Call of the wild rice: Oryza rufipogon shapes weedy rice evolution in Southeast Asia

Abstract

Agricultural weeds serve as productive models for studying the genetic basis of rapid adaptation, with weed-adaptive traits potentially evolving multiple times independently in geographically distinct but environmentally similar agroecosystems. Weedy relatives of domesticated crops can be especially interesting systems because of the potential for weed-adaptive alleles to originate through multiple mechanisms, including introgression from cultivated and/or wild relatives, standing genetic variation, and de novo mutations. Weedy rice populations have evolved multiple times through dedomestication from cultivated rice. Much of the genomic work to date in weedy rice has focused on populations that exist outside the range of the wild crop progenitor. In this study, we use genome-wide SNPs generated through genotyping-by-sequencing to compare the evolution of weedy rice in regions outside the range of wild rice (North America, South Korea) and populations in Southeast Asia, where wild rice populations are present. We find evidence for adaptive introgression of wild rice alleles into weedy rice populations in Southeast Asia, with the relative contributions of wild and cultivated rice alleles varying across the genome. In addition, gene regions underlying several weed-adaptive traits are dominated by genomic contributions from wild rice.Genome-wide nucleotide diversity is also much higher in Southeast Asian weeds than in North American and South Korean weeds. Besides reflecting introgression from wild rice, this difference in diversity likely reflects genetic contributions from diverse cultivated landraces that may have served as the progenitors of these weedy populations. These important differences in weedy rice evolution in regions with and without wild rice could inform region-specific management strategies for weed control. K E Y W O R D S

Re‐acquisition of the brittle rachis trait via a transposon insertion in domestication gene Q during wheat de‐domestication

“…De-domestication is a unique evolutionary process by which domesticated crops re-acquire wild-like traits to survive and persist in agricultural fields without the need for human cultivation (Ellstrand et al, 2010;Gamborg et al, 2010;Guo et al, 2018). Studying de-domestication may be useful for characterizing rapid convergent evolution (Xia et al, 2011;Vigueira et al, 2013Vigueira et al, , 2019, and it is also relevant for elucidating the origins of weeds, which are a considerable problem in agriculture (Ellstrand et al, 2010;Stewart, 2017). Weedy rice, which evolved mainly from cultivated rice through de-domestication (Ellstrand et al, 2010;Wedger & Olsen, 2018), has become a worldwide problem in rice fields (Wedger & Olsen, 2018).…”

Phylogenetic origin and dispersal pattern of Taiwan weedy rice

“…In areas without wild rice species, WRR can occur due to seed introduction into cultivated rice fields or by evolution as a result of adaptive mutation and de‐domestication of the cultivated species . In such cases where wild Oryza species do not occur, WRR has been found to trace to indica origins in Brazil, China, South Korea, and the southern USA and to japonica origins in Italy, California, South Korea, Japan and China …”

The genomics of domestication special issue editorial

“…The third section concerns introgression between wild and domestic populations (Owens, Baute, Hubner, & Rieseberg, ; Schreiber, Himmelbach, Börner, & Mascher, ; Taitano et al., ; Vigueira et al., ). The first of these studies authored by Vigueira et al.…”

“…The first of these studies authored by Vigueira et al. () explores weedy rice inside and outside the rice native range, to understand diverse mechanisms for de‐domestication. Not surprisingly, introgression from wild to weedy rice was found to play an important role in weed evolution in geographic regions where the two taxa co‐occur, but not where the wild progenitor is absent.…”

“…The third section concerns introgression between wild and domestic populations (Owens, Baute, Hubner, & Rieseberg, 2018;Schreiber, Himmelbach, Börner, & Mascher, 2018;Taitano et al, 2018;Vigueira et al, 2017). The first of these studies authored by Vigueira et al (2017) explores weedy rice inside and outside the rice native range, to understand diverse mechanisms for de-domestication. Not surprisingly, introgression from wild to weedy rice was found to play an important role in weed evolution in geographic regions where the two taxa co-occur, but not where the wild progenitor is absent.…”