Gene balance predicts transcriptional responses immediately following ploidy change in Arabidopsis thaliana

Abstract

The Gene Balance Hypothesis postulates that there is selection on gene copy number (gene dosage) to preserve stoichiometric balance among interacting proteins. This presupposes that gene product abundance is governed by gene dosage, and that the way in which gene product abundance is governed by gene dosage is consistent for all genes in a dosage-sensitive network or complex. Gene dosage responses, however, have rarely been quantified and the available data suggest that they are highly variable. We sequenced the transcriptomes of two synthetic autopolyploid accessions of Arabidopsis thaliana and their diploid progenitors, as well as one natural tetraploid and its synthetic diploid produced via haploid induction, to estimate transcriptome size and gene dosage responses immediately following ploidy change. We demonstrate that overall transcriptome size does not exhibit a simple doubling in response to genome doubling, and that individual gene dosage responses are highly variable in all three accessions, indicating that expression is not strictly coupled with gene dosage. Nonetheless, putatively dosage-sensitive gene groups (GO terms, metabolic networks, gene families, and predicted interacting protein pairs) exhibit both smaller and more coordinated dosage responses than do putatively dosage-insensitive gene groups, suggesting that constraints on dosage balance operate immediately following whole genome duplication. This supports the hypothesis that duplicate gene retention patterns are shaped by selection to preserve dosage balance.