Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant

Abstract

Polyploidy is an important driver of eukaryotic evolution, evident in many animals, fungi, and plants. One consequence of polyploidy is subfunctionalization, in which the ancestral expression profile becomes partitioned among duplicated genes (termed homoeologs). Subfunctionalization appears to be a common phenomenon insofar as it has been studied, at the scale of organs. Here, we use a high-resolution methodology to investigate the expression of thousands of pairs of homoeologs during the development of a single plant cell, using as a model the seed trichomes (“cotton fiber”) of allopolyploid (containing “A” and “D” genomes) cotton (Gossypium). We demonstrate that ≈30% of the homoeologs are significantly A- or D-biased at each of three time points studied during fiber development. Genes differentially biased toward the A or D genome belong to different biological processes, illustrating the functional partitioning of genomic contributions during cellular development. Interestingly, expression of the biased genes was shifted strongly toward the agronomically inferior D genome. Analyses of homoeologous gene expression during development of this cell showed that one-fifth of the genes exhibit changes in A/D ratios, indicating that significant alteration in duplicated gene expression is fairly frequent even at the level of development and maturation of a single cell. Comparing changes in homoeolog expression in cultivated versus wild cotton showed that most homoeolog expression bias reflects polyploidy rather than domestication. Evidence suggests, however, that domestication may increase expression bias in fibers toward the D genome, potentially implicating D-genome recruitment under human selection during domestication.