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Post-Genome Biology of Primates pp 227–240Cite as

Evolution and Biological Meaning of Genomic Wastelands (RCRO): Proposal of Hypothesis

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Part of the Primatology Monographs book series (PrimMono)

Abstract

Differences of subterminal regions of chromosomes between humans and African apes have long been a matter of great interest in cytogenetics because of the absence and presence, respectively, of large heterochromatin blocks. I tried to dissect such mysterious heterochromatic blocks of African apes using molecular techniques. Thus far, four DNA components were found as elements constructing the subtelomeric heterochromatin (terminal retrotransposable compound repeated DNA organizations, RCROs). Of the four components, one (subterminal satellite, StSat) was localized by PRINS reaction on chromosomes of chimpanzee, bonobo, gorilla, siamang, and rhesus macaque. Here, I discuss hypothetical evolutionary aspects of the terminal RCROs, their intragenomic dispersion, and their biological meaning. These aspects will probably become important clues at the chromosomal level in post-genomic research to elucidate human evolution.

Keywords

  • Repetitive Sequence
  • Subtelomeric Region
  • Euchromatic Region
  • Heterochromatic Block
  • Ectopic Recombination

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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  • DOI: 10.1007/978-4-431-54011-3_15
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Abbreviations

FISH:

Fluorescence in situ hybridization

GW:

Genomic wasteland

HERV:

Human endogenous retrovirus

PRINS:

Primed in situ

RCRO:

Retrotransposable compound repeated DNA organization

StSat:

Subterminal satellite

References

  • Bailey JA, Eichler EE (2006) Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 7:552–564

    PubMed  CrossRef  CAS  Google Scholar 

  • Chen J-M, Cooper DN, Chuzhanova N et al (2007) Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet 8:762–775

    PubMed  CrossRef  CAS  Google Scholar 

  • Cheng Z, Ventura M, She X et al (2005) A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature (Lond) 437:88–93

    CrossRef  CAS  Google Scholar 

  • Disotell TR (2006) ‘Chumanzee’ evolution: the urge to diverge and merge. Genome Biol 7:240

    PubMed  CrossRef  Google Scholar 

  • Egel R (2008) Meiotic crossing-over and disjunction: overt and hidden layers of description and control. In: Egel R, Lankenau D-H (eds) Recombination and meiosis: crossing-over and disjunction. Springer, Berlin, pp 1–30

    Google Scholar 

  • Fisher SM (2005) On gene, speech, and language. N Engl J Med 353:1655–1657

    PubMed  CrossRef  CAS  Google Scholar 

  • Freitas-Junior LH, Bottius E, Pirrit LA et al (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome cluster of P. falciparum. Nature (Lond) 407:1018–1022

    Google Scholar 

  • Fujiyama A, Watanabe H, Toyoda A et al (2002) Construction and analysis of a human–chimpanzee comparative clone map. Science 295:131–134

    PubMed  CrossRef  Google Scholar 

  • Haaf T, Schmid M (1987) Chromosome heteromorphisms in the gorilla karyotype. J Hered 78:287–292

    PubMed  CAS  Google Scholar 

  • Hirai H (2001) Relationship of telomere sequence and constitutive heterochromatin in the human and apes as detected by PRINS. Methods Cell Sci 23:29–35

    PubMed  CrossRef  CAS  Google Scholar 

  • Hirai H, Matsubayashi K, Kumazaki K et al (2005) Chimpanzee chromosomes: retrotransposable compound repeat DNA organization (RCRO) and its influence on meiotic prophase and crossing-over. Cytogenet Genome Res 108:248–254

    PubMed  CrossRef  CAS  Google Scholar 

  • International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature (Lond) 409:860–921

    CrossRef  Google Scholar 

  • John B (1988) The biology of heterochromatin. In: Verma RS (ed) Heterochromatin: molecular and structural aspects. Cambridge University Press, Cambridge, NY, pp 1–128

    Google Scholar 

  • Koga A, Notohara M, Hirai H (2011) Evolution of subterminal satellite (StSat) repeats in hominids. Genetica 139:167–175

    Google Scholar 

  • Kunze B, Weichenhan D, Virks P et al (1996) Copy numbers of a clustered long-range repeat determine C-band staining. Cytogenet Cell Genet 73:86–91

    PubMed  CrossRef  CAS  Google Scholar 

  • Liebe B, Alsheimer M, Hoog C, Benavente R, Scherthan H (2004) Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol Biol Cell 15:827–837

    PubMed  CrossRef  CAS  Google Scholar 

  • Linardopoulou E, Mefford HC, Nguyen O et al (2001) Transcriptional activity of multiple copies of a subtelomerically located olfactory receptor gene that is polymorphic in number and location. Hum Mol Genet 10:2373–2383

    PubMed  CrossRef  CAS  Google Scholar 

  • Marks J (1985) C-band variability in the common chimpanzee, Pan troglodytes. J Hum Evol 14:669–675

    CrossRef  Google Scholar 

  • Mefford HC, Trask BJ (2002) The complex structure and dynamic evolution of human subtelomeres. Nat Rev Genet 3:91–102

    PubMed  CrossRef  CAS  Google Scholar 

  • Mefford HC, Linardopoulou E, Coil D et al (2001) Comparative sequencing of a multicopy subtelomeric region containing olfactory receptor genes reveals multiple interactions between non-homologous chromosomes. Hum Mol Genet 21:2363–2372

    CrossRef  Google Scholar 

  • Navarro A, Barton NH (2003a) Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447–459

    PubMed  Google Scholar 

  • Navarro A, Barton NH (2003b) Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes. Science 300:321–324

    PubMed  CrossRef  CAS  Google Scholar 

  • Olson MV, Varki A (2002) Sequencing the chimpanzee genome: insights into human evolution and disease. Nat Rev Genet 4:20–28

    CrossRef  Google Scholar 

  • Patterson N, Richter DJ, Gnerre S et al (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature (Lond) 441:1103–1108

    CrossRef  CAS  Google Scholar 

  • Pfeiffer P, Goedecke W, Obe G (2000) Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 15:289–302

    PubMed  CrossRef  CAS  Google Scholar 

  • Reiter LT, Liehr T, Rautenstrauss B et al (1999) Localization of mariner DNA transposons in the human genome by PRINS. Genome Res 9:839–843

    PubMed  CrossRef  CAS  Google Scholar 

  • Reithman H, Ambrosini A, Paul S (2005) Human subtelomere structure and variation. Chromosome Res 13:505–515

    CrossRef  Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358

    PubMed  CrossRef  Google Scholar 

  • Rothkamm K, Kruger I, Thompson LH, Lobrich M (2003) Pathways of DNA double-strand break repair during the mammalian. Mol Cell Biol 23:5706–5715

    PubMed  CrossRef  CAS  Google Scholar 

  • Royle NJ, Barid DM, Jeffereys AJ (1994) A subterminal satellite located adjacent to telomeres in chimpanzees is absent from the human genome. Nat Genet 6:52–56

    Google Scholar 

  • Scherthan H (2007) Telomere attachment and clustering during meiosis. Cell Mol Life Sci 64:117–124

    PubMed  CrossRef  CAS  Google Scholar 

  • Scherthan H, Weich S, Schwegler H et al (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134:1109–1125

    PubMed  CrossRef  CAS  Google Scholar 

  • Someville MJ, Mervis CB, Young EJ et al (2005) Severe expressive-language delay related to duplication of the Williams–Beuren locus. N Engl J Med 353:1694–1701

    CrossRef  Google Scholar 

  • Stanyon R, Chiarelli B, Gottlieb K, Patton W (1986) The phylogenetic and taxonomic status of Pan paniscus: a chromosomal perspective. Am J Phys Anthropol 69:489–498

    CrossRef  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    PubMed  CrossRef  CAS  Google Scholar 

  • Sumner AT (2003) Chromosomes: organization and function. Blackwell, Oxford

    Google Scholar 

  • Teng S-C, Zakian VA (1999) Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cervisiae. Mol Cell Biol 19:8083–8093

    PubMed  CAS  Google Scholar 

  • van Overveld PGM, Lemmers RJFL, Deidda G et al (2000) Interchromosomal repeat array interactions between chromosomes 4 and 10: a model for subtelomeric plasticity. Hum Mol Genet 19:2879–2884

    CrossRef  Google Scholar 

  • Winkler W, Myers SR, Richter DJ et al (2005) Comparison of fine-scale recombination rates in humans and chimpanzees. Science 308:107–111

    CrossRef  Google Scholar 

  • Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530

    PubMed  CrossRef  CAS  Google Scholar 

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Acknowledgments

Primate biomaterials were supplied from KUPRI, Japan; JMC, Japan; and Ouji Zoo, Japan, through the GAIN project; PSSP, IPB, Indonesia; and PBZT, Madagascar. I thank Dr. A Koga for his critical reading of the manuscript and valuable comments, and Dr. Elizabeth Nakajima for revision of the English. This research was supported in part by the Global COE Program (A06 to Kyoto University) of the Ministry of Education, Culture, Sports, Science and Technology-Japan and a grant of the Japan Society for the Promotion of Science (20405016, 22247037).

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  1. Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi, 484-8506, Japan

    Hirohisa Hirai

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  1. Hirohisa Hirai
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Editors and Affiliations

  1. Primate Research Institute, Kyoto University, Kanrin 41-2, Inuyama, Aichi, 484-8506, Japan

    Hirohisa Hirai

  2. Department of Cellular and Molecular Bio., Inuyama, 484-8506, Japan

    Hiroo Imai

  3. Kyoto University, Primates Research Institute, Kanbayashi, Inuyama, 484-8506, Aichi, Japan

    Yasuhiro Go

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Hirai, H. (2012). Evolution and Biological Meaning of Genomic Wastelands (RCRO): Proposal of Hypothesis. In: Hirai, H., Imai, H., Go, Y. (eds) Post-Genome Biology of Primates. Primatology Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54011-3_15

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