Evolutionary history and genomic consequences of polyploidization in natural populations of Orychophragmus taibaiensis

Abstract

Polyploidization has occurred throughout the tree of life and is particularly common in plants. Despite its ubiquity, our understanding of the short- and long-term effects and consequences of genome doubling in natural populations remains incomplete. In this study, we identified a novel ploidy-variable species system within the ornamental and industrial oilseed genus Orychophragmus (Brassicaceae), which comprises six species, including diploid and tetraploid cytotypes of Orychophragmus taibaiensis. By integrating population-scale genomic and transcriptomic datasets across the species in this genus, we constructed a robust phylogenetic framework and investigated the divergence and demographic history of O. taibaiensis in comparison to its relatives. Specifically, we characterized the geographical distribution patterns of diploids and tetraploids in natural populations of O. taibaiensis, confirmed the autopolyploid origin of tetraploids, and inferred their origin time relative to diploid counterparts. Our findings further revealed that, following genome doubling, tetraploids accumulated a higher genetic load of deleterious mutations, likely due to relaxed purifying selection facilitated by allelic redundancy. Additionally, genome doubling was associated with pronounced changes in gene expression patterns, with differentially expressed genes evolving under relaxed selective constraints. These results highlight that the initial masking of deleterious mutations, changes in expression regulation, and divergent efficacy of selection likely all contribute to shaping the establishment and evolutionary potential of polyploids.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32000265) and Fundamental Research Funds for the Central Universities (2023SCUNL105) to J.W.

Authors contributions

J.W. conceived and supervised the study. Q.L., C.J., R.W., Y.L., and Y.H. handled the sampling, material collection, and performed experiments. Q.L., Z.W., X. Q., and Z.Z. analyzed the data. Q.L. and J.W. wrote the manuscript with the input from P.K.I and J.L. All authors approved the final version of the manuscript.

Data availability

All data needed to evaluate the conclusions in this study are present in the paper and/or the Supplementary information. The newly generated whole-genome resequencing data and transcriptome data of the samples produced in this study have been deposited in the National Genomics Data Center (https://ngdc.cncb.ac.cn) under the accession number PRJCA035915.

Conflicts of interest statement

The authors declare no competing interests.

Supplementary material

Supplementary material is available at Horticulture Research online.

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