Biological pathway expression complementation contributes to biomass heterosis in Arabidopsis

Abstract

Significance Heterosis, referring to the better performance of an F1 hybrid compared with its parents, has been greatly exploited in agriculture to improve yield. Nevertheless, our understanding of its genetic and molecular mechanism has remained limited. We investigated the temporally dynamic phenotypes and transcriptomes during early seedling development in two Arabidopsis ecotypes together with their hybrid and unveiled differences in the transcriptional regulatory network between the hybrid and parents, orchestrating the hybrid growth vigor. Moreover, we found complementary high-parent expression in the hybrid between the network hub genes involved in photosynthesis and cell cycle. Our findings provide molecular-level evidence that dominant expression complementation between genes involved in two fundamental biological pathways contributes to heterosis. The mechanisms underlying heterosis have long remained a matter of debate, despite its agricultural importance. How changes in transcriptional networks during plant development are relevant to the continuous manifestation of growth vigor in hybrids is intriguing and unexplored. Here, we present an integrated high-resolution analysis of the daily dynamic growth phenotypes and transcriptome atlases of young Arabidopsis seedlings (parental ecotypes [Col-0 and Per-1] and their F1 hybrid). Weighted gene coexpression network analysis uncovered divergent expression patterns between parents of the network hub genes, in which genes related to the cell cycle were more highly expressed in one parent (Col-0), whereas those involved in photosynthesis were more highly expressed in the other parent (Per-1). Notably, the hybrid exhibited spatiotemporal high-parent–dominant expression complementation of network hub genes in the two pathways during seedling growth. This suggests that the integrated capacities of cell division and photosynthesis contribute to hybrid growth vigor, which could be enhanced by temporal advances in the progression of leaf development in the hybrid relative to its parents. Altogether, this study provides evidence of expression complementation between fundamental biological pathways in hybrids and highlights the contribution of expression dominance in heterosis.