, Volume 127, Issue 1, pp 73–83 | Cite as

New high copy tandem repeat in the content of the chicken W chromosome

  • Aleksey S. Komissarov
  • Svetlana A. Galkina
  • Elena I. Koshel
  • Maria M. Kulak
  • Aleksander G. Dyomin
  • Stephen J. O’Brien
  • Elena R. Gaginskaya
  • Alsu F. Saifitdinova
Original Article


The content of repetitive DNA in avian genomes is considerably less than in other investigated vertebrates. The first descriptions of tandem repeats were based on the results of routine biochemical and molecular biological experiments. Both satellite DNA and interspersed repetitive elements were annotated using library-based approach and de novo repeat identification in assembled genome. The development of deep-sequencing methods provides datasets of high quality without preassembly allowing one to annotate repetitive elements from unassembled part of genomes. In this work, we search the chicken assembly and annotate high copy number tandem repeats from unassembled short raw reads. Tandem repeat (GGAAA)n has been identified and found to be the second after telomeric repeat (TTAGGG)n most abundant in the chicken genome. Furthermore, (GGAAA)n repeat forms expanded arrays on the both arms of the chicken W chromosome. Our results highlight the complexity of repetitive sequences and update data about organization of sex W chromosome in chicken.


Satellite DNA Raw reads analysis Kmer analysis Tandem repeats Gallus gallus Domesticus Lampbrush chromosomes 



Council for International Organizations of Medical Sciences


Chicken repeat 1




Gallus_gallus-4.0 assembly of the chicken genome (GCA_000002315.2)


Gallus_gallus-5.0 assembly of the chicken genome (GCA_000002315.3)


Billions of base pairs


International Chicken Genome Sequencing Consortium


Long interspersed element


Long terminal repeat


Millions of base pairs


Nucleolus organizer region


Short interspersed element


Sodium salt citrate


Tandem repeat finder



We are grateful to the anonymous Reviewers for their very useful comments and suggestions. The authors acknowledge Dr. Irina Solovei for providing plasmids pUGD0600 and pUGD1202. We would like to thank Dr. Denis Bogomaz for his assistance in oligonucleotide synthesis and Dr. Inna Kuznetsova for her fruitful discussion. This work was supported by the grant from Russian Foundation for Basic Research (16-04-01823). Aleksey Komissarov and Stephen O’Brien are financially supported by Russian Science Foundation (17-14-01138). The postdoctoral fellowship from St. Petersburg State University was provided for Elena I. Koshel (1.50.1043.2014). The equipment and software of Chromas Research Resource Center and Theodosius Dobzhansky Centre for Genome Bioinformatics of Saint Petersburg State University were used.


This study was funded by the grant from Russian Foundation for Basic Research (16–04-01823).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest regarding the publication of this paper.

Animal rights statement

All procedures performed in studies involving animals were in accordance with International Guiding Principles for Biomedical Research Involving Animals established by Council for International Organizations of Medical Sciences (CIOMS) and approved by Saint-Petersburg State University Ethics Committee (statement # 131–03-2).


  1. Abrusán G, Krambeck HJ, Junier T, Giordano J, Warburton PE (2008) Biased distributions and decay of long interspersed nuclear elements in the chicken genome. Genetics 178(1):573–581. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arthur RR, Straus NA (1978) DNA-sequence organization in the genome of the domestic chicken (Gallus domesticus). Can J Biochem 56:257–263CrossRefGoogle Scholar
  3. Bellott DW, Skaletsky H, Cho TJ, Brown L, Locke D, Chen N, Galkina S, Pyntikova T, Koutseva N, Graves T, Kremitzki C, Warren WC, Clark AG, Gaginskaya E, Wilson RK, Page DC (2017) Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators. Nat Genet 49(3):387–394CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bellott DW, Skaletsky H, Pyntikova T, Mardis ER, Graves T, Kremitzki C, Brown LG, Rozen S, Warren WC, Wilson RK, Page DC (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466:612–613CrossRefPubMedPubMedCentralGoogle Scholar
  5. Belotserkovskii BP, Veselkov AG, Filippov SA, Dobrynin VN, Mirkin SM, Frank-Kamenetskii MD (1990) Formation of intramolecular triplex in homopurine-homopyrimidine mirror repeats with point substitutions. Nucleic Acids Res 18:6621–6624CrossRefPubMedPubMedCentralGoogle Scholar
  6. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beridze T (1986) Satellite DNA. In: Beridze (ed). Published by Springer-Verlag, 1986. Hardcover. Berlin, Heidelberg, New York, London: Springer VerlagGoogle Scholar
  8. Berlin S, Ellegren H (2004) Chicken W: a genetically uniform chromosome in a highly variable genome. Proc Natl Acad Sci U S A 101(45):15967–15969CrossRefPubMedPubMedCentralGoogle Scholar
  9. Biltueva LS, Prokopov DY, Makunin AI, Komissarov AS, Kudryavtseva AV, Lemskaya NA, Vorobieva NV, Serdyukova NA, Romanenko SA, Gladkikh OL, Graphodatsky AS (2017) Genomic organization and physical mapping of Tandemly arranged repetitive DNAs in Sterlet (Acipenser Ruthenus). Cytogenet Genome Res.
  10. Biscotti MA, Olmo E, Heslop-Harrison JS (2015) Repetitive DNA in eukaryotic genomes. Chromosom Res 23(3):415–420. CrossRefGoogle Scholar
  11. Burt DW (2002) Origin and evolution of avian microchromosomes. Cytogenet Genome Res 96:97–112CrossRefPubMedGoogle Scholar
  12. Burt DW (2005) Chicken genome: current status and future opportunities. Genome Res 15:1692–1698CrossRefPubMedGoogle Scholar
  13. Callan HG (1986) Lampbrush chromosomes. Mol Biol Biochem Biophys 36:1–252CrossRefPubMedGoogle Scholar
  14. Chen N, Bellott DW, Page DC, Clark AG (2012) Identification of avian W-linked contigs by short-read sequencing. BMC Genomics 13:183. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cheng YK, Pettitt BM (1992) Stabilities of double- and triple-strand helical nucleic acids. Prog Biophys Mol Biol 58(3):225–257CrossRefPubMedGoogle Scholar
  16. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grützner F, Kaessmann H (2014) Origins and functional evolution of Y chromosomes across mammals. Nature 508:488–493CrossRefPubMedGoogle Scholar
  17. Cui J, Zhao W, Huang Z, Jarvis ED, Gilbert MTP, Walker PJ, Holmes EC, Zhang G (2014) Low frequency of paleoviral infiltration across the avian phylogeny. Genome Biol 15:539 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cunningham F, Amode MR, Barrell D et al (2015) Ensembl 2015. Nucleic Acids Res 43(Database issue):D662–D669. CrossRefPubMedGoogle Scholar
  19. Delany ME, Daniels LM, Swanberg SE, Taylor HA (2003) Telomeres in the chicken: genome stability and chromosome ends. Poult Sci 82:917–926CrossRefPubMedGoogle Scholar
  20. Deryusheva S, Krasikova A, Kulikova T, Gaginskaya E (2007) Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription analysis on lampbrush chromosomes. Chromosoma 116:519–530CrossRefPubMedGoogle Scholar
  21. Dobrynin P, Liu S, Tamazian G et al (2015) Genomic legacy of the African cheetah, Acinonyx jubatus. Genome Biol 16:277. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Enukashvily NI, Ponomartsev NV (2013) Mammalian satellite DNA: a speaking dumb. Adv Protein Chem Struct Biol 90:31–65CrossRefPubMedGoogle Scholar
  23. Eöry L, Gilbert MTP, Li C, Li B, Archibald A, Aken BL, Zhang G, Jarvis E, Flicek P, Burt DW (2015) Avianbase: a community resource for bird genomics. Genome Biol 16:21. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Epplen JT, Engel W, Leipoldt M, Schmidtke J (1978) DNA-sequence organization in avian genomes. Chromosoma 69:307–321CrossRefPubMedGoogle Scholar
  25. Ezaz T, Deakin JE (2014) Repetitive sequence and sex chromosome evolution in vertebrates. Adv Evol Biol 2014:ID104683 CrossRefGoogle Scholar
  26. Galkina S, Fillon V, Saifitdinova A, Daks A, Kulak M, Dyomin A, Koshel E, Gaginskaya ER (2017) Chicken microchromosomes in the Lampbrush phase: a cytogenetic description. Cytogenet Genome Res 152:46–54. CrossRefPubMedGoogle Scholar
  27. Garrido-Ramos MA (2012) Repetitive DNA. Karger Medical and Scientific Publishers, p 238.
  28. Graves JAM (2014) Avian sex, sex chromosomes, and dosage compensation in the age of genomics. Chromosom Res 22:45–57CrossRefGoogle Scholar
  29. Gregory TR (2012) Animal genome size database. Available from Accessed 26 Oct 2016
  30. Guizard S, Piégu B, Arensburger P, Guillou F, Bigot Y (2016) Deep landscape update of dispersed and tandem repeats in the genome model of the red jungle fowl, Gallus gallus, using a series of de novo investigating tools. BMC Genomics 17:659. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Handley LJ, Ceplitis H, Ellegren H (2004) Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics 167:367–376CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hughes AL, Piontkivska H (2005) DNA repeat arrays in chicken and human genomes and the adaptive evolution of avian genome size. BMC Evol Biol 5:6CrossRefGoogle Scholar
  33. International Chicken Genome Sequencing Consortium (ICGSC) (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716CrossRefGoogle Scholar
  34. Itoh Y, Kampf K, Arnold AP (2008) Molecular cloning of zebra finch W chromosome repetitive sequences: evolution of the avian W chromosome. Chromosoma 117:111–121CrossRefPubMedGoogle Scholar
  35. Itoh Y, Mizuno S (2002) Molecular and cytological characterization of SspI-family repetitive sequence on the chicken W chromosome. Chromosom Res 10:499–511CrossRefGoogle Scholar
  36. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–427CrossRefPubMedGoogle Scholar
  37. Kasai F, O’Brien PCM, Ferguson-Smith MA (2012) Reassessment of genome size in turtle and crocodile based on chromosome measurement by flow karyotyping: close similarity to chicken. Biol Lett 8:631–635CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kodama H, Saitoh H, Tone M, Kuhara S, Sakaki Y, Mizuno S (1987) Nucleotide sequences and unusual electrophoretic behavior of the W chromosome-specific repeating DNA units of the domestic fowl, Gallus gallus domesticus. Chromosoma 96:18–25CrossRefPubMedGoogle Scholar
  39. Komissarov AS, Gavrilova EV, Demin SJ, Ishov AM, Podgornaya OI (2011) Tandemly repeated DNA families in the mouse genome. BMC Genomics 12:531. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Krasikova A, Derjusheva S, Galkina S, Kurganova A, Evteev A, Gaginskaya E (2006) On the positions of centromeres in chicken lampbrush chromosomes. Chromosom Res 14:777–789CrossRefGoogle Scholar
  41. Kuznetsova IS, Thevasagayam NM, Sridatta PSR, Komissarov AS, Saju JM, Ngoh SY, Jiang J, Shen X, Orban L (2014) Primary analysis of repeat elements of the Asian seabass (Lates Calcarifer) transcriptome and genome. Front Genet 5:223CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ladjali–Mohammedi K, Bitgood JJ, Tixier-Boichard M, Ponce De Leon FA (1999) International system for standardized avian karyotypes (ISSAK): standardized banded karyotypes of the domestic fowl (Gallus domesticus). Cytogenet Cell Genet 86:271–276CrossRefPubMedGoogle Scholar
  43. Marcais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764–770CrossRefPubMedPubMedCentralGoogle Scholar
  44. Maroteaux L, Heilig R, Dupret D, Mandel JL (1983) Repetitive satellite-like sequences are present within or upstream from 3 avian protein-coding genes. Nucleic Acids Res 11:1227–1243CrossRefPubMedPubMedCentralGoogle Scholar
  45. Masabanda JS, Burt DW, O’Brien PCM, Vignal A, Fillon V, Walsh PS, Cox H, Tempest HG, Smith J, Habermann F, Schmid M, Matsuda Y, Ferguson-Smith MA, Crooijmans R, Groenen MAM, Griffin DK (2004) Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166:1367–1373CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mason AS, Fulton JE, Hocking PM, Burt DW (2016) A new look at the LTR retrotransposon content of the chicken genome. BMC Genomics 17:688. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Matzke MA, Varga F, Berger H, Schernthaner J, Schweizer D, Mayr B, Matzke AJM (1990) A 41-42 bp tandemly repeated sequence isolated from nuclear envelopes of chicken erythrocytes is located predominantly on microchromosomes. Chromosoma 99:131–137CrossRefPubMedGoogle Scholar
  48. Mirkin SM, Frank-Kamenetskii MD (1994) H-DNA and related structures. Annu Rev Biophys Biomol Struct 23:541–576CrossRefPubMedGoogle Scholar
  49. Mizuno S, Kunita R, Nakabayashi O, Kuroda Y, Arai N, Harata M, Ogawa A, Itoh Y, Teranishi M, Hori T (2002) Z and W chromosomes of chickens: studies on their gene functions in sex determination and sex differentiation. Cytogenet Genome Res 99:236–244CrossRefPubMedGoogle Scholar
  50. Mizuno S, Macgregor H (1998) The ZW lampbrush chromosomes of birds: a unique opportunity to look at the molecular cytogenetics of sex chromosomes. Cytogenet Cell Genet 80:149–157CrossRefPubMedGoogle Scholar
  51. Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schäffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24(16):1757–1764. CrossRefPubMedPubMedCentralGoogle Scholar
  52. O’Meally D, Patel HR, Stiglec R, Sarre SD, Georges A, Marshall Graves JA, Ezaz T (2010) Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosom Res 18:787–800CrossRefGoogle Scholar
  53. Ogawa A, Solovei I, Hutchison N, Saitoh Y, Ikeda JE, Macgregor H, Mizuno S (1997) Molecular characterization and cytological mapping of a non-repetitive DNA sequence region from the W chromosome of chicken and its use as a universal probe for sexing Carinatae birds. Chromosom Res 5:93–101CrossRefGoogle Scholar
  54. Pezer Z, Brajković J, Feliciello I, Ugarkovć D (2012) Satellite DNA-mediated effects on genome regulation. Genome Dyn 7:153–169CrossRefPubMedGoogle Scholar
  55. Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y (2012) A tale of three next generation sequencing platforms: comparison of ion torrent, pacific biosciences and Illumina miseq sequencers. BMC Genomics 13:341CrossRefPubMedPubMedCentralGoogle Scholar
  56. Raghu G, Tevosian S, Anant S, Subramanian KN, George DL, Mirkin SM (1994) Transcriptional activity of the homopurine-homopyrimidine repeat of the c-Ki-ras promoter is independent of its H-forming potential. Nucleic Acids Res 22:3271–3279CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rajagopal P, Feigon J (1989) Triple-strand formation in the homopurine: homopytimidine DNA oligonucleotides d(G-A)4 and d(T-C)4. Nature 339:637–640. CrossRefPubMedGoogle Scholar
  58. Randsholt NB, Muller J-P, Loones M-T (1989) Transcription of dispersed repeated sequences during Pleurodeles Waltl oogenesis. Biol Cell 67:9–18CrossRefPubMedGoogle Scholar
  59. Saifitdinova A, Derjusheva S, Krasikova A, Gaginskaya E (2003) Lampbrush chromosomes of the chaffinch (Fringilla coelebs L.) Chromosom Res 11:99–113CrossRefGoogle Scholar
  60. Saifitdinova AF, Derjusheva SE, Malykh AG, Zhurov VG, Andreeva TF, Gaginskaya ER (2001) Centromeric tandem repeat from the chaffinch genome: isolation and molecular characterization. Genome 44:96–103CrossRefPubMedGoogle Scholar
  61. Saifitdinova AF, Galkina SA, Koshel EI, Gaginskaya ER (2016) The role of repetitive sequences in the evolution of sex chromosomes in birds. Tsitologiia 58:393–398Google Scholar
  62. Saitoh Y, Harata M, Mizuno S (1989) Presence of female-specific bent-repetitive DNA sequences in the genome of turkey and pheasant and their interactions with W-protein of chicken. Chromosoma 98:250–258CrossRefPubMedGoogle Scholar
  63. Saitoh Y, Mizuno S (1992) Distribution of XhoI and EcoRI family repetitive DNA-sequences into separate domains in the chicken W-chromosome. Chromosoma 101:474–477CrossRefPubMedGoogle Scholar
  64. Saitoh Y, Saitoh H, Ohtomo K, Mizuno S (1991) Occupancy of the majority of DNA in the chicken W chromosome by bent-repetitive sequences. Chromosoma 101:32–40CrossRefPubMedGoogle Scholar
  65. Schmid M, Enderle E, Schindler D, Schempp W (1989) Chromosome-banding and DNA-replication patterns in bird karyotypes. Cytogenet Cell Genet 52:139–146CrossRefPubMedGoogle Scholar
  66. Schmid M, Nanda I, Guttenbach M et al (2000) First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet 90:169–218CrossRefPubMedGoogle Scholar
  67. Schmid M, Smith J, Burt DW et al (2015) Third report on chicken genes and chromosomes. Cytogenet Genome Res 145:78–179CrossRefPubMedGoogle Scholar
  68. Shang WH, Hori T, Toyoda A, Kato J, Popendorf K, Sakakibara Y, Fujiyama A, Fukagawa T (2010) Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences. Genome Res 20:1219–1228CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shapiro JA, von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biol Rev Camb Philos Soc 80:227–250CrossRefPubMedGoogle Scholar
  70. Smeds L, Warmuth V, Bolivar P, Uebbing S, Burri R, Suh A, Nater A, Bureš S, Garamszegi LZ, Hogner S, Moreno J, Qvarnström A, Ružić M, Sæther SA, Sætre GP, Török J, Ellegren H (2015) Evolutionary analysis of the female-specific avian W chromosome. Nat Commun 6:7330CrossRefPubMedPubMedCentralGoogle Scholar
  71. Smit AFA, Hubley R, Green P (2013) RepeatMasker Open-4.0. (2013–2015) Available from Accessed 04 Aug 2015
  72. Solovei I, Gaginskaya E, Hutchison N, Macgregor HC (1993) Avian sex chromosomes in the lampbrush form: ZW lampbrush bivalents from six species of bird. Chromosom Res 1:153–166CrossRefGoogle Scholar
  73. Solovei I, Gaginskaya ER, Macgregor HC (1994) The arrangement and transcription of telomere DNA sequences at the ends of lampbrush chromosomes of birds. Chromosom Res 2:460–470CrossRefGoogle Scholar
  74. Solovei I, Ogawa A, Naito M, Mizuno S, Macgregor H (1998) Specific chromomeres on the chicken W lampbrush chromosome contain specific repetitive DNA sequence families. Chromosom Res 6:323–327CrossRefGoogle Scholar
  75. Starostina E, Tamazian G, Dobrynin P, O’Brien S, Komissarov A (2015). Cookiecutter: a tool for kmer-based read filtering and extraction. bioRxiv 024679. doi:
  76. Stepakov A, Galkina S, Bogomaz D, Gaginskaya E, Saifitdinova A (2015) Modified synthesis of 6-carboxyfluorescein (6-FAM): application to probe labeling for conventional Cytogenetics. Br J Appl Sci Technol 7:423–428CrossRefGoogle Scholar
  77. Stumph WE, Kristo P, Tsai MJ, Omalley BW (1981) A chicken middle-repetitive DNA-sequence which shares homology with mammalian ubiquitous repeats. Nucleic Acids Res 9:5383–5397CrossRefPubMedPubMedCentralGoogle Scholar
  78. Suka N, Shinohara Y, Saitoh Y, Saitoh H, Ohtomo K, Harata M, Shpigelman E, Mizuno S (1993) W-heterochromatin of chicken - its unusual DNA components, late replication, and chromatin structure. Genetica 88:93–105CrossRefPubMedGoogle Scholar
  79. Szarski H (1976) Cell-size and nuclear-DNA content in vertebrates. Int Rev Cytol 44:93–111CrossRefPubMedGoogle Scholar
  80. Tamazian G, Simonov S, Dobrynin P, Makunin A, Logachev A, Komissarov A, Shevchenko A, Brukhin V, Cherkasov N, Svitin A, Koepfli K, Pontius J, Driscoll C, Blackistone K, Barr C, Goldman D, Antunes A, Quilez J, Lorente-Galdos B, Alkan C, Marques-Bonet T, Menotti-Raymond M, David V, Narfström K, O’Brien S (2014) Annotated features of domestic cat – Felis Catus genome. Gigascience 3:13. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Tautz D, Renz M (1984) Simple sequences are ubiquitous repetitive components of eukaryote genomes. Nucleic Acids Res 12:4127–4138CrossRefPubMedPubMedCentralGoogle Scholar
  82. Treangen T, Salzberg S (2011) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46CrossRefPubMedPubMedCentralGoogle Scholar
  83. Tripathi J, Brahmachari SK (1991) Distribution of simple repetitive (TG/GA)n and (CT/GA)n sequences in human and rodent genomes. J Biomol Struct Dyn 9:387–397CrossRefPubMedGoogle Scholar
  84. Trofimova I, Krasikova A (2016) Transcription of highly repetitive tandemly organized DNA in amphibians and birds: a historical overview and modern concepts. RNA Biol 13:1246–1257. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Ugarkovic D (2005) Functional elements residing within satellite DNAs. EMBO Rep 6:1035–1039CrossRefPubMedPubMedCentralGoogle Scholar
  86. Usdin K, Furano AV (1988) Rat L (long interspersed repeated DNA) elements contain guanine-rich homopurine sequences that induce unpairing of contiguous duplex DNA. Proc Natl Acad Sci 85:4416–4420CrossRefPubMedPubMedCentralGoogle Scholar
  87. Varley JM, Macgregor HC, Erba HP (1980) Satellite DNA is transcribed on lampbrush chromosomes. Nature 283:686–688CrossRefPubMedGoogle Scholar
  88. Wang XF, Li J, Leung FC (2002) Partially inverted tandem repeat isolated from pericentric region of chicken chromosome 8. Chromosom Res 10:73–82CrossRefGoogle Scholar
  89. Warren WC, Hillier LW, Tomlinson C, Minx P, Kremitzki M, Graves T, Markovic C, Bouk N, Pruitt KD, Thibaud-Nissen F, Schneider V, Mansour TA, Brown CT, Zimin A, Hawken R, Abrahamsen M, Pyrkosz AB, Morisson M, Fillon V, Vignal A, Chow W, Howe K, Fulton JE, Miller MM, Lovell P, Mello CV, Wirthlin M, Mason AS, Kuo R, Burt DW, Dodgson JB, Cheng HH (2017) A new chicken genome assembly provides insight into avian genome structure. G3 (Bethesda) 7:109–117. CrossRefGoogle Scholar
  90. Wells RD, Collier DA, Hanvey JC, Shimizu M, Wohlrab F (1988) The chemistry and biology of unusual DNA structures adopted by oligopurine-oligopyrimidine sequences. FASEB J 2:2939–2949CrossRefPubMedGoogle Scholar
  91. Wicker T, Robertson JS, Schulze SR, Feltus FA, Magrini V, Morrison JA, Mardis ER, Wilson RK, Peterson DG, Paterson AH, Ivarie R (2005) The repetitive landscape of the chicken genome. Genome Res 15:126–136CrossRefPubMedPubMedCentralGoogle Scholar
  92. Xiong Y, Sundaralingam M (2000) Crystal structure of a DNA·RNA hybrid duplex with a polypurine RNA r(gaagaagag) and a complementary polypyrimidine DNA d(CTCTTCTTC). Nucleic Acids Res 28:2171–2176CrossRefPubMedPubMedCentralGoogle Scholar
  93. Zhang G, Li C, Li Q et al (2014) Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–1320CrossRefPubMedPubMedCentralGoogle Scholar
  94. Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, Gilbert MT, Zhang G (2014) Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346:1246338CrossRefPubMedGoogle Scholar
  95. Zopl D, Dineva B, Betz H, Gundelfinger ED (1990) Isolation of the chicken middle-molecular weight neurofilament (NF-M) gene and characterization of its promoter. Nucleic Acids Res 18:521–529CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Aleksey S. Komissarov
    • 1
  • Svetlana A. Galkina
    • 2
    • 3
  • Elena I. Koshel
    • 4
  • Maria M. Kulak
    • 4
  • Aleksander G. Dyomin
    • 3
    • 5
  • Stephen J. O’Brien
    • 1
    • 6
  • Elena R. Gaginskaya
    • 4
  • Alsu F. Saifitdinova
    • 5
    • 7
  1. 1.Theodosius Dobzhansky Center for Genome BioinformaticsSaint Petersburg State UniversitySaint PetersburgRussia
  2. 2.Department of Genetics and BiotechnologySaint Petersburg State UniversitySaint PetersburgRussia
  3. 3.Saint Petersburg Association of Scientists and ScholarsSaint PetersburgRussia
  4. 4.Department of Cytology and HistologySaint Petersburg State UniversitySaint PetersburgRussia
  5. 5.Chromas Research Resource CenterSaint Petersburg State UniversitySaint PetersburgRussia
  6. 6.Oceanographic CenterNova Southeastern UniversityFloridaUSA
  7. 7.International Centre of Reproductive MedicineSaint PetersburgRussia

Personalised recommendations