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The rice production system in Japan is changing due to the aging of rice farmers, shortage of labor, mechanization, and increase of large-scale rice fields and increased application of direct sowing, all of which contribute to the lack of sophisticated weed management practices. Because the changing production system has not improved and likely worsened weed management practices, weedy rice (Oryza sativa L.) has become a serious threat to rice production in Japan. We analyzed weedy rice accessions from Nagano, the central part of Japan, and other rice accessions to elucidate the origin of this weedy rice using a whole-genome single nucleotide polymorphism (SNP) array. For developing sustainable weedy rice management practices, the elucidation of the origin of re-emerging weedy rice is crucial. Population genetic analysis indicated that weedy rice in Nagano was phylogenetically independent from the local red rice cultivar with low genetic diversity. Past and recently re-emerging weedy rice ecotypes in Nagano shared a similar genetic background which implies the evolution of weedy rice by severe natural selection. Window-based FST and selection sweep analysis revealed the divergence of some of the known key domestication-related genes, such as shattering gene sh4 and qsh1, of weedy rice from domesticated rice cultivars. [ABSTRACT FROM AUTHOR]