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Summary Root system architecture (RSA) is a critical aspect of plant growth and competitive ability. Here we used two independently evolved strains of weedy rice, a de‐domesticated form of rice, to study the evolution of weed‐associated RSA traits and the extent to which they evolve through shared or different genetic mechanisms. We characterised 98 two‐dimensional and three‐dimensional RSA traits in 671 plants representing parents and descendants of two recombinant inbred line populations derived from two weed × crop crosses. A random forest machine learning model was used to assess the degree to which root traits can predict genotype and the most diagnostic traits for doing so. We used quantitative trait locus (QTL) mapping to compare genetic architecture between the weed strains. The two weeds were distinguishable from the crop in similar and predictable ways, suggesting independent evolution of a ‘weedy’ RSA phenotype. Notably, comparative QTL mapping revealed little evidence for shared underlying genetic mechanisms. Our findings suggest that despite the double bottlenecks of domestication and de‐domestication, weedy rice nonetheless shows genetic flexibility in the repeated evolution of weedy RSA traits. Whereas the root growth of cultivated rice may facilitate interactions among neighbouring plants, the weedy rice phenotype may minimise below‐ground contact as a competitive strategy.

Weedy relatives of crop species infest agricultural fields worldwide, reducing harvests and threatening global food security. These weeds can potentially evolve and adapt through gene flow from both domesticated crop varieties and reproductively compatible wild relatives. We studied populations of weedy rice in Thailand to investigate the role of introgression from cultivated and wild rice in their evolution. We examined 2 complementary sources of genetic data: allelic variation at 3 rice domestication genes (Bh4, controlling hull color; Rc, controlling pericarp color and seed dormancy; and sh4, controlling seed shattering), and 12 previously published SSR markers. Sampling spanned 3 major rice growing regions in Thailand (Lower North, North East, and Central Plain) and included 124 cultivated rice accessions, 166 weedy rice accessions, and 98 wild rice accessions. Weedy rice strains were overall closely related to the cultivated varieties with which they co-occur. Domestication gene data revealed potential adaptive introgression of sh4 shattering alleles from wild rice. Introgression of potentially maladaptive rc crop alleles (conferring reduced dormancy) was also detected, with the frequency of the crop allele highest in northern populations. Although SSR markers also indicated introgression into weed populations from wild and cultivated rice, there was little overlap with domestication genes in the accessions showing admixed ancestry. This suggests that much of the introgression we detected at domestication genes most likely reflects past introgression rather than recent gene flow. This finding has implications for understanding long-term gene flow dynamics between rice and its weedy and wild relatives, including potential risks of transgene escape.

Weedy rice is a close relative of cultivated rice that devastates rice productivity worldwide. In the southern United States, two distinct strains have been historically predominant, but the 21st century introduction of hybrid rice and herbicide resistant rice technologies has dramatically altered the weedy rice selective landscape. Here, we use whole-genome sequences of 48 contemporary weedy rice accessions to investigate the genomic consequences of crop-weed hybridization and selection for herbicide resistance. We find that population dynamics have shifted such that most contemporary weeds are now crop-weed hybrid derivatives, and that their genomes have subsequently evolved to be more like their weedy ancestors. Haplotype analysis reveals extensive adaptive introgression of cultivated alleles at the resistance gene ALS, but also uncovers evidence for convergent molecular evolution in accessions with no signs of hybrid origin. The results of this study suggest a new era of weedy rice evolution in the United States.

PREMISE During plant domestication, traits can be subject to a variety of types of selection, ranging from strong directional selection for traits such as seed or fruit size to diversifying selection for traits like color or flavor. These types of selection interact with other evolutionary processes including genetic bottlenecks and interspecific gene flow to generate different levels of genetic diversity across the genome and at target genes in domesticated lineages, but little is known about the impacts of these processes in perennial fruit crops. METHODS We used sequence capture by hybridization to examine patterns of diversity at a suite of candidate domestication and anonymous background genes in domesticated apple (Malus ×domestica) in comparison to its wild relatives Malus sieversii and Malus orientalis. RESULTS We found no change in average diversity at these candidate domestication genes across the three species. However, a subset of the genes did exhibit patterns of very high or very low diversity in M. ×domestica compared to its progenitor, M. sieversii. Of the genes with characterized function, the low‐diversity genes mainly contributed to fruit quality traits like color and flavor, predicted to be under conscious, directional selection relatively late in the domestication process, while the high‐diversity genes included a variety of functions. CONCLUSIONS Overall, these results are consistent with predictions based on the likely timing and nature of selection during domestication and open new avenues for understanding genes with high diversity in a perennial crop compared to its wild relatives.