Population Genomic Analysis and De Novo Assembly Reveal the Origin of Weedy Rice as an Evolutionary Game

Abstract Crop weediness, especially that of weedy rice ( Oryza sativa f . spontanea ), remains mysterious. Weedy rice possesses robust ecological adaptability; however, how this strain originated and gradually formed proprietary genetic features remains unclear. Here, we demonstrate that weedy rice at Asian high latitudes ( WRAH ) is phylogenetically well defined and possesses unselected genomic characteristics in many divergence regions between weedy and cultivated rice. We also identified novel quantitative trait loci underlying weedy-specific traits, and revealed that a genome block on the end of chromosome 1 is associated with rice weediness. To identify the genomic modifications underlying weedy rice evolution, we generated the first de novo assembly of a high-quality weedy rice genome (WR04-6), and conducted a comparative genomics study between WR04-6 with other rice reference genomes. Multiple lines of evidence, including the results of demographic scenario comparisons, suggest that differentiation between weedy rice and cultivated rice was initiated by genetic improvement of cultivated rice and that the essence of weediness arose through semi-domestication. A plant height model further implied that the origin of WRAH can be modeled as an evolutionary game and indicated that strategy-based selection driven by fitness shaped its genomic diversity.