Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids

Whole-genome duplications happen repeatedly in a typical flowering plant lineage. Following most ancient tetraploidies, the two subgenomes are distinguishable because one subgenome, the dominant subgenome, tends to have more genes than the other subgenome. Additionally, among retained pairs, the gene on the dominant subgenome tends to be expressed more than its recessive homeolog. Using comparative genomics, we show that genome dominance is heritable. The dominant subgenome of one postpolyploidy event remains dominant through a subsequent polyploidy event. We show that transposon-derived 24-nt RNAs target and cover the upstream region of retained genes preferentially when located on the recessive subgenome, and with little regard for a gene's level of expression. We hypothesize that small RNA (smRNA)-mediated silencing of transposons near genes causes position-effect down-regulation. Unlike 24-nt smRNA coverage, transposon coverage tracks gene expression, so not all transposons behave identically. We propose that successful ancient tetraploids begin as wide crosses between two lines, each evolved for different tradeoffs between transposon silencing and negative position effects on gene expression. We hypothesize that following a chaotic wide-cross/new tetraploid period, genes acquire their new expression balances based on differences in transposon coverage in the parents. We envision patches of silenceable transposon as quantitative cis-regulators of baseline transcription rate. Attractive solutions to heterosis and the C-value paradox are mentioned.