Purifying selection on deleterious variants affected by the combination of subgenomes and gene expression in bread wheat

Authors: HALSTEAD-NUSSLOCH, GWYNETH - University Of Zurich; OKADA, MOEKO - University Of Zurich; HABERER, GEORG - German Research Center For Environmental Health; LUX, THOMAS - German Research Center For Environmental Health; ISLAM, A S M FARIDUL - Texas A&M University Institute For Advancing Health Through Agriculture; HATAKEYAMA, MASAOMI - University Of Zurich; BRISKINE, ROMAN - University Of Zurich; WHITE, BEN - Earlham Institute; HALL, ANTHONY - Earlham Institute; POZNIAK, CURTIS - University Of Saskatchewan; SPANNAGL, MANUEL - German Research Center For Environmental Health; Paape, Timothy; SHIMIZU, KENTARO - University Of Zurich

Submitted to: Cell Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2025
Publication Date: 1/26/2026
Citation: Halstead-Nussloch, G., Okada, M., Haberer, G., Lux, T., Islam, A., Hatakeyama, M., Briskine, R., White, B., Hall, A., Pozniak, C., Spannagl, M., Paape, T.D., Shimizu, K.K. 2026. Purifying selection on deleterious variants affected by the combination of subgenomes and gene expression in bread wheat. Cell Reports. Article 116785. https://doi.org/10.1016/j.celrep.2025.116785.
DOI: https://doi.org/10.1016/j.celrep.2025.116785

Interpretive Summary: Wheat is the most broadly grown crop species on earth, but the complex allopolyploid genome (~15 Gb) has been a major obstacle to studying genetic diversity and gene expression. The 10+ Wheat Genome Project has revolutionized genomic studies of wheat. In 2020, we reported the de novo chromosome-scale assemblies of 10 worldwide cultivars. The pan-transcriptome data provided high-quality de novo annotation of the wheat pan-genome and highlighted diversity in the transcriptome. Here we took advantage of the integration of the genome-wide polymorphism data and pan-transcriptome data. We quantified the strength of selection on deleterious variants, a long-standing issue in biology and breeding, but much less is known in wheat compared with major diploid crop species such as rice, maize, and cassava. To our knowledge, this is the first study to report a significant interaction effect of the subgenome and tissue-specific expression on selection. We showed that homeologous genes that are expressed highly in root tissues in the D subgenome experienced stronger purifying selection than those expressed in other tissues. Our results suggested the environmental adaptation after polyploidization. Furthermore, our study informs the target of future breeding to mitigate the effect of deleterious variants as a major goal of breeding through genome editing and hybrid breeding.

Technical Abstract: The genome-wide pattern of purifying selection on deleterious variants has attracted broad interest in breeding and evolutionary biology. Little is known about purifying selection in bread wheat, an allohexaploid species with potential functional redundancy of duplicated homeologs. Using the de novo annotated assemblies and transcriptome data of the 10+ wheat genome projects, we examined the pattern of polymorphisms and the effect of both subgenome and gene expression on estimates of purifying selection. Despite the presence of introgressed chromosomal segments in modern cultivars, purifying selection was observed, consistent with the efficacy of hybrid breeding in wheat. Interestingly, strong purifying selection was observed in the category of genes that are highly expressed in root tissues and are in the D subgenome, which suggests environmental adaptation after allopolyploidization. We suggest that the interaction of expressed tissues and subgenomes will inform the targets of future breeding to mitigate the effects of deleterious variants in bread wheat.