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Pooled Single-Molecule transcriptomics identifies a giant gene under balancing selection in sunflower

View ORCID ProfileHélène Badouin, Marie-Claude Boniface, Nicolas Pouilly, Anne-Laure Fuchs, Felicity Vear, View ORCID ProfileNicolas B. Langlade, View ORCID ProfileJérôme Gouzy, View ORCID ProfileStéphane Muños
doi: https://doi.org/10.1101/2021.03.17.435796
Hélène Badouin
1Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, F-69622 Villeurbanne, France
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  • For correspondence: helene.badouin@univ-lyon1.fr
Marie-Claude Boniface
2LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
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Nicolas Pouilly
2LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
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Anne-Laure Fuchs
1Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, F-69622 Villeurbanne, France
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Felicity Vear
2LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
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Nicolas B. Langlade
2LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
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Jérôme Gouzy
2LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
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Stéphane Muños
2LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
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Summary

Genes under balancing selection control phenotypes such as immunity, color or sex, but are difficult to identify. Self-incompatibility genes are under negative frequency-dependent selection, a special case of balancing selection, with up to 30 to 50 alleles segregating per population. We developed a method based on pooled Single-Molecule transcriptomics to identify balanced polymorphisms expressed in tissues of interest. We searched for multi-allelic, non-recombining genes causing self-incompatibility in wild sunflower (Helianthus annuus). A diversity scan in pistil identified a gene, Ha7650b,that displayed balanced polymorphism and colocalized with a quantitative trait locus for self-incompatibility. Unexpectedly, Ha7650b displayed gigantism (400 kb), which was caused by increase in intron size as a consequence of suppressed recombination. Ha7650b emerged after a whole-genome duplication (29 millions years ago) followed by tandem duplications and neofunctionalisation. Ha7650b shows expression, genetic location, genomic neighbourhood and predicted function that provide strong evidence that it is involved in self-incompatibility. Pooled Single-Molecule transcriptomics is an affordable and powerful new method that makes it possible to identify diversity and structural outliers simultaneously. It will allow a breakthrough in the discovery of self-incompatibility genes and other expressed genes under balancing selection.

Competing Interest Statement

The authors have declared no competing interest.

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 March 19, 2021.
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Pooled Single-Molecule transcriptomics identifies a giant gene under balancing selection in sunflower
Hélène Badouin, Marie-Claude Boniface, Nicolas Pouilly, Anne-Laure Fuchs, Felicity Vear, Nicolas B. Langlade, Jérôme Gouzy, Stéphane Muños
bioRxiv 2021.03.17.435796; doi: https://doi.org/10.1101/2021.03.17.435796
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Pooled Single-Molecule transcriptomics identifies a giant gene under balancing selection in sunflower
Hélène Badouin, Marie-Claude Boniface, Nicolas Pouilly, Anne-Laure Fuchs, Felicity Vear, Nicolas B. Langlade, Jérôme Gouzy, Stéphane Muños
bioRxiv 2021.03.17.435796; doi: https://doi.org/10.1101/2021.03.17.435796

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