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Cited by 42Chromosomal and Genetic VariationsGenomic variations and chromosomal abnormalitiesGenome Rearrangement Algorithms

The evolution of African great ape subtelomeric heterochromatin and the fusion of human chromosome 2

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Ventura, Mario, Catacchio, Claudia R., Sajjadian, Saba, Vives, Laura, Sudmant, Peter H., Marques-Bonet, Tomas, Graves, Tina A., Wilson, Richard K. +1 more·2012·Genome Research
DOI 10.1101/gr.136556.111PMC PMC3371704
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Abstract

Chimpanzee and gorilla chromosomes differ from human chromosomes by the presence of large blocks of subterminal heterochromatin thought to be composed primarily of arrays of tandem satellite sequence. We explore their sequence composition and organization and show a complex organization composed of specific sets of segmental duplications that have hyperexpanded in concert with the formation of subterminal satellites. These regions are highly copy number polymorphic between and within species, and copy number differences involving hundreds of copies can be accurately estimated by assaying read-depth of next-generation sequencing data sets. Phylogenetic and comparative genomic analyses suggest that the structures have arisen largely independently in the two lineages with the exception of a few seed sequences present in the common ancestor of humans and African apes. We propose a model where an ancestral human-chimpanzee pericentric inversion and the ancestral chromosome 2 fusion both predisposed and protected the chimpanzee and human genomes, respectively, to the formation of subtelomeric heterochromatin. Our findings highlight the complex interplay between duplicated sequences and chromosomal rearrangements that rapidly alter the cytogenetic landscape in a short period of evolutionary time.

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  • Chimpanzee chromosomes 2A and 2B are capped with hyper-expanded segmental duplications and tandem repeats (StSats) not existing in the human genome.

    “since the chimpanzee chromosomes 2A and 2B are capped with hyper-expanded segmental duplications and tandem repeats (StSats) not existing in the human genome [8, 40], we cannot measure the magnitude of the accumulation of BCS in those fragments comparing to the human reference.”

    From Revised time estimation of the ancestral human chromosome 2 fusion (2022) · cites this paper as [40]

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Research works printed but not linked: 38

  1. Bandyopadhyay R, Berend SA, Page SL, Choo KH, Shaffer LG 2001a Satellite III sequences on 14p and their relevance to Robertsonian translocation formation. Chromosome Res 9: 235– 242 11330398
  2. Bandyopadhyay R, McQuillan C, Page SL, Choo KH, Shaffer LG 2001b Identification and characterization of satellite III subfamilies to the acrocentric chromosomes. Chromosome Res 9: 223– 233 11330397
  3. Carreto L, Eiriz MF, Gomes AC, Pereira PM, Schuller D, Santos MA 2008 Comparative genomics of wild type yeast strains unveils important genome diversity. BMC Genomics 9: 524 doi: 10.1186/1471-2164-9-524 18983662 PMC2588607 · DOI
  4. Fan Y, Linardopoulou E, Friedman C, Williams E, Trask BJ 2002 Genomic structure and evolution of the ancestral chromosome fusion site in 2q13-2q14.1 and paralogous regions on other human chromosomes. Genome Res 12: 1651– 1662 12421751 PMC187548
  5. Gerber JC, Neuhann TM, Tyshchenko N, Smitka M, Hackmann K 2011 Expanding the clinical and neuroradiological phenotype of 6q27 microdeletion: Olfactory bulb aplasia and anosmia. Am J Med Genet A 155: 1981– 1986 21744487
  6. Gonzalez-Garcia M, Gonzalez-Sanchez M, Puertas MJ 2006 The high variability of subtelomeric heterochromatin and connections between nonhomologous chromosomes, suggest frequent ectopic recombination in rye meiocytes. Cytogenet Genome Res 115: 179– 185 17065801
  7. Gross M, Starke H, Trifonov V, Claussen U, Liehr T, Weise A 2006 A molecular cytogenetic study of chromosome evolution in chimpanzee. Cytogenet Genome Res 112: 67– 75 16276092
  8. Haaf T, Schmid M 1987 Chromosome heteromorphisms in the gorilla karyotype. Analyses with distamycin A/DAPI, quinacrine and 5-azacytidine. J Hered 78: 287– 292 2445809
  9. Hirai H, Matsubayashi K, Kumazaki K, Kato A, Maeda N, Kim HS 2005 Chimpanzee chromosomes: Retrotransposable compound repeat DNA organization (RCRO) and its influence on meiotic prophase and crossing-over. Cytogenet Genome Res 108: 248– 254 15545737
  10. IJdo JW, Baldini A, Ward DC, Reeders ST, Wells RA 1991 Origin of human chromosome 2: An ancestral telomere-telomere fusion. Proc Natl Acad Sci 88: 9051– 9055 1924367 PMC52649
  11. Jarmuz M, Glotzbach CD, Bailey KA, Bandyopadhyay R, Shaffer LG 2007 The evolution of satellite III DNA subfamilies among primates. Am J Hum Genet 80: 495– 501 17273970 PMC1821104
  12. Kidd JM, Graves T, Newman TL, Fulton R, Hayden HS, Malig M, Kallicki J, Kaul R, Wilson RK, Eichler EE 2010 A human genome structural variation sequencing resource reveals insights into mutational mechanisms. Cell 143: 837– 847 21111241 PMC3026629
  13. Koga A, Notohara M, Hirai H 2011 Evolution of subterminal satellite (StSat) repeats in hominids. Genetica 139: 167– 175 21136140
  14. Kudo H, Emi M, Ishigaki Y, Tsunoda U, Hinokio Y, Ishii M, Sato H, Yamada T, Katagiri H, Oka Y 2011 Frequent loss of genome gap region in 4p16.3 subtelomere in early-onset type 2 diabetes mellitus. Exp Diabetes Res 2011: 498460 doi: 10.1155/2011/498460 21754918 PMC3132460 · DOI
  15. Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camano P, Dauwerse JG, Snider L, Straasheijm KR, van Ommen GJ, Padberg GW, 2010 A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329: 1650– 1653 20724583 PMC4677822
  16. Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ 2005 Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94– 100 16136133 PMC1368961
  17. Linardopoulou EV, Parghi SS, Friedman C, Osborn GE, Parkhurst SM, Trask BJ 2007 Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet 3: e237 doi: 10.1371/journal.pgen.0030237 18159949 PMC2151093 · DOI
  18. Marques-Bonet T, Kidd JM, Ventura M, Graves TA, Cheng Z, Hillier LW, Jiang Z, Baker C, Malfavon-Borja R, Fulton LA, 2009 A burst of segmental duplications in the genome of the African great ape ancestor. Nature 457: 877– 881 19212409 PMC2751663
  19. McPherson JD, Marra M, Hillier L, Waterston RH, Chinwalla A, Wallis J, Sekhon M, Wylie K, Mardis ER, Wilson RK, 2001 A physical map of the human genome. Nature 409: 934– 941 11237014
  20. Mefford HC, Trask BJ 2002 The complex structure and dynamic evolution of human subtelomeres. Nat Rev Genet 3: 91– 102 11836503
  21. Miklos GL, Nankivell RN 1976 Telomeric satellite DNA functions in regulating recombination. Chromosoma 56: 143– 167 976019
  22. Nieves M, De Oliveira EH, Amaral PJ, Nagamachi CY, Pieczarka JC, Muhlmann MC, Mudry MD 2011 Analysis of the heterochromatin of Cebus (Primates, Platyrrhini) by micro-FISH and banding pattern comparisons. J Genet 90: 111– 117 21677395
  23. Parsons JD 1995 Miropeats: Graphical DNA sequence comparisons. Comput Appl Biosci 11: 615– 619 8808577
  24. Prieto P, Martin A, Cabrera A 2004 Chromosomal distribution of telomeric and telomeric-associated sequences in Hordeum chilense by in situ hybridization. Hereditas 141: 122– 127 15660972
  25. Ptak SE, Hinds DA, Koehler K, Nickel B, Patil N, Ballinger DG, Przeworski M, Frazer KA, Paabo S 2005 Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet 37: 429– 434 15723063
  26. Riethman H, Ambrosini A, Paul S 2005 Human subtelomere structure and variation. Chromosome Res 13: 505– 515 16132815
  27. Roberto R, Misceo D, D'Addabbo P, Archidiacono N, Rocchi M 2008 Refinement of macaque synteny arrangement with respect to the official rheMac2 macaque sequence assembly. Chromosome Res 16: 977– 985 18841486
  28. Royle NJ, Baird DM, Jeffreys AJ 1994 A subterminal satellite located adjacent to telomeres in chimpanzees is absent from the human genome. Nat Genet 6: 52– 56 8136835
  29. Rudd MK, Willard HF 2004 Analysis of the centromeric regions of the human genome assembly. Trends Genet 20: 529– 533 15475110
  30. Rudd MK, Endicott RM, Friedman C, Walker M, Young JM, Osoegawa K, de Jong PJ, Green ED, Trask BJ 2009 Comparative sequence analysis of primate subtelomeres originating from a chromosome fission event. Genome Res 19: 33– 41 18952852 PMC2612970
  31. Sudmant PH, Kitzman JO, Antonacci F, Alkan C, Malig M, Tsalenko A, Sampas N, Bruhn L, Shendure J, Eichler EE 2010 Diversity of human copy number variation and multicopy genes. Science 330: 641– 646 21030649 PMC3020103
  32. van der Maarel SM, Tawil R, Tapscott SJ 2011 Facioscapulohumeral muscular dystrophy and DUX4: Breaking the silence. Trends Mol Med 17: 252– 258 21288772 PMC3092836
  33. Ventura M, Archidiacono N, Rocchi M 2001 Centromere emergence in evolution. Genome Res 11: 595– 599 11282974 PMC311056
  34. Ventura M, Weigl S, Carbone L, Cardone MF, Misceo D, Teti M, D'Addabbo P, Wandall A, Bjorck E, de Jong PJ, 2004 Recurrent sites for new centromere seeding. Genome Res 14: 1696– 1703 15342555 PMC515314
  35. Ventura M, Catacchio CR, Alkan C, Marques-Bonet T, Sajjadian S, Graves TA, Hormozdiari F, Navarro A, Malig M, Baker C, 2011 Gorilla genome structural variation reveals evolutionary parallelisms with chimpanzee. Genome Res 21: 1640– 1649 21685127 PMC3202281
  36. Wallace BM, Hulten MA 1985 Meiotic chromosome pairing in the normal human female. Ann Hum Genet 49: 215– 226 4073835
  37. Wienberg J, Jauch A, Ludecke HJ, Senger G, Horsthemke B, Claussen U, Cremer T, Arnold N, Lengauer C 1994 The origin of human chromosome 2 analyzed by comparative chromosome mapping with a DNA microlibrary. Chromosome Res 2: 405– 410 7981945
  38. Yunis JJ, Prakash O 1982 The origin of man: A chromosomal pictorial legacy. Science 215: 1525– 1530 7063861

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Authors
Ventura, M., Catacchio, C. R., Sajjadian, S., Vives, L., Sudmant, P. H., Marques-Bonet, T., Graves, T. A., Wilson, R. K., & Eichler, E. E.
Affiliations
  • University of Washington (US)
  • Washington University in St. Louis (US)
  • Howard Hughes Medical Institute (US)
Corresponding author
Eichler, Evan E.
ORCID
Venue
Genome Research
Publisher
Cold Spring Harbor Laboratory
Published
2012-03-14
Volume
22
Issue
6
Pages
1036-1049
ISSN
1088-9051 (ISSN-L)
DOI
10.1101/gr.136556.111
PMC
PMC3371704
OpenAlex
W2116003061
Cited by
42
References
3
Citations by year
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Type
posted content
Language
en
Open access
Locations
  • Genome Research (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (publishedVersion, cc-by-nc)
  • Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
  • HighWire Press Open Archive (submittedVersion)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, cc-by-nc)
  • CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health
  • National Human Genome Research Institute (HG002385, U54HG003079, R01HG002385)
  • National Institute of General Medical Sciences (GM 058815, R01GM058815)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
Keywords
subtelomeric heterochromatin, segmental duplication, copy number variation, pericentric inversion, chimpanzees, gorillas, African apes, chromosomal rearrangements, comparative genomics, phylogenetic analysis
MeSH terms
Amino Acid Sequence, Animals, Pan troglodytes, Chromosomes, Human, Pair 2, DNA, Satellite, Gorilla gorilla, Heterochromatin, Humans, Models, Genetic, Molecular Sequence Data, Phylogeny, Hominidae, Telomere, Evolution, Molecular, Gene Duplication, Cytogenetic Analysis

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