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

Gutiérrez-Valencia, Juanita; Fracassetti, Marco; Berdan, Emma L.; Bunikis, Ignas; Soler, Lucile; Dainat, Jacques; Kutschera, Verena E.; Losvik, Aleksandra; Désamoré, Aurélie; Hughes, P. William; Foroozani, Alireza; Laenen, Benjamin; Pesquet, Edouard; Abdelaziz, Mohamed; Pettersson, Olga Vinnere; Nystedt, Björn; Brennan, Adrian C.; Arroyo, Juan; Slotte, Tanja

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Authors

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

Juan Arroyo

Tanja Slotte



Abstract

Supergenes govern multi-trait-balanced polymorphisms in a wide range of systems; however, our understanding of their origins and evolution remains incomplete. 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 whether hemizygosity is pervasive among distyly S-loci. As hemizygosity has major consequences for supergene evolution and loss, clarifying whether this genetic architecture is shared among distylous species is critical. 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, provide a counterexample to classic inversion-based supergenes, and shed new light on the origin and maintenance of an iconic floral polymorphism.

Citation

Gutiérrez-Valencia, J., Fracassetti, M., Berdan, E. L., Bunikis, I., Soler, L., Dainat, J., …Slotte, T. (2022). Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level. Current Biology, 32(20), 4360-4371. https://doi.org/10.1016/j.cub.2022.08.042

Journal Article Type Article
Acceptance Date Aug 15, 2022
Online Publication Date Sep 9, 2022
Publication Date Oct 24, 2022
Deposit Date Oct 12, 2022
Publicly Available Date Mar 21, 2023
Journal Current Biology
Print ISSN 0960-9822
Publisher Cell Press
Peer Reviewed Peer Reviewed
Volume 32
Issue 20
Article Number E6
Pages 4360-4371
DOI https://doi.org/10.1016/j.cub.2022.08.042

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