackson SM Gillam B The B73 maize genome: complexity, diversity, and dynamics.Science2009 1411121115

    Not in our library10.1126/science.1178534

  36. 36.

    Ananiev EV Phillips RL Rines HW Complex structure of knobs and centromeric regions in maize chromosomes.Tsitol Genet2000 141115

    Not in our library

  37. 37.

    Dawe RK Bennetzen JL Hake S Maize Centromeres and Knobs (neocentromeres) Handbook of Maize2009 New York: Springer239250

    Not in our library

  38. 38.

    Chia JM Song C Bradbury P Costich D de Leon N Doebley JC Elshire RJ Gaunt BS Geller L Glaubitz JC Gore M Guill KE Holland J Hufford MB Lai J Liu X Lu Y McCombie R Nelson R Poland J Prasanna BM Pyhäjärvi T Rong T Shekhon RS Sun Q Tenaillon M Tian F Wang J Xu X Zhang Z Kaeppler S Ross-Ibarra J McMullen M Buckler ES Zhang G Xu Y Ware D Capturing extant variation from a genome in flux: maize HapMap II.Nat Genet2012 14803807

    Not in our library10.1038/ng.2313

  39. 39.

    Carone DM Longo MS Ferreri GC Hall L Harris M Shook N Bulazel KV Carone BR Obergfell C O'Neill MJ O'Neill RJ A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres.Chromosoma2009 14113125

    Not in our library10.1007/s00412-008-0181-5

  40. 40.

    Hosouchi T Kumekawa N Tsuruoka H Kotani H Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3.DNA Res2002 14117121

    Not in our library10.1093/dnares/9.4.117

All 102 references

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