Pervasive Under-Dominance in Gene Expression Underlying Emergent Growth Trajectories inArabidopsis thalianaHybrids

Abstract

Complex traits, such as growth and fitness, are typically controlled by a very large number of variants, which can interact in both additive and non-additive fashion. In an attempt to gauge the relative importance of both types of genetic interactions, we have turned to hybrids, which provide a facile means for creating many novel allele combinations. We focused on the interaction between alleles of the same locus and performed a transcriptomic study involving 141 random crosses between different accessions of the plant model speciesArabidopsis thaliana. Additivity is rare, consistently observed for only about 300 genes enriched for roles in stress response and cell death. Regulatory rare-allele burden affects the expression level of these genes but does not correlate with F1rosette size. Non-additive gene expression in F1hybrids is much more common, with the vast majority of genes (over 90%) being expressed below parental average. Unlike in the additive genes, regulatory rare-allele burden in the non-additive gene set is strongly correlated with F1rosette size, even though it only mildly covary with the expression level of these genes. Our study underscores under-dominance as the predominant gene action associated with emergence of rosette growth trajectories in theA. thalianahybrid model. Our work lays the foundation for understanding molecular mechanisms and evolutionary forces that lead to dominance complementation of rare regulatory alleles.