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Structural variations of subterminal satellite blocks and their source mechanisms as inferred from the meiotic configurations of chimpanzee chromosome termini

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Abstract

African great apes have large constitutive heterochromatin (C-band) blocks in subtelomeric regions of the majority of their chromosomes, but humans lack these. Additionally, the chimpanzee meiotic cell division process demonstrates unique partial terminal associations in the first meiotic prophase (pachytene). These are likely formed as a result of interaction among subtelomeric C-band blocks. We thus conducted an extensive study to define the features in the subtelomeric heterochromatic regions of chimpanzee chromosomes undergoing mitotic metaphase and meiotic cell division. Molecular cytogenetic analyses with probes of both subterminal satellite DNA (a main component of C-band) and rDNA demonstrated principles of interaction among DNA arrays. The results suggest that homologous and ectopic recombination through persistent subtelomeric associations (post-bouquet association observed in 32% of spermatocytes in the pachytene stage) appears to create variability in heterochromatin patterns and simultaneously restrain subtelomeric genome polymorphisms. That is, the meeting of non-homologous chromosome termini sets the stage for ectopic pairing which, in turn, is the mechanism for generating variability and genomic dispersion of subtelomeric C-band blocks through a system of concerted evolution. Comparison between the present study and previous reports indicated that the chromosomal distribution rate of sutelomeric regions seems to have antagonistic correlation with arm numbers holding subterminal satellite blocks in humans, chimpanzees, and gorillas. That is, the increase of subterminal satellite blocks probably reduces genomic diversity in the subtelomeric regions. The acquisition vs. loss of the subtelomeric C-band blocks is postulated as the underlying engine of this chromosomal differentiation yielded by meiotic chromosomal interaction.

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Abbreviations

C-band:

Constitutive heterochromatin

CeC:

Centromeric C-band

DAPI:

4′-6-Diamidino-2-phenylindole

FISH:

Fluorescent in situ hybridization

NaC:

NOR-adjoining C-band

NOR:

Nucleolus organizer region

SCB:

Subterminal constitutive heterochromatin block

StC:

Subterminal C-band

StSat:

Subterminal satellite

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Acknowledgments

We thank the staff members of the Center of Human Evolution Modeling Research, Primate Research Institute, and the Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, for their technical assistance. We are grateful to the Japan Monkey Center and Ishikawa Zoo for supplying blood samples of bonobo and gorilla, respectively.

Funding

This research was supported by grants from the Japan Society for the Promotion of Science (JSPS; 15H04427 to AK, 20405016 and 22247037 to HH), the Global Center of Excellence of the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT; Program A06, Kyoto University), the Unit of Human-Nature Interlaced Life Science, Kyoto University Research Coordination Alliance, and the Kyoto University Foundation.

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Authors and Affiliations

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

    Hirohisa Hirai, Yuriko Hirai, Kiyoaki Matsubayashi & Akihiko Koga

  2. The Unit of Human-Nature Interlaced Life Science, Kyoto University Research Coordination Alliance, Kyoto, Japan

    Hirohisa Hirai

  3. Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, Uto, Kumamoto, Japan

    Toshifumi Udono

  4. Department of Anthropology and School of Biomedical Science, Kent State University, Kent, OH, 44242, USA

    Anthony J. Tosi

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  1. Hirohisa Hirai
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  2. Yuriko Hirai
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  4. Kiyoaki Matsubayashi
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  6. Akihiko Koga
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Correspondence to Hirohisa Hirai.

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Animal ethics approval was obtained from the Monkey Care and Use Committee of Primate Research Institute, Kyoto University (approvals 07–1632, 08–1703, 09–1787, 2010–084).

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Hirai, H., Hirai, Y., Udono, T. et al. Structural variations of subterminal satellite blocks and their source mechanisms as inferred from the meiotic configurations of chimpanzee chromosome termini. Chromosome Res 27, 321–332 (2019). https://doi.org/10.1007/s10577-019-09615-z

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