A weed x ancestral cultivar cross identifies evolutionarily relevant weediness QTLs

Authors: LI, XIANG - University Of Massachusetts, Amherst; ZHANG, SHULIN - Mianyang Normal University; LOWEY, DANIEL - University Of Massachusetts, Amherst; HISSAM, CARTER - University Of Massachusetts, Amherst; CLEVENGER, JOSH - Hudsonalpha Institute For Biotechnology; Jia, Yulin; CAICEDO, ANA - University Of Massachusetts, Amherst

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/6/2023
Publication Date: 10/20/2023
Citation: Li, X., Zhang, S., Lowey, D., Hissam, C., Clevenger, J., Jia, Y., Caicedo, A.L. 2023. A weed x ancestral cultivar cross identifies evolutionarily relevant weediness QTLs. Molecular Ecology. https://doi.org/10.1111/mec.17172.
DOI: https://doi.org/10.1111/mec.17172

Interpretive Summary: Weedy rice is a weedy relative of cultivated rice that poses a significant threat to crop production by competing with crops and causes considerable yield loss. The annual yield loss in the United States alone due to weedy rice infestations could feed approximately 12 million people. Weedy rice has evolved independently from various cultivated rice groups through a process of de-domestication, during which it has evolved a suite of traits collectively known as the "agricultural weed syndrome." These traits include rapid growth, high nutrient use efficiency, seed dormancy, seed dispersal, and herbicide resistance. However, the genetic basis underlying these weediness traits remains to be fully elucidated. To address this knowledge gap, we developed a novel mapping population through a cross between BHA weedy rice and aus cultivars to explore the genetic mechanisms underpinning three key weedy traits: flowering time, plant height, and seed shattering. A significant novelty of this study is that we took into consideration the phylogenetic relationships between the parents of the cross. We leveraged population genomic data to identify regions under selection and overlapping these selective sweeps with quantitative trait loci (QTLs) could enable us to identify the QTLs that contribute to the evolution of weediness traits. We performed QTL mapping using a combination of bulked segregant analysis and high-throughput whole-genome re-sequencing, resulting in a more time-efficient and accurate method. The loci and candidate genes identified not only provide insights into the genetic basis of evolutionary mechanisms of these traits but also have the potential to inform weed management strategies and help identify rice varieties that are more likely to produce weedy descendants.

Technical Abstract: Weedy rice (Oryza spp.) is a weedy relative of the cultivated rice that competes with the crop and causes significant production loss. The BHA (Blackhull Awned) U.S. weedy rice group has evolved from aus cultivated rice and differs from its ancestors in several important weediness traits, including flowering time, plant height, and seed shattering. Prior attempts to determine the genetic basis of weediness traits in plants using linkage mapping approaches have not often considered weed origins. However, the timing of divergence between crossed parents can affect the detection of Quantitative Trait Loci (QTL) relevant to the evolution of weediness. Here, we used a QTL-seq approach that combines bulked segregant analysis and high-throughput whole genome re-sequencing to map the three important weediness traits in an F2 population derived from a cross between BHA weedy rice with an ancestral aus cultivar. We compared these QTLs with those previously detected in a cross of BHA with a more distantly related crop, indica. We identified multiple QTLs that overlapped with regions under selection during the evolution of weedy BHA rice, and some candidate genes possibly underlying the evolution weediness traits in BHA. These include OsNF-YB9 and DTH2, which may explain the weed’s later flowering time; OsGH3.8, which possibly account for the group's greater height; and SHAT1, which could contribute to high seed shattering in BHA. We show that QTLs detected with ancestor-descendant crosses are more likely to be involved in the evolution of weediness traits, than those detected from crosses of more diverged taxa.