The origin and evolution of cultivated rice and genomic signatures of heterosis for yield traits in super-hybrid rice

Abstract

Unraveling evolutionary history and genomic basis of heterosis is fundamental for advancing rice productivity. We developed a genome-scale phylogeny of Oryzeae by coalescing 39,984 gene trees. Our analysis supports parallel, independent origins and nearly synchronous evolutionary trajectories leading to the subsequent domestication of indica and japonica, evidenced by molecular dating and synonymous substitution rates for syntenic and domestication-associated genes. Our survey of 1,383 gene duplications in ancestor of O. sativa uncovers their roles in vital biological processes, highlighting the significance in environmental adaptability. Additionally, we confirm the lack of hybridization event among subspecies ancestors through gene tree topology and D-statistical analyses. We generated 71.67 GB whole-genome sequencing data for five super-hybrid rice varieties and their progenitors, revealing differential positive selection and genetic exchanges between subspecies, essential for heterosis formation. Crucially, our study underscores the role of non-additive gene expression in heterosis, particularly in genes associated with DNA repair and recombination, which may confer resistance traits. Furthermore, eQTL and de novo mutation analyses identify key developmental and stress response genes, offering targets for enhancing heterosis in rice. Overall, our research reveals crucial insights into the genetics of rice domestication and heterosis, offering a genomic resource to improve rice's agricultural productivity.