Genomic architecture of biomass heterosis in Arabidopsis

Significance

Heterosis, the phenotypic superiority of a hybrid over its parents, has been extensively exploited in agriculture to improve biomass and yield. Despite its great agricultural importance, the genetic components underlying heterosis remain largely unclear. Here, we characterize the genomic architecture of heterosis in Arabidopsis that have not undergone domestication and identify hundreds of genetic loci that collectively contribute to biomass heterosis using genome-wide association studies. The functional investigation of candidate genes and transcriptomic analysis in representative hybrids suggest that the accumulation of superior genes involved in basic biological processes and the repression of stimulus-responsive genes in hybrids contribute to biomass heterosis in Arabidopsis, thus providing a comprehensive understanding of the genetic bases of heterosis in natural populations of plant species.

Abstract

Heterosis is most frequently manifested by the substantially increased vigorous growth of hybrids compared with their parents. Investigating genomic variations in natural populations is essential to understand the initial molecular mechanisms underlying heterosis in plants. Here, we characterized the genomic architecture associated with biomass heterosis in 200 Arabidopsis hybrids. The genome-wide heterozygosity of hybrids makes a limited contribution to biomass heterosis, and no locus shows an obvious overdominance effect in hybrids. However, the accumulation of significant genetic loci identified in genome-wide association studies (GWAS) in hybrids strongly correlates with better-parent heterosis (BPH). Candidate genes for biomass BPH fall into diverse biological functions, including cellular, metabolic, and developmental processes and stimulus-responsive pathways. Important heterosis candidates include WUSCHEL, ARGOS, and some genes that encode key factors involved in cell cycle regulation. Interestingly, transcriptomic analyses in representative Arabidopsis hybrid combinations reveal that heterosis candidate genes are functionally enriched in stimulus-responsive pathways, including responses to biotic and abiotic stimuli and immune responses. In addition, stimulus-responsive genes are repressed to low-parent levels in hybrids with high BPH, whereas middle-parent expression patterns are exhibited in hybrids with no BPH. Our study reveals a genomic architecture for understanding the molecular mechanisms of biomass heterosis in Arabidopsis, in which the accumulation of the superior alleles of genes involved in metabolic and cellular processes improve the development and growth of hybrids, whereas the overall repressed expression of stimulus-responsive genes prioritizes growth over responding to environmental stimuli in hybrids under normal conditions.