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

Author
item HUANG, ZHONGYUN - University Of Massachusetts
item YOUNG, NELSON - University Of Massachusetts
item HYMA, KATIE - University Of Massachusetts
item OLSEN, KENNETH - Washington University
item Jia, Yulin
item CAICEDO, ANA - University Of Massachusetts

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2017
Publication Date: 4/10/2017
Citation: Huang, Z., Young, N.D., Hyma, K., Olsen, K.M., Jia, Y., Caicedo, A.L. 2017. All roads lead to weediness: patterns of genomic divergence reveal extensive recurrent weedy rice origins from South Asian Oryza. Molecular Ecology. doi:10.1111/mec.14120.

Interpretive Summary: Weedy rice (Oryza spp.) is one of the most important agricultural pests causing significant reduction of grain yield in cultivated rice (Oryza sativa) worldwide. However, the genes involved in metabolic processes, phenotypes, population structure, and origins of weedy rice globally are not fully understood. We found that the two major groups of weedy rice in the USA were related to different aus and indica cultivars in comparison with that of Asian weeds. Weedy rice ecotypes in South Asia are heterogeneous with the ancestry from cultivated varieties (aus and indica) and wild rice and differ in most growth-related traits, but largely coincide in weedy traits such as red pericarp, awns and shattering. More genes are involved in the metabolic processes in weedy biotypes from the USA and South Asia as compared to their crop relatives; however, few genes are shared between the weedy and cultivated rice. Some candidate genes for common weedy traits are highly divergent between some weed and crop groups, but are not shared amongst all weed and cultivated rice. Our results show that weedy rice has used a different genetic mechanism to evolve compared with cultivated rice. Weedy rice is genetically diverse presenting significant challenges to manage in agricultural production systems.

Technical Abstract: Weedy rice (Oryza spp.), a weedy relative of cultivated rice (O. sativa), invades 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 and phylogenetic analyses of South Asian weedy rice, we show that weeds in this region have highly heterogeneous genetic backgrounds, with close relationships both to cultivated varieties (aus and indica) and wild rice. Both de-domestication and domestication-independent origins are detected in crop-related weeds. Moreover, the two main groups of weedy rice in the US, 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 pericarp and awns and on ease of shattering. Genome-wide divergence scans between weed groups from the US 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 and crop groups, but are not shared amongst all weed-crop comparisons. Our results show that weedy rice is an extreme example of evolution at a global scale, and suggest that most populations are evolving through use of different genetic mechanisms.