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Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway

A Corrigendum to this article was published on 01 March 2006

Abstract

The mammalian Y chromosome has unique characteristics compared with the autosomes or X chromosomes. Here we report the finished sequence of the chimpanzee Y chromosome (PTRY), including 271 kb of the Y-specific pseudoautosomal region 1 and 12.7 Mb of the male-specific region of the Y chromosome. Greater sequence divergence between the human Y chromosome (HSAY) and PTRY (1.78%) than between their respective whole genomes (1.23%) confirmed the accelerated evolutionary rate of the Y chromosome. Each of the 19 PTRY protein-coding genes analyzed had at least one nonsynonymous substitution, and 11 genes had higher nonsynonymous substitution rates than synonymous ones, suggesting relaxation of selective constraint, positive selection or both. We also identified lineage-specific changes, including deletion of a 200-kb fragment from the pericentromeric region of HSAY, expansion of young Alu families in HSAY and accumulation of young L1 elements and long terminal repeat retrotransposons in PTRY. Reconstruction of the common ancestral Y chromosome reflects the dynamic changes in our genomes in the 5–6 million years since speciation.

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Figure 1: Schematic view of the sequenced area and major landmarks on chimpanzee chromosome Y.
Figure 2: Features of the PTRY sequence.
Figure 3: Comparison of the PAR1 and MSY regions of PTRY.
Figure 4: Evolutionary relationship between inserted repetitive elements.
Figure 5: Synteny blocks in the sequenced region of PTRY and comparison with HSAY.
Figure 6: Comparison of the palindromic structures between PTRY and HSAY.

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Acknowledgements

We are grateful to all the technical staff of RIKEN Genomic Sciences Center (RIKEN-GSC) and Genome Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB). In addition, we wish to thank Y. Nakahori (Tokushima University), T. Matsuzawa (Primate Research Institute, Kyoto University), T. Ishida (The University of Tokyo), N. Collier (National Institute of Informatics) for the supply of the human and chimpanzee samples, and discussion. We also thank the Osaka Municipal Tennoji (Osaka, Japan) for discussions on the subspecies of chimpanzee. We would also like to thank A. Frankish, E. Hart and J. Harrow from the HAVANA group, the Wellcome Trust Sanger Institute, for providing annotation of the human Y chromosome. We are also thankful for D.C. Page (Whitehead Institute), R.K. Wilson (Washington University School of Medicine) and the Chimpanzee Sequencing and Analysis Consortium for the availability of the sequences in the public databases. This work was supported in part by: Special Fund for RIKEN-GSC; Grant-in-Aid for Scientific Research on Priority Areas “Genome Science” from the Ministry of Education, Culture, Sports, Science and Technology, Japan; The Ministry of Science & Technology, Korea, and Special Fund of KRIBB, Korea.

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Correspondence to Hong-Seog Park or Asao Fujiyama.

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Supplementary information

Supplementary Fig. 1

Gene landscape of PTRY. (PDF 695 kb)

Supplementary Fig. 2

Presence or absence of CD24L4 in primates. (PDF 148 kb)

Supplementary Fig. 3

Correlation between nucleotide substitution and indel frequencies. (PDF 329 kb)

Supplementary Fig. 4

Analysis of the 200 kb duplicated segments. (PDF 176 kb)

Supplementary Fig. 5

Structural changes of human and chimpanzee Y chromosome during sex chromosome evolution. (PDF 225 kb)

Supplementary Fig. 6

Features of the PTRY ampliconic units. (PDF 94 kb)

Supplementary Table 1

List of the clones analyzed in this study. (PDF 37 kb)

Supplementary Table 2

List of annotated genes. (PDF 93 kb)

Supplementary Table 3

Gene analysis. (PDF 17 kb)

Supplementary Table 4

Summary of base substitutions between PTRY and HSAY, and between PTR22 and HSA21. (PDF 14 kb)

Supplementary Table 5

List of accession numbers for the clones used in this study. (PDF 17 kb)

Supplementary Table 6

Positions of LINE1 and Alu sequences in the HSAY and PTRY sequences. (PDF 21 kb)

Supplementary Table 7

Positions of the synteny blocks and the alignments. (PDF 13 kb)

Supplementary Methods (PDF 23 kb)

Supplementary Note (PDF 36 kb)

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Kuroki, Y., Toyoda, A., Noguchi, H. et al. Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nat Genet 38, 158–167 (2006). https://doi.org/10.1038/ng1729

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