Abstract
Homomorphic sex chromosomes and their turnover are common in teleosts. We investigated the evolution of nascent sex chromosomes in several populations of two sister species of African annual killifishes, Nothobranchius furzeri and N. kadleci, focusing on their under-studied repetitive landscape. We combined bioinformatic analyses of the repeatome with molecular cytogenetic techniques, including comparative genomic hybridization, fluorescence in situ hybridization with satellite sequences, ribosomal RNA genes (rDNA) and bacterial artificial chromosomes (BACs), and immunostaining of SYCP3 and MLH1 proteins to mark lateral elements of synaptonemal complexes and recombination sites, respectively. Both species share the same heteromorphic XY sex chromosome system, which thus evolved prior to their divergence. This was corroborated by sequence analysis of a putative master sex determining (MSD) gene gdf6Y in both species. Based on their divergence, differentiation of the XY sex chromosome pair started approximately 2 million years ago. In all populations, the gdf6Y gene mapped within a region rich in satellite DNA on the Y chromosome long arms. Despite their heteromorphism, X and Y chromosomes mostly pair regularly in meiosis, implying synaptic adjustment. In N. kadleci, Y-linked paracentric inversions like those previously reported in N. furzeri were detected. An inversion involving the MSD gene may suppress occasional recombination in the region, which we otherwise evidenced in the N. furzeri population MZCS-121 of the Limpopo clade lacking this inversion. Y chromosome centromeric repeats were reduced compared with the X chromosome and autosomes, which points to a role of relaxed meiotic drive in shaping the Y chromosome repeat landscape. We speculate that the recombination rate between sex chromosomes was reduced due to heterochiasmy. The observed differences between the repeat accumulations on the X and Y chromosomes probably result from high repeat turnover and may not relate closely to the divergence inferred from earlier SNP analyses.
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Data availability
The following nucleotide sequences were deposited in NCBI GenBank: 5S rDNA from N. kadleci (accession number MZ694985), 18S rDNA from N. guentheri (MZ682111), and X- and Y-linked gdf6 gene variants from N. kadleci (ON921000-ON921004). Measurements related to the construction of cytogenetic maps of sex chromosomes are available from the Dryad digital data repository: https://doi.org/10.5061/dryad.4mw6m90ck (Štundlová et al. 2022). All other relevant data are within the paper and its supplementary material.
Abbreviations
- 2n:
-
Diploid chromosome number
- a:
-
Acrocentric chromosome
- BAC:
-
Bacterial artificial chromosome
- BSA:
-
Bovine serum albumin
- CDS:
-
Coding sequence
- CGH:
-
Comparative genomic hybridization
- CMA3 :
-
Chromomycin A3
- DABCO:
-
1,4-Diazabicyclo(2.2.2)-octane
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- DOP-PCR:
-
Degenerate oligonucleotide-primed PCR
- dUTP:
-
2′-Deoxyuridine-5′-triphosphate
- FISH:
-
Fluorescence in situ hybridization
- FITC:
-
Fluorescein isothiocyanate
- gdf6 :
-
Growth differentiation factor 6
- gDNA:
-
Genomic DNA
- KY:
-
Thousand years
- m:
-
Metacentric chromosome
- MLH1:
-
MutL homolog 1
- MSD:
-
Master sex-determining (gene)
- MYA:
-
Million years ago
- MY:
-
Million years
- ND-FISH:
-
Non-denaturing FISH
- NGS:
-
Normal goat serum
- p-arm:
-
Short chromosome arm
- PBS:
-
Phosphate-buffered saline
- PCR:
-
Polymerase chain reaction
- q-arm:
-
Long chromosome arm
- rDNA:
-
Ribosomal DNA
- RT:
-
Room temperature
- SA:
-
Sexual antagonism
- SD:
-
Sex-determining (region)
- SDS:
-
Sodium dodecyl sulfate
- SNP:
-
Single-nucleotide polymorphism
- SSC:
-
Saline-sodium citrate
- SYCP3:
-
Synaptonemal complex protein 3
- st:
-
Subtelocentric chromosome
- UTR:
-
Untranslated region
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Acknowledgements
The authors are grateful to S. Förste and M. Platzer (The Leibniz Institute on Aging – Fritz Lipmann Institute, Jena, Germany) for providing BAC clones from the N. furzeri genomic library, to D. R. Valenzano and D. E. M. de Bakker (The Leibniz Institute on Aging – Fritz Lipmann Institute, Jena, Germany) for providing fish material for the gdf6 sequence analyses and P. Koch (Core Facility Life Science Computing, The Leibniz Institute on Aging – Fritz Lipmann Institute, Jena, Germany) for providing alignments of genomic sequencing reads from Reichwald et al. (2015). We are also thankful to P. Šejnohová and D. Dedukh (both Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Liběchov, Czech Republic) for the laboratory assistance and advice on the immunostaining protocol, respectively, and to C. Johnson as well as A.-M. Dion-Côté (Université de Moncton, Canada) for copyediting. We would also like to thank two anonymous reviewers for their feedback and valuable comments.
Funding
This study was supported by The Czech Science Foundation (grant no. 19-22346Y) (J. Š., P. N., M. H., K. L., A. V., T. P., M. A., Š. P., M. H., M. J., A. S.) and further by a grant (EN 280/15–1) from the Deutsche Forschungsgemeinschaft (C. E., A. R.) and the projects EXCELLENCE CZ.02.1.01/0.0/0.0/15_003/0000460 OP RDE (Ministry of Education, Youth and Sports) (P. R.); RVO:67985904 of IAPG CAS, Liběchov (Czech Academy of Sciences) (M. A., A. M., T. D., J. B., Š. P., P. R., A. S.); and the Charles University Research Centre program No. 204069 (M. A.). Computational resources were supplied by the project “e-Infrastruktura CZ” (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures and the ELIXIR-CZ project (LM2018131), part of the international ELIXIR infrastructure. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Conceptualization: A. S., P. N., M. R.; data curation: P. N., A. V., M. D., T. D., A. R.; formal analysis: J. Š., P. N., A. V., M. D.; funding acquisition: A. S., C. E.; investigation: J. Š., M. H., K. L., A. V., T. P., M. A., A. R., M. D., Š. P., A. M., S. A. S., M. H., M. J., T. D., J. B., P. N., A. S.; methodology: J. Š., A. S., P. N., A. V., M. D., A. M., S. A. S., A. R.; project administration: A. S., P. N.; resources: A. S., P. N., M. R., C. E., P. R.; supervision: A. S., P. N., M. R., P. R., J. B.; validation: J. Š., A. S., P. N., A. R.; writing original draft: A. S.; writing—review and editing: P. N., A. S., A. R., J. Š., M. R., A. V., M. A., J. B., P. R., S. A. S., M. D., C. E.
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To prevent fish suffering, all handling of fish individuals followed European standards in agreement with §17 of the Act No. 246/1992 coll. The procedures involving fishes were supervised by the Institutional Animal Care and Use Committee of the Institute of Animal Physiology and Genetics CAS, v.v.i., and the supervisor’s permit number CZ 02361 was certified and issued by the Ministry of Agriculture of the Czech Republic. For direct preparations of chromosomes from kidney and gonads, fishes were euthanized using 2-phenoxyethanol (Sigma-Aldrich) before organ sampling. Fin samples (a narrow strip of the caudal fin) were taken from live individuals after fishes were anesthetized using MS-222 (Merck KGaA, Darmstadt, Germany).
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Štundlová, J., Hospodářská, M., Lukšíková, K. et al. Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci. Chromosome Res 30, 309–333 (2022). https://doi.org/10.1007/s10577-022-09707-3
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DOI: https://doi.org/10.1007/s10577-022-09707-3