The role of standing variation in the evolution of weediness traits in south Asian weedy rice (oryza spp.)

Authors: HUANG, ZHONGYUN - University Of Massachusetts; KELLY, SHANNON - University Of Massachusetts; MATSUO, RIKA - University Of Massachusetts; LI, LIN-FENG - Washington University; LI, YALING - Washington University; OLSEN, KENNETH - Washington University; Jia, Yulin; CAICEDO, ANA - University Of Massachusetts

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/20/2018
Publication Date: 11/1/2018
Citation: Huang, Z., Kelly, S., Matsuo, R., Li, L., Li, Y., Olsen, K.M., Jia, Y., Caicedo, A.L. 2018. The role of standing variation in the evolution of weediness traits in south Asian weedy rice (oryza spp.). G3, Genes/Genomes/Genetics. https://doi.org/10.1534/g3.118.200605.
DOI: https://doi.org/10.1534/g3.118.200605

Interpretive Summary: Weedy rice is a problematic weed of cultivated rice around the world. Recent studies suggest that there may be multiple, but independent, evolutionary origins of weedy rice which raises questions about which traits and genes are necessary for its evolution. South Asia has the most diverse weedy rice populations that can be traced to at least three origins, two from the de-domestication of rice cultivars and one from local wild rice. A set of traits considered typical of or advantageous to weedy rice were analyzed to determine the similarities, both genetic and morphological, between the three weedy groups. It was discovered that three traits were common among all three weed groups in South Asia suggesting that easy seed shattering, red pericarp color, and compact plant architecture are essential for weedy rice success in the South Asian agricultural environment. It was also found that black hull color was common among weeds with wild ancestors and weeds that evolved from cultivated rice group aus. Two different known candidate genes are likely expressed for weed seed pericarp color and hull color. Weedy alleles segregate in the ancestral populations, as do alleles for the seed dormancy linked gene. The presence of a domestication-related allele in the seed shattering locus in weedy rice populations with cultivated ancestry supports a de-domestication origin for these weedy groups and raises more questions about the reacquisition of the shattering trait in these weedy populations. The characterization of weedy rice groups in South Asia and the associated candidate genes contributes to the understanding of weedy rice evolution and the role of ancestral variation of cultivated and wild rice. This knowledge will help to control rice red contamination in rice fields.

Technical Abstract: Weedy rice (Oryza spp.) is a problematic weed of cultivated rice (O. sativa) around the world. Recent studies have established multiple independent evolutionary origins of weedy rice, raising the question regarding the traits and genes that are essential for the evolution of this weed. Among world regions, South Asia stands out due to the heterogeneity of its weedy rice populations, which can be traced to at least three origins: two through de-domestication from distinct cultivated rice varieties, and one from local wild rice (O. rufipogon/O. nivara). Here, we examine a set of traits considered typical of or advantageous to weedy rice, and establish that convergence among all three weed groups in South Asia occurs for easy seed shattering, red pericarp color, and compact plant architecture, suggesting that these traits are essential for weed success in the South Asian agricultural environment. A high degree of convergence for black hull color is also seen among weeds with wild ancestors and weeds evolved from the aus cultivated rice group. Known candidate genes Rc and Bh4 likely underlie weed seed pericarp color and hull color, respectively, and weedy alleles segregate in the ancestral populations, as do alleles for the seed dormancy linked gene Sdr4. The presence of a domestication related allele in the seed shattering locus sh4 in weedy rice populations with cultivated ancestry, supports a de-domestication origin for these weedy groups, and raises questions about the reacquisition of the shattering traits of these weedy populations. Our characterization of weedy rice phenotypes in South Asia and the associated candidate genes contributes to the emerging understanding of the mechanisms by which weedy rice evolves worldwide, suggesting that standing ancestral variation is often the source of weedy traits in independently evolved groups, and highlighting the reservoir of genetic variation that is present in cultivated varieties as well as in wild rice, and its potential for phenotypic evolution.