Cis-trans controls and regulatory novelty accompanying allopolyploidization

Allopolyploidy is a prevalent process in plants, having important physiological, ecological and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression-level dominance and revamping of co-expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis-trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele-specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher-order effects that impact gene expression. Finally, we suggest that the extended cis-trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome-wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy.