All roads lead to weediness: Patterns of genomic divergence reveal extensive recurrent weedy rice origins from South Asian Oryza

Abstract

Weedy rice (Oryza spp.), a weedy relative of cultivated rice (O. sativa), infests and persists in cultivated rice fields worldwide. Many weedy rice populations have evolved similar adaptive traits, considered part of the 'agricultural weed syndrome', making this an ideal model to study the genetic basis of parallel evolution. Understanding parallel evolution hinges on accurate knowledge of the genetic background and origins of existing weedy rice groups. Using population structure analyses of South Asian and US weedy rice, we show that weeds in South Asia have highly heterogeneous genetic backgrounds, with ancestry contributions both from cultivated varieties (aus and indica) and wild rice. Moreover, the two main groups of weedy rice in the USA, which are also related to aus and indica cultivars, constitute a separate origin from that of Asian weeds. Weedy rice populations in South Asia largely converge on presence of red pericarps and awns and on ease of shattering. Genomewide divergence scans between weed groups from the USA and South Asia, and their crop relatives are enriched for loci involved in metabolic processes. Some candidate genes related to iconic weedy traits and competitiveness are highly divergent between some weed-crop pairs, but are not shared among all weed-crop comparisons. Our results show that weedy rice is an extreme example of recurrent evolution, and suggest that most populations are evolving their weedy traits through different genetic mechanisms.

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

“…As a conspecific weed of a genomic model crop species, weedy rice has provided a productive system for studying the dynamics of agricultural weed adaptation. Studies over the last two decades have characterized the population structure of weed strains and revealed independent weed origins in different world regions, with most weed strains closely related to domesticated rice (Akasaka, Ushiki, Iwata, Ishikawa, & Ishii, 2009;Cao et al, 2006;Cho, Chung, & Suh, 1995;Huang et al, 2017;Londo & Schaal, 2007;Song, Chuah, Tam, & Olsen, 2014). Weedy rice strains in the southern United States are among the genetically best characterized.…”

Discordant Patterns of Introgression Suggest Historical Gene Flow into Thai Weedy Rice from Domesticated and Wild Relatives

“…In other regions, such as the United States, the weeds are genetically distinct from local crop varieties and likely evolved through dedomestication in Asia, with subsequent unintentional introductions into their present range (Reagon et al 2010;Li et al 2017). In areas of tropical Asia where wild rice is present, weedy rice strains have typically been found to show some evidence of introgression from wild populations, although they are still primarily descended from domesticated rice (Cao et al 2006;Song et al 2014;Huang et al 2017).…”

The 21st Century Agriculture: When Rice Research Draws Attention to Climate Variability and How Weedy Rice and Underutilized Grains Come in Handy

“…Most successful examples of MAS include the development of rice introgressed with Xa genes for bacterial blight resistance and Sub1A for submergence tolerance [56]. Genome-wide association studies (GWAS) represent another powerful tool used to dissect the genetics and identify markers associated with complex traits in rice, including flowering time, plant height, grain yield, and grain shape for use in MAS [57,58].…”