Polyploidy, or whole genome duplication, is a common feature among plants, occurring in possibly more than half of all angiosperm species. Decades of research has revealed that polyploidy can have profound impacts on phenotypic, genomic, and epigenetic traits. Some changes associated with polyploidy arise immediately from the “genomic shock” caused by duplicating and combining genomes, while other changes result from long-term evolutionary processes that operate on duplicated and redundant genes and genomes. Within this context, this dissertation specifically explores allopolyploidy (polyploidy involving divergent genomes) and its effects on members of the cotton genus (Gossypium). The work in this dissertation focuses on gene expression evolution, utilizing natural and synthetic Gossypium allopolyploids and a F1 hybrid to characterize the expression changes contributed by various stages of the allopolyploidization process.
From these efforts, we find significant levels of expression evolution among the Gossypium species, which all include a maternal “A-genome” and a paternal “D-genome”. In the course of this research we have revealed several surprising results, for example that genes from the D-genome of the F1 hybrid and allopolyploids are more often over-expressed relative to the A-genome, when they are compared to the ancestral condition, meaning that genomic merger and allopolyplody in Gossypium has the net effect of creating D-genome expression biases. Furthermore, for some genes we find cases where this expression bias has gone to completion, leading to total silencing of expression from one of copies of the merged genomes. We also show evidence that cis-regulatory changes are a primary contributor to expression differences between the A and D Gossypium genomes. Finally, by analyzing linked genes along two genomic locations we find that proximity can play a role in constraining expression evolution, though we also show that this proximity effect is not universally true.
Beyond these unexpected findings, we also capitalized on the well-understood phylogenetic framework of the Gossypium species to place expression evolution in a temporal context. We find that there are immediate effects associated with the genome merger, and that these effects may explain approximately one-quarter of the expression biases found among the natural allotetraploid species, or to put it another way, one-quarter of the expression alterations found in the 1-2 million year old allotetraploids happened immediately upon their formations. Furthermore, among all five natural allotetraploids, we find that expression biases tend to become more extreme, indicating that when maintained in duplicate, the expression profiles of Gossypium genes tend to diverge. Finally, between the five diversified natural Gossypium allotetraploids we find the most extreme expression evolution in G. tomentosum, a wild species endemic to the Hawaiian Islands, followed by G. barbadense and G. hirsutum , the two allotetraploids cottons domesticated for fiber production. These results indicate that natural histories may contribute to expression biases, including domestication and island colonization.