Towards the new normal: Transcriptomic convergence and genomic legacy of the two subgenomes of an allopolyploid weed ( Capsella bursa-pastoris)

摘要

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. Author summary Most plant species have a polyploid at some stage of their ancestry. Polyploidy, genome doubling through either multiple copies of a single species or through genomes of different species coming into the same nucleus, is therefore a crucial step in plant evolution. Understanding its impact on basic biological functions is thus a matter of interest. Shepherd’s purse ( Capsella bursa-pastoris ) is a major weed that appeared about 100,000 years ago through hybridization of two diploid species of the same genus. In the present project, we measured genetic diversity and analyzed gene expression patterns in flowers, roots, and leaves of C. bursa-pastoris individuals as well as in its two parental species, the outcrossing C. grandiflora and the self-fertilizing C. orientalis . Our data shows that, after 100,000 generations of evolution, the origin of the two subgenomes can still be seen: the genome inherited from C. grandiflora still differs from the one inherited from self-fertilizing C. orientalis . However, there are also signs that the two genomes have started to work together and are jointly regulated, and the way expression pattern varied across the three tissues indicates that the evolution of gene expression was adaptive.