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.

Using demographic model selection to untangle allopatric divergence and diversification mechanisms in the Rheum palmatum complex in the Eastern Asiatic Region

“…DNA was extracted using the Qiagen plant genomic DNA Kit following the manufacturer's instructions. Approximately 400 ng of DNA per sample was sent to Biomarker Technologies Corporation for specific‐locus amplified fragment sequencing (SLAF‐seq), a reduced‐representation genomic approach (Sun et al., 2013), which has been successfully applied in population genomics analyses (e.g., Chong et al., 2016; Han et al., 2016; Sun et al., 2019). This technique is an optimized version of ddRADseq (double digest restriction‐site associated DNA sequencing) specifically intended for large‐scale genotyping experiments (https://www.illumina.com/science/sequencing-method-explorer/kits-and-arrays/slaf-seq.html?langsel=/us/) using deep sequencing to ensure genotyping accuracy and predesigning reduced representation library (RRL) schemes to avoid large numbers of repetitive sequences (Sun et al., 2013; Wang et al., 2019).…”

Getting Back to Nature: Feralization in Animals and Plants

“…Altogether, these examples show that, at the genetic level, domestication-related changes are not predictably reversed by feralization. In systems where phenotypic reversion has occurred despite this (e.g., in weedy rice), we can now begin to disentangle how stochastic factors, the reversibility or irreversibility of evolution, and/or differences between ancestral and feral environments (e.g., emergent competition with domesticated counterparts [99]) steer the process of feralization.…”

Analysis of evolutionary relationships provides new clues to the origins of weedy rice

“…Recent studies have indicated that WR plants growing in different regions around the world appear to have multiple origins (He et al, 2017;Li et al, 2017;Qiu et al, 2014Qiu et al, , 2017Sun et al, 2013Sun et al, , 2019. Recent studies have indicated that WR plants growing in different regions around the world appear to have multiple origins (He et al, 2017;Li et al, 2017;Qiu et al, 2014Qiu et al, , 2017Sun et al, 2013Sun et al, , 2019.…”

“…Sun et al (2013) found that introgression and selection from cultivated rice contributed to the genome of WR in northern China, and Sun et al (2019) showed that WR from high latitude regions in Asia possesses many unselected genomic characteristics. Genetic studies have indicated that WR has diverse origins, and that it evolved independently from domesticated rice or its wild relatives in different regions.…”

“…Many studies of WR are mainly focused on those geographical regions where no reproductively compatible wild rice species occur, such as North America, North China, and Korea. Sun et al (2013) found that introgression and selection from cultivated rice contributed to the genome of WR in northern China, and Sun et al (2019) showed that WR from high latitude regions in Asia possesses many unselected genomic characteristics. The study of He, Kim, and Park (2017) indicated that Korean WR originated from hybridization of modern indica/indica or japonica/ japonica varieties rather than from wild rice, while Li, Li, Jia, Caicedo, and Olsen (2017) showed that WR has evolved through de-domestication from cultivated varieties in America.…”