Genomic divergence during feralization reveals both conserved and distinct mechanisms of parallel weediness evolution

Yoshihiro Kawahara,Hiroyuki Kobayashi,Akira Koarai,Kaworu Ebana,Toshiyuki Imaizumi,Kenneth M Olsen,Chiaki Muto

doi:10.1038/s42003-021-02484-5

Abstract

Agricultural weeds are the most important biotic constraints to global crop production, and chief among these is weedy rice. Despite increasing yield losses from weedy rice in recent years worldwide, the genetic basis of weediness evolution remains unclear. Using whole-genome sequence analyses, we examined the origins and adaptation of Japanese weedy rice. We find evidence for a weed origin from tropical japonica crop ancestry, which has not previously been documented in surveys of weedy rice worldwide. We further show that adaptation occurs largely through different genetic mechanisms between independently-evolved temperate japonica- and tropical japonica-derived strains; most genomic signatures of positive selection are unique within weed types. In addition, some weedy rice strains have evolved through hybridization between weedy and cultivated rice with adaptive introgression from the crop. Surprisingly, introgression from cultivated rice confers not only crop-like adaptive traits (such as shorter plant height, facilitating crop mimicry) but also weedy-like traits (such as seed dormancy). These findings reveal how hybridization with cultivated rice can promote persistence and proliferation of weedy rice.

Highlights

Agricultural weeds are the most important biotic constraints to global crop production, and chief among these is weedy rice
Principal component analysis (PCA) and phylogenetic analysis indicated that weedy rice in Japan shares ancestry predominantly with varieties of the temperate japonica (TEJ) and tropical japonica (TRJ) groups of cultivated rice
Japanese weedy rice evolved from East Asian japonica cultivated rice[10,11], and this study has revealed that black hull (BH) and SH_TRJ weedy rice evolved from East Asian TEJ or TRJ cultivated rice, respectively

Summary

Introduction

Agricultural weeds are the most important biotic constraints to global crop production, and chief among these is weedy rice. Weedy rice is an especially good model system for studying these mechanisms given its very close relationship to the genomic model system rice, and its evolutionary history of multiple independent origins from different crop varieties[15] While both cultivated and weedy rice are primarily self-pollinating, outcrossing occasionally occurs, and the proximity of weed strains and crop varieties within rice fields can facilitate hybridization and adaptive introgression into weed populations, including for traits such as herbicide resistance[16,17,18]. Both are closely related to japonica rice varieties (the major cultivars in Japan) but evolved through independent feralization events[11] Both strains possess typical weedy rice traits, including a red pericarp, shattered seeds and persistent seed dormancy[20]; these traits are all characteristic of wild Oryza species and were selected against during rice domestication. To the extent that SH weeds are of crop-weed hybrid origin, these strains can provide a valuable system to study weed adaptation via cultivated rice introgression

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Conclusion