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Allopolyploidy has played a major role in plant evolution but its impact on genome diversity and expression patterns remains to be understood. Some studies found important genomic and transcriptomic changes in allopolyploids, whereas others detected a strong parental legacy and more subtle changes. The allotetraploid C.bursa-pastoris originated around 100,000 years ago and one could expect the genetic polymorphism of the two subgenomes to follow similar trajectories and their transcriptomes to start functioning together. To test this hypothesis, we sequenced the genomes and the transcriptomes (three tissues) of allotetraploid C.bursa-pastoris and its parental species, the outcrossing C.grandiflora and the self-fertilizing C.orientalis. Comparison of the divergence in expression between subgenomes, on the one hand, and divergence in expression between the parental species, on the other hand, indicated a strong parental legacy with a majority of genes exhibiting a conserved pattern and cis-regulation. However, a large proportion of the genes that were differentially expressed between the two subgenomes, were also under trans-regulation reflecting the establishment of a new regulatory pattern. Parental dominance varied among tissues: expression in flowers was closer to that of C.orientalis and expression in root and leaf to that of C.grandiflora. Since deleterious mutations accumulated preferentially on the C.orientalis subgenome, the bias in expression towards C.orientalis observed in flowers indicates that expression changes could be adaptive and related to the selfing syndrome, while biases in the roots and leaves towards the C.grandiflora subgenome may be reflective of the differential genetic load.

Data associated with the paper. Abstract: Allopolyploidy is generally perceived as a major source of evolutionary novelties and as an instantaneous way to create isolation barriers. However, we do not have a clear understanding of how two subgenomes evolve and interact once they have fused in an allopolyploid species nor how isolated they are from their relatives. Here, we address these questions by analyzing genomic and transcriptomic data of allotetraploid Capsella bursa-pastoris in three differentiated populations, Asia, Europe, and the Middle East. We phased the two subgenomes, one descended from the outcrossing and highly diverse Capsella grandiflora (CbpCg) and the other one from the selfing and genetically depauperate Capsella orientalis (CbpCo). For each subgenome, we assessed its relationship with the diploid relatives, temporal changes of effective population size (Ne), signatures of positive and negative selection, and gene expression patterns. In all three regions, Ne of the two subgenomes decreased gradually over time and the CbpCo subgenome accumulated more deleterious changes than CbpCg . There were signs of widespread admixture between C. bursa-pastoris and its diploid relatives. The two subgenomes were impacted differentially depending on geographic region suggesting either strong interploidy gene flow or multiple origins of C. bursa-pastoris. Selective sweeps were more common on the CbpCg subgenome in Europe and the Middle East, and on the CbpCo subgenome in Asia. In contrast, differences in expression were limited with the CbpCg subgenome slightly more expressed than CbpCo in Europe and the Middle-East. In summary, after more than 100,000 generations of co-existence, the two subgenomes of C. bursa-pastoris still retained a strong signature of parental legacy but their evolutionary trajectory strongly varied across geographic regions.

Additional file 1: Figure S1. Seurat snRNAseq workflow quality control statistics. From left to right, first figure reports the number of expressed genes per cell, second figure reports the number of UMIs (library size) per cell, third figure shows the fraction of reads mapped to mitochondrial genes per cell. Figure S2. The initial average sequencing depth of 35 million paired-end (PE) reads were ´down-sampled´ and mean square errors between the ATPase and totRNAseq predicted fractions of Type I fibers were calculated. Figure S3. Principal Component Analysis (PCA) plot of gene exppression from human skeletal muscle snRNAseq colored by the cluster annotation, see Figure 1A, obtained from the Louvain clustering on the number of significant principal components (according to Seurat workflow). Figure S4. (a) Principal Component Analysis (PCA) plot, and (b) tSNE plot of gene expression from human skeletal muscle snRNAseq colored by the cell cycle annotation obtained from the CellCycleScoring function from Seurat workflow. No obvious cluster formation based on the cell cycle can be observed from neither the PCA nor the tSNE plot.