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Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level

View ORCID ProfileJuanita Gutiérrez-Valencia, View ORCID ProfileMarco Fracassetti, View ORCID ProfileEmma L. Berdan, Ignas Bunikis, View ORCID ProfileLucile Soler, View ORCID ProfileJacques Dainat, View ORCID ProfileVerena E. Kutschera, Aleksandra Losvik, Aurélie Désamoré, P. William Hughes, Alireza Foroozani, Benjamin Laenen, View ORCID ProfileEdouard Pesquet, Mohamed Abdelaziz, View ORCID ProfileOlga Vinnere Pettersson, View ORCID ProfileBjörn Nystedt, View ORCID ProfileAdrian Brennan, View ORCID ProfileJuan Arroyo, View ORCID ProfileTanja Slotte
doi: https://doi.org/10.1101/2022.05.27.493681
Juanita Gutiérrez-Valencia
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Marco Fracassetti
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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  • ORCID record for Marco Fracassetti
Emma L. Berdan
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Ignas Bunikis
2Uppsala Genome Center, Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden
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Lucile Soler
3Department of Medical Biochemistry and Microbiology, Uppsala University, National Bioinformatics Infrastructure Sweden (NBIS), Uppsala, Sweden
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  • ORCID record for Lucile Soler
Jacques Dainat
3Department of Medical Biochemistry and Microbiology, Uppsala University, National Bioinformatics Infrastructure Sweden (NBIS), Uppsala, Sweden
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Verena E. Kutschera
4Department of Biochemistry and Biophysics, National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Stockholm University, Solna, Sweden
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  • ORCID record for Verena E. Kutschera
Aleksandra Losvik
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Aurélie Désamoré
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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P. William Hughes
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Alireza Foroozani
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Benjamin Laenen
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Edouard Pesquet
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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Mohamed Abdelaziz
5Department of Genetics, University of Granada, Granada, Spain
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Olga Vinnere Pettersson
2Uppsala Genome Center, Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden
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Björn Nystedt
6Department of Cell and Molecular Biology, National Bioinformatics Infrastructure Sweden (NBIS), Uppsala University, Uppsala, Sweden
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Adrian Brennan
7Department of Biosciences, Durham University, Durham, UK
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Juan Arroyo
8Department of Plant Biology and Ecology, University of Seville, Seville, Spain
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Tanja Slotte
1Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden
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  • ORCID record for Tanja Slotte
  • For correspondence: tanja.slotte@su.se
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Abstract

Supergenes govern balanced polymorphisms in a wide range of systems. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown if hemizygosity is pervasive among distyly S-loci. Here we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes. The chromosome-level genome assembly and detailed characterization of the distyly S-locus in L. tenue will facilitate elucidation of molecular mechanisms underlying the different forms of flowers described by Darwin.

Competing Interest Statement

The authors have declared no competing interest.

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Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level
Juanita Gutiérrez-Valencia, Marco Fracassetti, Emma L. Berdan, Ignas Bunikis, Lucile Soler, Jacques Dainat, Verena E. Kutschera, Aleksandra Losvik, Aurélie Désamoré, P. William Hughes, Alireza Foroozani, Benjamin Laenen, Edouard Pesquet, Mohamed Abdelaziz, Olga Vinnere Pettersson, Björn Nystedt, Adrian Brennan, Juan Arroyo, Tanja Slotte
bioRxiv 2022.05.27.493681; doi: https://doi.org/10.1101/2022.05.27.493681
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Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level
Juanita Gutiérrez-Valencia, Marco Fracassetti, Emma L. Berdan, Ignas Bunikis, Lucile Soler, Jacques Dainat, Verena E. Kutschera, Aleksandra Losvik, Aurélie Désamoré, P. William Hughes, Alireza Foroozani, Benjamin Laenen, Edouard Pesquet, Mohamed Abdelaziz, Olga Vinnere Pettersson, Björn Nystedt, Adrian Brennan, Juan Arroyo, Tanja Slotte
bioRxiv 2022.05.27.493681; doi: https://doi.org/10.1101/2022.05.27.493681

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