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

• Published in: Nature communications Vol. 16; no. 1; pp. 6458 - 14
• Main Authors: Salson, Marine, Duranton, Maud, Huynh, Stella, Mariac, Cédric, Tranchant-Dubreuil, Christine, Orjuela, Julie, Cubry, Philippe, Thuillet, Anne-Céline, Burgarella, Concetta, de Navascués, Miguel, Zekraouï, Leïla, Couderc, Marie, Arribat, Sandrine, Rodde, Nathalie, Barnaud, Adeline, Faye, Adama, Kane, Ndjido, Vigouroux, Yves, Berthouly-Salazar, Cécile
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12.07.2025; Nature Publishing Group; Nature Portfolio
• Subjects: 45; 45/23; 45/43; 631/181/2474; 631/208/182; 631/208/726/649/2157; 631/449/2491; Alleles; Biodiversity; Chromosome 3; Chromosomes; Chromosomes, Plant - genetics; Complementation; Cultivation; Diploids; Genetic diversity; Genetic Variation; Genetics; Genome, Plant - genetics; Genomes; Genomics; Haplotypes; Heterozygote; Heterozygotes; Homozygotes; Humanities and Social Sciences; Inversions; Life Sciences; Local population; Millet; multidisciplinary; Mutation; Pennisetum - genetics; Pennisetum glaucum; Plants genetics; Polymorphism; Population; Population genetics; Population structure; Populations; Populations and Evolution; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-025-61529-z

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. Pseudo-overdominance describes haplotypic combinations of recessive deleterious alleles complement each other and result in enhanced fitness in heterozygotes compared to homozygotes. Here, the authors show the role of pseudo-overdominance in maintaining genetic diversity in populations of cultivated pearl millet.