Key Roles of De-Domestication and Novel Mutation in Origin and Diversification of Global Weedy Rice

SIMPLE SUMMARY: Weedy rice is a noxious weed infesting rice fields worldwide and causing tremendous losses of rice yield and quality. The control of this conspecific weed is difficult owing to abundant genetic diversity associated with its complex origins and evolution. Applying different molecular methods, we demonstrate the multiple origins of weedy rice with the major pathway from its cultivar progenitors. The origin and diversification of weedy rice are also closely associated with differentiation of indica-japonica rice varieties. In addition, novel mutations are identified, which may promote continued evolution and genetic diversity of weedy rice. Knowledge generated from this study provides deep insights into the origin and evolution of conspecific weeds, in addition to the design of effective measures to control these weeds. ABSTRACT: Agricultural weeds pose great challenges to sustainable crop production, owing to their complex origins and abundant genetic diversity. Weedy rice (WD) infests rice fields worldwide causing tremendous losses of rice yield/quality. To explore WD origins and evolution, we analyzed DNA sequence polymorphisms of the seed shattering genes (sh4 and qsh1) in weedy, wild, and cultivated rice from a worldwide distribution. We also used microsatellite and insertion/deletion molecular fingerprinting to determine their genetic relationship and structure. Results indicate multiple origins of WD with most samples having evolved from their cultivated progenitors and a few samples from wild rice. WD that evolved from de-domestication showed distinct genetic structures associated with indica and japonica rice differentiation. In addition, the weed-unique haplotypes that were only identified in the WD samples suggest their novel mutations. Findings in this study demonstrate the key role of de-domestication in WD origins, in which indica and japonica cultivars stimulated further evolution and divergence of WD in various agroecosystems. Furthermore, novel mutations promote continued evolution and genetic diversity of WD adapting to different environments. Knowledge generated from this study provides deep insights into the origin and evolution of conspecific weeds, in addition to the design of effective measures to control these weeds.