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.
High reproductive compatibility between crops and their wild relatives can provide benefits for crop breeding but also poses risks for agricultural weed evolution. Weedy rice is a feral relative of rice that infests paddies and causes severe crop losses worldwide. In regions of tropical Asia where the wild progenitor of rice occurs, weedy rice could be influenced by hybridization with the wild species. Genomic analysis of this phenomenon has been very limited. Here we use whole genome sequence analyses of 217 wild, weedy and cultivated rice samples to show that wild rice hybridization has contributed substantially to the evolution of Southeast Asian weedy rice, with some strains acquiring weed-adaptive traits through introgression from the wild progenitor. Our study highlights how adaptive introgression from wild species can contribute to agricultural weed evolution, and it provides a case study of parallel evolution of weediness in independently-evolved strains of a weedy crop relative.
more » « less- Award ID(s):
- 1947609
- PAR ID:
- 10491854
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Weedy rice is a close relative of cultivated rice that devastates rice productivity worldwide. In the southern United States, two distinct strains have been historically predominant, but the 21stcentury introduction of hybrid rice and herbicide resistant rice technologies has dramatically altered the weedy rice selective landscape. Here, we use whole-genome sequences of 48 contemporary weedy rice accessions to investigate the genomic consequences of crop-weed hybridization and selection for herbicide resistance. We find that population dynamics have shifted such that most contemporary weeds are now crop-weed hybrid derivatives, and that their genomes have subsequently evolved to be more like their weedy ancestors. Haplotype analysis reveals extensive adaptive introgression of cultivated alleles at the resistance gene
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Abstract Weedy rice, a pervasive and troublesome weed found across the globe, has often evolved through fertilization of rice cultivars with little importance of crop‐weed gene flow. In Argentina, weedy rice has been reported as an important constraint since the early 1970s, and, in the last few years, strains with herbicide‐resistance are suspected to evolve. Despite their importance, the origin and genetic composition of Argentinian weedy rice as well its adaptation to agricultural environments has not been explored so far. To study this, we conducted genotyping‐by‐sequencing on samples of Argentinian weedy and cultivated rice and compared them with published data from weedy, cultivated and wild rice accessions distributed worldwide. In addition, we conducted a phenotypic characterization for weedy‐related traits, a herbicide resistance screening and genotyped accessions for known mutations in the acetolactate synthase (
ALS ) gene, which confers herbicide resistance. Our results revealed large phenotypic variability in Argentinian weedy rice. Most strains were resistant to ALS‐inhibiting herbicides with a high frequency of the ALS mutation (A122T) present in Argentinian rice cultivars. Argentinian cultivars belonged to the three major genetic groups of rice:japonica ,indica andaus while weeds were mostlyaus oraus‐indica admixed, resembling weedy rice strains from the Southern Cone region. Phylogenetic analysis supports a single origin foraus‐like South American weeds, likely as seed contaminants from the United States, and then admixture with localindica cultivars. Our findings demonstrate that crop to weed introgression can facilitate rapid adaptation to agriculture environments. -
Abstract There are two species of cultivated rice in the world— Oryza sativa L. from Asia and Oryza glaberrima Steud. from Africa. The former was domesticated from the wild progenitor Oryza rufipogon Griff. and the latter from the African wild rice species Oryza barthii A. Shiv. The first known center of rice cultivation in China generated the O. sativa subspecies japonica . The indica subspecies arose from the second center of domestication in the Ganges River plains of India. Variants of domesticated lines and the continuous hybridization between cultivated varieties and the wild progenitor(s) resulted in weedy rice types. Some weedy types resemble the wild ancestor, but the majority of weedy rices today bear close resemblance to cultivated rice. Weedy rice accompanies rice culture and has increased in occurrence with the global shift in rice establishment from transplanting to direct-seeded or dry-drill-seeded rice. Weedy rice ( Oryza spp.) is the most difficult weed to control in rice, causing as much as 90% yield loss or abandonment of severely infested fields. The gene flow continuum between cultivar and weedy rice or wild relative, crop de-domestication, and regionalized adaptation have resulted in a myriad of weedy rice types. The complex lineage of weedy rice has resulted in confusion of weedy rice nomenclature. Two names are generally used for weedy rice— Oryza sativa L. and Oryza sativa f. spontanea . Genomic data show that O. sativa L. applies to weedy rice populations derived from cultivated O. sativa , whereas O. sativa f. spontanea applies only to weedy types that primarily descended from O. rufipogon . Neither of these names applies to African weedy rice, which is of African wild rice or O. glaberrima lineage. Therefore, unless the lineage of the weedy population in question is known, the proper name to use is the generalized name Oryza spp.more » « less
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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 theRc 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.
