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Chromosome Research

, Volume 24, Issue 4, pp 437–450 | Cite as

Centromere inactivation on a neo-Y fusion chromosome in threespine stickleback fish

  • Jennifer N. Cech
  • Catherine L. PeichelEmail author
Original Article

Abstract

Having one and only one centromere per chromosome is essential for proper chromosome segregation during both mitosis and meiosis. Chromosomes containing two centromeres are known as dicentric and often mis-segregate during cell division, resulting in aneuploidy or chromosome breakage. Dicentric chromosome can be stabilized by centromere inactivation, a process which reestablishes monocentric chromosomes. However, little is known about this process in naturally occurring dicentric chromosomes. Using a combination of fluorescence in situ hybridization (FISH) and immunofluorescence combined with FISH (IF-FISH) on metaphase chromosome spreads, we demonstrate that centromere inactivation has evolved on a neo-Y chromosome fusion in the Japan Sea threespine stickleback fish (Gasterosteus nipponicus). We found that the centromere derived from the ancestral Y chromosome has been inactivated. Our data further suggest that there have been genetic changes to this centromere in the two million years since the formation of the neo-Y chromosome, but it remains unclear whether these genetic changes are a cause or consequence of centromere inactivation.

Keywords

Dicentric chromosome fusion Centromere inactivation CENP-A ChIP-seq Gasterosteus aculeatus Gasterosteus nipponicus 

Abbreviations

BAC

Bacterial artificial chromosome

CENP-A

Centromere protein A

ChIP-seq

Chromatin immunoprecipitation sequencing

Chr

Chromosome

DAPI

4′,6′-Diamidino-2-phenylindole

FISH

Fluorescence in situ hybridization

GacCEN

Threespine stickleback (Gasterosteus aculeatus) centromeric repeat sequence

IF-FISH

Immunofluorescence combined with FISH

IP

Immunoprecipitation

PBS

Phosphate-buffered saline

PBST

Phosphate-buffered saline Tween-20

Notes

Acknowledgments

We thank Kohta Yoshida for his initial observations, and the Peichel Lab, Sue Biggins, and Steve Henikoff for helpful discussions on this project and manuscript. We thank the Fred Hutchinson Cancer Research Center Genomics Shared Resource for the help with the ChIP-seq experiment and Ryan Basom for the help with data analysis. This research was supported by a National Science Foundation Graduate Research Fellowship (DGE-1256082), the National Institutes of Health Chromosome Metabolism and Cancer Training Grant (T32 CA009657), a National Institutes of Health grant (R01 GM116853), and the Fred Hutchinson Cancer Research Center.

Supplementary material

10577_2016_9535_MOESM1_ESM.pdf (51 kb)
Fig. S1 Pacific Ocean (ancestral) and Japan Sea (derived) chromosomes used in this study. A fusion between the acrocentric chromosome 9 and the metacentric Y chromosome from the ancestral Pacific Ocean species gave rise to the neo-Y chromosome in the Japan Sea species around two million years ago. The Japan Sea sticklebacks still retain the ancestral submetacentric X chromosome (now termed X1), and the unfused acrocentric chromosome 9 (now termed X2). (PDF 50 kb)
10577_2016_9535_MOESM2_ESM.pdf (659 kb)
Fig. S2 The ancestral state of chromosome 9, and the X and Y in Pacific Ocean stickleback fish. FISH with the ancestral X and Y chromosome BACs 188J19 (purple) and 101E08 (green) and the chromosome 9 BAC 44L12 (purple) on a Pacific Ocean male metaphase spread (a) shows the two unfused chromosome 9 s, the X chromosome, and the unfused Y chromosome each highlighted with a square box. Higher magnification of the boxed regions in panel (a) shows the X chromosome with two regions of BAC hybridization (b), the unfused Y chromosome with two regions of BAC hybridization (c), and the two unfused chromosome 9s (d, e). Scale bar, 5 μm (PDF 658 kb)
10577_2016_9535_MOESM3_ESM.pdf (2.7 mb)
Fig. S3 Telomere staining in Japan Sea male and female metaphase spreads. Telomere staining is seen on the ends of chromosomes in (a) Japan Sea female metaphase chromosomes and (b) Japan sea male metaphase chromosomes. The neo-Y is the largest chromosome and is highlighted by a box in panel (b). Panel (c) shows a higher magnification view of the neo-Y with no internal telomere signal. The primary centromeric constriction on the neo-Y is indicated by the white arrowhead. Scale bar, 5 μm (PDF 2775 kb)
10577_2016_9535_MOESM4_ESM.pdf (730 kb)
Fig. S4 The BAC clone 91G03 is a Y specific BAC. (a) FISH was performed on a Pacific Ocean male metaphase spread with BACs 101E08 (green), and 91G03 (purple). 101E08 hybridizes to the X and Y chromosome, while 91G03 only hybridizes to the Y. Panel (b) is a magnification of the Y chromosome from (a) showing hybridization of the known sex chromosome BAC 101E08 and BAC 91G03 to the very end of the Y chromosome. Panel (c) is a magnification of the X chromosome from (a), with hybridization of BAC 101E08 to the middle of the long arm, and no hybridization of BAC 91G03. Scale bar, 5 μm (PDF 730 kb)
10577_2016_9535_MOESM5_ESM.pdf (2.6 mb)
Fig. S5 CENP-A antibody staining on the ancestral Pacific Ocean Y chromosome. (a) A metaphase spread from Pacific Ocean embryos was stained with the CENP-A antibody (green) and the Y chromosome specific BAC 91G03 (purple). Panel (b) is a magnification of the boxed region in panel (a), highlighting the Y chromosome with 91G03 staining on the end of the long arm, and two distinct CENP-A puncta hybridizing to the centromere of each sister chromatid on the Y chromosome. Scale bar, 5 μm (PDF 2611 kb)
10577_2016_9535_MOESM6_ESM.pdf (50 kb)
Fig. S6 Comparison of the CENP-A protein amino acid sequence between the Pacific Ocean (PO) and Japan Sea (JS) sticklebacks. There is only one amino acid difference (red asterisk) between the two proteins, which is not in the amino acid sequence targeted by the CENP-A antibody (red letters). (PDF 49 kb)
10577_2016_9535_MOESM7_ESM.pdf (49 kb)
Fig. S7 Comparison of the CENP-A associated centromeric sequence between the Pacific Ocean (PO) and Japan Sea (JS) stickleback species. The Japan Sea consensus sequence is 98.9 % similar to the GacCEN sequence previously identified in the Pacific Ocean species (Cech and Peichel 2015). The red asterisk denotes the only three nucleotide differences between these two consensus sequences. Nucleotide ambiguities: Y = C or T; R = A or G. (PDF 48 kb)
10577_2016_9535_MOESM8_ESM.pdf (1.2 mb)
Fig. S8 The GacCEN probe hybridizes to the centromere on Japan Sea chromosomes. (a) The GacCEN probe hybridizes to a single region on each chromosome in a metaphase spread from a Japan Sea male. Panel (b) shows a magnification of the boxed region in (a), highlighting the hybridization of the GacCEN probe to the primary constriction (white arrowheads) on each chromosome. Scale bar, 5 μm (PDF 1270 kb)
10577_2016_9535_MOESM9_ESM.pdf (3 mb)
Fig. S9 The GacCEN probe colocalizes with CENP-A on Japan Sea chromosomes. The GacCEN probe (green) colocalizes with the CENP-A antibody (purple) at distinct puncta in interphase nuclei (a) as well as to a single region on each chromosome in a metaphase spread from a Japan Sea embryo (b). Panel (c) shows a magnification of the metaphase spread shown in (b). Scale bar, 5 μm (PDF 3103 kb)
10577_2016_9535_MOESM10_ESM.pdf (1.5 mb)
Fig. S10 Both submetacentric X1 chromosomes in the Japan Sea female show strong GacCEN hybridization. FISH with an X chromosome BAC 188J19 (purple), and GacCEN (green) on a Japan Sea female metaphase spread is in shown in panel (a). Panels (b) and (c) are magnifications of the boxed regions in panel (a), showing the two ancestral X1 chromosomes, with strong GacCEN staining (green arrowhead) consistent with the submetacentric position of the centromere. Scale bar, 5 μm (PDF 1488 kb)
10577_2016_9535_MOESM11_ESM.pdf (938 kb)
Fig. S11 GacCEN and centromere flanking regions on Japan Sea female X1 chromosomes. FISH with the X and Y BACs 180J08 and 171H24 (purple) and GacCEN (green) on a metaphase spread from a Japan Sea female is shown in panel (a). Panels (b) and (c) are magnifications of the boxed regions in (a) showing two distinct regions of BAC hybridization (purple arrowheads) flanking strong GacCEN staining (green arrowhead) on both X1 chromosomes. Scale bar, 5 μm (PDF 938 kb)

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Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Divisions of Basic Sciences and Human BiologyFred Hutchinson Cancer Research CenterSeattleUSA
  2. 2.Graduate Program in Molecular and Cellular BiologyUniversity of WashingtonSeattleUSA
  3. 3.Institute of Ecology and EvolutionUniversity of BernBernSwitzerland

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