Multiple compensatory mutations contribute to the de‐domestication of Iberian weedy rice

Abstract

Societal Impact Statement Weedy plants are a major constraint on agricultural productivity. Weedy rice is a weed that invades rice fields worldwide and is responsible for reductions in rice yields. Studies to date have detected multiple independent weedy rice origins in different parts of the world. We investigated the origin of weedy rice in Spain and Portugal and found that it has evolved from a cultivated rice variety group grown locally. Iberian weeds carry mutations that reverse domesticated pericarp color to its ancestral red color. Our results imply that management strategies are needed to prevent the evolution of troublesome weeds from cultivated ancestors. Summary Weedy rice, a damaging conspecific weed of cultivated rice, has arisen multiple times independently around the world. Understanding all weedy rice origins is necessary to create more effective weed management strategies. The origins of weedy rice in Spain and Portugal, where there are no native Oryza species, are unknown. In this study, we try to identify the likely ancestors of Iberian weedy rice and the mechanisms involved in the evolution of two weedy traits, seed shattering, and red pericarps. We used genotyping by sequencing to understand the origin of Iberian weedy rice and its relationship to other weedy, wild, and cultivated rice groups worldwide. We also genotyped candidate genes for shattering and pericarp color. We find that weedy rice in the Iberian Peninsula has primarily evolved through de‐domestication of temperate japonica cultivars, with minor origins from exotic weedy rice. Iberian weeds have evolved the capacity to shatter seeds via novel loci and have acquired red pericarps via compensatory mutations in the Rc domestication gene. Our results suggest the Iberian weeds have experienced selection at multiple locations in the genome to establish as weeds, likely targeting male fertility genes among other functions. Our characterization of Iberian weedy rice adds to the growing evidence that de‐domestication of cultivated rice varieties is the main source of weedy rice worldwide. Their evolutionary versatility explains why weedy rice continues to be one of the most problematic weeds of cultivated rice.

Agricultural weeds: the contribution of domesticated species to the origin and evolution of feral weeds

“…Its genetic control has been associated with major loci with stable effects, which are related to crop domestication (for example, sh1, sh4, SHAT1, SHAT1-5, SHP1, Pdh1). 35 Interestingly, most feral weeds restore ancestral shattering phenotypes, not necessary by reversal of domesticated alleles, but through novel genetic mechanisms, 25 for example, weedy rice [36][37][38][39] and Tibetan weedy wheat. 40 Seed dormancy, defined as a temporary failure of viable seeds to germinate under environmental conditions that are favorable for germination, is another key trait in weeds because it regulates the timing of germination so that the environmental conditions are favorable for seedling survival and reproduction.…”

“…Its genetic control has been associated with major loci with stable effects, which are related to crop domestication (for example, sh1, sh4, SHAT1, SHAT1‐5, SHP1, Pdh1) 35 . Interestingly, most feral weeds restore ancestral shattering phenotypes, not necessary by reversal of domesticated alleles, but through novel genetic mechanisms, 25 for example, weedy rice 36–39 and Tibetan weedy wheat 40 …”

“…70,71 Therefore, not all feral weeds share all traits, suggesting that different genetic backgrounds may evolve weediness through distinct genetic mechanisms. 23,38,47 For example, some populations of weedy rice, feral rye, feral radish, and weedy Brassica rapa have not evolved seed dormancy; 8,46,72,73 feral rye, weedy artichoke and some weedy rice populations have not evolved early flowering; [74][75][76] and feral radish has not evolved seed shattering. 77,78 However, they are all important feral weeds.…”

Building a feral future: Open questions in crop ferality

“…Is feralization achieved primarily through few changes of large effect or small effect changes across many loci? feral rice, some of the selected alleles were derived from new mutations (Li et al, 2022;Scossa & Fernie, 2021). Also in rice, researchers have found that, in some cases, independently evolving feral populations have several shared "de-domestication" genomic blocks (Qiu et al, 2020).…”

“…For example, advances have been made in understanding the pathways to ferality, with feralization occurring either through introgression from wild relatives (exoferality) or without such introgression (endoferality) (Cronin et al, 2020;Gressel, 2005). Many of our insights into the genetic and phenotypic changes involved in ferality are derived from research on feral rice, which has identified key loci, traits, and evolutionary pathways associated with feralization (Li et al, 2022;Wedger & Olsen, 2018;Zhou et al, 2021). Recently, ferality has also become a topic of interest in the study of domestication, as wild-weedy-domesticated complexes were likely frequent in the early stages of domestication for many plants (Allaby et al, 2021;Purugganan, 2019Purugganan, , 2022.…”