The causes and consequences of subgenome dominance in hybrids and recent polyploids

Ancient tetraploidies are found throughout the eukaryotes. After duplication, one copy of each duplicate gene pair tends to be lost (fractionate). For all studied tetraploidies, the loss of duplicated genes, known as homeologs, homoeologs, ohnologs, or syntenic paralogs, is uneven between duplicate regions. In maize, a species that experienced a tetraploidy 5-12 million years ago, we show that in addition to uneven ancient gene loss, the two complete genomes contained within maize are differentiated by ongoing fractionation among diverse inbreds as well as by a pattern of overexpression of genes from the genome that has experienced less gene loss. These expression differences are consistent over a range of experiments quantifying RNA abundance in different tissues. We propose that the universal bias in gene loss between the genomes of this ancient tetraploid, and perhaps all tetraploids, is the result of selection against loss of the gene responsible for the majority of total expression for a duplicate gene pair. Although the tetraploidy of maize is ancient, biased gene loss and expression continue today and explain, at least in part, the remarkable genetic diversity found among modern maize cultivars.

Transposable elements (TEs) are ubiquitous genomic parasites. The deleterious consequences of the presence and activity of TEs have fueled debate about the evolutionary forces countering their expansion. Purifying selection is thought to purge TE insertions from the genome, and TE sequences are targeted by hosts for epigenetic silencing. However, the interplay between epigenetic and evolutionary forces countering TE expansion remains unexplored. Here we analyze genomic, epigenetic, and population genetic data from Arabidopsis thaliana to yield three observations. First, gene expression is negatively correlated with the density of methylated TEs. Second, the signature of purifying selection is detectable for methylated TEs near genes but not for unmethylated TEs or for TEs far from genes. Third, TE insertions are distributed by age and methylation status, such that older, methylated TEs are farther from genes. Based on these observations, we present a model in which host silencing of TEs near genes has deleterious effects on neighboring gene expression, resulting in the preferential loss of methylated TEs from gene-rich chromosomal regions. This mechanism implies an evolutionary tradeoff in which the benefit of TE silencing imposes a fitness cost via deleterious effects on the expression of nearby genes.