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Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus

View ORCID ProfileJoanna L. Rifkin, Solomiya Hnatovska, Meng Yuan, Bianca M. Sacchi, Baharul I. Choudhury, Yunchen Gong, Pasi Rastas, Spencer C.H. Barrett, Stephen I. Wright
doi: https://doi.org/10.1101/2021.11.03.466946
Joanna L. Rifkin
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
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  • ORCID record for Joanna L. Rifkin
  • For correspondence: joanna.rifkin@utoronto.ca joannarifkin@gmail.com stephen.wright@utoronto.ca
Solomiya Hnatovska
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
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Meng Yuan
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
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Bianca M. Sacchi
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
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Baharul I. Choudhury
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
2Department of Biology, Queen’s University, Kingston, ON, Canada
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Yunchen Gong
3Centre for Analysis of Genome Evolution and Function, University of Toronto, Toronto, ON Canada
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Pasi Rastas
4Institute of Biotechnology, University of Helsinki, Finland
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Spencer C.H. Barrett
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
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Stephen I. Wright
1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON Canada
3Centre for Analysis of Genome Evolution and Function, University of Toronto, Toronto, ON Canada
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  • For correspondence: joanna.rifkin@utoronto.ca joannarifkin@gmail.com stephen.wright@utoronto.ca
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Summary

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Ethics Does your article include research that required ethical approval or permits?: This article does not present research with ethical considerations

  • Statement (if applicable): CUST_IF_YES_ETHICS :No data available.

  • Data It is a condition of publication that data, code and materials supporting your paper are made publicly available. Does your paper present new data?: Yes

  • Statement (if applicable): CUST_IF_YES_DATA :No data available.

  • Conflict of interest I/We declare we have no competing interests

  • Statement (if applicable): CUST_STATE_CONFLICT :No data available.

  • Statement (if applicable): Joanna L. Rifkin coordinated and performed descriptive genomics analyses and linear models and participated in conceiving and writing the paper

    Solomiya Hnatovska performed the TE annotation

    Meng Yuan performed differential expression analyses

    Bianca Sacchi performed differential expression analyses and SNP-calling

    Baharul Choudhury coordinated plant growth and nucleic acid expression

    Yunchen Gong created the transcriptome annotation

    Pasi Rastas generated the linkage maps and the improved genome assembly

    Spencer C.H. Barrett provided funding, development, and editing

    Stephen I. Wright conceived, funded, coordinated, and coauthored the paper

  • https://github.com/joannarifkin/Rumex-sex-specific

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 04, 2021.
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Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus
Joanna L. Rifkin, Solomiya Hnatovska, Meng Yuan, Bianca M. Sacchi, Baharul I. Choudhury, Yunchen Gong, Pasi Rastas, Spencer C.H. Barrett, Stephen I. Wright
bioRxiv 2021.11.03.466946; doi: https://doi.org/10.1101/2021.11.03.466946
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Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus
Joanna L. Rifkin, Solomiya Hnatovska, Meng Yuan, Bianca M. Sacchi, Baharul I. Choudhury, Yunchen Gong, Pasi Rastas, Spencer C.H. Barrett, Stephen I. Wright
bioRxiv 2021.11.03.466946; doi: https://doi.org/10.1101/2021.11.03.466946

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