Interplay between large low-recombining regions and pseudo-overdominance in a plant genome

Marine Salson, Maud Duranton, Stella Huynh, Cédric Mariac, Christine Tranchant-Dubreuil, Julie Orjuela, Philippe Cubry, Anne-Céline Thuillet, Concetta Burgarella, Miguel Navascués, Leïla Zekraouï, Marie Couderc, Sandrine Arribat, Nathalie Rodde, Adeline Barnaud, Adama Faye, Ndjido Kane, Yves Vigouroux () and Cécile Berthouly-Salazar ()
Additional contact information
Marine Salson: CIRAD
Maud Duranton: CIRAD
Stella Huynh: CIRAD
Cédric Mariac: CIRAD
Christine Tranchant-Dubreuil: CIRAD
Julie Orjuela: CIRAD
Philippe Cubry: CIRAD
Anne-Céline Thuillet: CIRAD
Concetta Burgarella: Uppsala University
Miguel Navascués: University of Montpellier
Leïla Zekraouï: CIRAD
Marie Couderc: CIRAD
Sandrine Arribat: INRAE
Nathalie Rodde: INRAE
Adeline Barnaud: CIRAD
Adama Faye: ISRA
Ndjido Kane: ISRA
Yves Vigouroux: CIRAD
Cécile Berthouly-Salazar: CIRAD

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract To what extent overdominance might contribute to the maintenance of genetic diversity within genomes is still an ongoing research question. Pseudo-overdominance created by the complementation of deleterious alleles in heterozygotes has recently become a subject of particular interest. Simulations and theory suggest that pseudo-overdominance may occur in low recombining regions. Here, we conduct a comprehensive investigation of large low-recombining (LLR) regions in cultivated populations of pearl millet, an outcrossing diploid African cereal. We examine seven large regions ranging from 5 to 88 Mb and six of them are pericentromeric. These LLR regions exhibit an excess of heterozygotes, a distinctive hallmark of overdominance. They display a tendency toward a higher diversity and a larger ratio of non-synonymous and deleterious variants. We conduct a more in-depth study of the largest 88 Mb region, identified on chromosome 3. Interestingly, haplotypes of this region have been introgressed from wild relatives. Using long read sequencing, we confirm their strong divergence and the presence of inversions across one of them. One of the haplotypes seems to be highly deleterious in the homozygous state. A total of 17% of the cultivated pearl millet genome exhibit a local population structure suggestive of overdominance or possibly pseudo-overdominance. Our empirical results contribute to the accumulation of knowledge, which will enhance our understanding of the potential role of overdominance or pseudo-overdominance in maintaining genetic diversity, particularly in low recombining regions.

Date: 2025
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DOI: 10.1038/s41467-025-61529-z

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