Worldwide feralization of crop species into agricultural weeds threatens global food security. Weedy rice is a feral form of rice that infests paddies worldwide and aggressively outcompetes ...cultivated varieties. Despite increasing attention in recent years, a comprehensive understanding of the origins of weedy crop relatives and how a universal feralization process acts at the genomic and molecular level to allow the rapid adaptation to weediness are still yet to be explored.
We use whole-genome sequencing to examine the origin and adaptation of 524 global weedy rice samples representing all major regions of rice cultivation. Weed populations have evolved multiple times from cultivated rice, and a strikingly high proportion of contemporary Asian weed strains can be traced to a few Green Revolution cultivars that were widely grown in the late twentieth century. Latin American weedy rice stands out in having originated through extensive hybridization. Selection scans indicate that most genomic regions underlying weedy adaptations do not overlap with domestication targets of selection, suggesting that feralization occurs largely through changes at loci unrelated to domestication.
This is the first investigation to provide detailed genomic characterizations of weedy rice on a global scale, and the results reveal diverse genetic mechanisms underlying worldwide convergent rice feralization.
White clover (Trifolium repens) is a globally important perennial forage legume. This species also serves as an eco-evolutionary model system for studying within-species chemical defense variation; ...it features a well-studied polymorphism for cyanogenesis (HCN release following tissue damage), with higher frequencies of cyanogenic plants favored in warmer locations worldwide. Using a newly generated haplotype-resolved genome and two other long-read assemblies, we tested the hypothesis that copy number variants (CNVs) at cyanogenesis genes play a role in the ability of white clover to rapidly adapt to local environments. We also examined questions on subgenome evolution in this recently evolved allotetraploid species and on chromosomal rearrangements in the broader IRLC legume clade. Integration of PacBio HiFi, Omni-C, Illumina, and linkage map data yielded a completely de novo genome assembly for white clover (created without a priori sequence assignment to subgenomes). We find that white clover has undergone extensive transposon diversification since its origin but otherwise shows highly conserved genome organization and composition with its diploid progenitors. Unlike some other clover species, its chromosomal structure is conserved with other IRLC legumes. We further find extensive evidence of CNVs at the major cyanogenesis loci; these contribute to quantitative variation in the cyanogenic phenotype and to local adaptation across wild North American populations. This work provides a case study documenting the role of CNVs in local adaptation in a plant species, and it highlights the value of pan-genome data for identifying contributions of structural variants to adaptation in nature.
Domestication is a multifaceted evolutionary process, involving changes in individual genes, genetic interactions, and emergent phenotypes. There has been extensive discussion of the phenotypic ...characteristics of plant domestication, and recent research has started to identify the specific genes and mutational mechanisms that control domestication traits. However, there is an apparent disconnect between the simple genetic architecture described for many crop domestication traits, which should facilitate rapid phenotypic change under selection, and the slow rate of change reported from the archeobotanical record. A possible explanation involves the middle ground between individual genetic changes and their expression during development, where gene-by-gene (epistatic) and gene-by-environment interactions can modify the expression of phenotypes and opportunities for selection. These aspects of genetic architecture have the potential to significantly slow the speed of phenotypic evolution during crop domestication and improvement. Here we examine whether epistatic and gene-by-environment interactions have shaped how domestication traits have evolved. We review available evidence from the literature, and we analyze two domestication-related traits, shattering and flowering time, in a mapping population derived from a cross between domesticated foxtail millet and its wild progenitor. We find that compared with wild progenitor alleles, those favored during domestication often have large phenotypic effects and are relatively insensitive to genetic background and environmental effects. Consistent selection should thus be able to rapidly change traits during domestication. We conclude that if phenotypic evolution was slow during crop domestication, this is more likely due to cultural or historical factors than epistatic or environmental constraints.
Premise
Camelina (gold‐of‐pleasure or false flax) is an ancient oilseed crop with emerging applications in the production of sustainable, low‐input biofuels. Previous domestication hypotheses ...suggested a European or western Asian origin, yet little genetic evidence has existed to assess the geographical origin for this crop, and archaeological data have not been systematically surveyed.
Methods
We utilized genotyping‐by‐sequencing of 185 accessions of C. sativa and its wild relatives to examine population structure within the crop species and its relationship to populations of its wild progenitor, C. microcarpa; cytotype variation was also assessed in both species. In a complementary analysis, we surveyed the archaeological literature to identify sites with archaeobotanical camelina remains and assess the timing and prevalence of usage across Europe and western Asia.
Results
The majority of C. microcarpa sampled in Europe and the United States belongs to a variant cytotype (2n = 38) with a distinct evolutionary origin from that of the crop lineage (2n = 40). Populations of C. microcarpa from Transcaucasia (South Caucasus) are most closely related to C. sativa based on cytotype and population structure; in combination with archaeological insights, these data refute prior hypotheses of a European domestication origin.
Conclusions
Our findings support a Caucasus, potentially Armenian, origin of C. sativa domestication. We cannot definitively determine whether C. sativa was intentionally targeted for domestication in its own right or instead arose secondarily through selection for agricultural traits in weedy C. sativa, as originally proposed by Vavilov for this species.
There is increasing interest in documenting adaptation of weedy plant species to agricultural ecosystems, beyond the evolution of herbicide resistance. Waterhemp (Amaranthus tuberculatus) is a native ...plant of the Midwestern U.S. that began infesting agricultural fields in the 20th century within the central portion of its range. We hypothesized that the vegetative growth and reproductive traits of waterhemp from this heavily infested central region provide differential fitness benefits in agricultural environments. We collected seeds from across the species' native range, representing regions with varying degrees of waterhemp infestation, and planted them together in common garden soybean plots. A 2010 common garden experiment was conducted within the range of agriculturally weedy waterhemp (in Missouri), and a 2011 common garden experiment was conducted outside of this range (in Ohio). Days to flowering and flowering plant height, mature plant size data (height, number of branches, and length of the longest branch), and above-ground biomass were measured to estimate relative fitness. In both common garden locations, plants from regions where waterhemp occurs as an agricultural weed - including those from the heavily infested Mississippi Valley region (Iowa, Illinois, and Missouri) and the less severely infested Plains region (Nebraska, Kansas, and Oklahoma) - had higher relative performance in almost all fitness-related measures than plants from the Northeast region (Ohio, Michigan, and Ontario), which had little to no agriculturally weedy waterhemp at the time of our study. Further analysis revealed that fewer days to flowering in the Northeast populations can be largely accounted for by latitude of origin, suggesting a strong genetic influence on this reproductive trait. These findings suggest intraspecific variation in agricultural adaptation in a native U.S. weed, and support the use of agricultural weeds to study adaptation.
Since the time of Darwin, biologists have understood the promise of crop plants and their wild relatives for providing insight into the mechanisms of phenotypic evolution. The intense selection ...imposed by our ancestors during plant domestication and subsequent crop improvement has generated remarkable transformations of plant phenotypes. Unlike evolution in natural settings, descendent and antecedent conditions for crop plants are often both extant, providing opportunities for direct comparisons through crossing and other experimental approaches. Moreover, since domestication has repeatedly generated a suite of "domestication syndrome" traits that are shared among crops, opportunities exist for gaining insight into the genetic and developmental mechanisms that underlie parallel adaptive evolution. Advances in our understanding of the genetic architecture of domestication-related traits have emerged from combining powerful molecular technologies with advanced experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies may be combined with high-throughput evaluations of the various "omics" involved in trait transformation, revealing a diversity of underlying causative mutations affecting phenotypes and their downstream propagation through biological networks. We summarize the state of our knowledge of the mutational spectrum that generates phenotypic novelty in domesticated plant species, and our current understanding of how domestication can reshape gene expression networks and emergent phenotypes. An exploration of traits that have been subject to similar selective pressures across crops (e.g., flowering time) suggests that a diversity of targeted genes and causative mutational changes can underlie parallel adaptation in the context of crop evolution.
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.
Camelina sativa (gold-of-pleasure) is a traditional European oilseed crop and emerging biofuel source with high levels of desirable fatty acids. A twentieth century germplasm bottleneck depleted ...genetic diversity in the crop, leading to recent interest in using wild relatives for crop improvement. However, little is known about seed oil content and genetic diversity in wild Camelina species.
We used gas chromatography, environmental niche assessment, and genotyping-by-sequencing to assess seed fatty acid composition, environmental distributions, and population structure in C. sativa and four congeners, with a primary focus on the crop's wild progenitor, C. microcarpa. Fatty acid composition differed significantly between Camelina species, which occur in largely non-overlapping environments. The crop progenitor comprises three genetic subpopulations with discrete fatty acid compositions. Environment, subpopulation, and population-by-environment interactions were all important predictors for seed oil in these wild populations. A complementary growth chamber experiment using C. sativa confirmed that growing conditions can dramatically affect both oil quantity and fatty acid composition in Camelina.
Genetics, environmental conditions, and genotype-by-environment interactions all contribute to fatty acid variation in Camelina species. These insights suggest careful breeding may overcome the unfavorable FA compositions in oilseed crops that are predicted with warming climates.
Despite its status as one of the world's major crops, linkage disequilibrium (LD) patterns have not been systematically characterized across the genome of Asian rice (Oryza sativa). Such information ...is critical to fully exploit the genome sequence for mapping complex traits using association techniques. Here we characterize LD in five 500-kb regions of the rice genome in three major cultivated rice varieties (indica, tropical japonica, and temperate japonica) and in the wild ancestor of Asian rice, Oryza rufipogon. Using unlinked SNPs to determine the amount of background linkage disequilibrium in each population, we find that the extent of LD is greatest in temperate japonica (probably >500 kb), followed by tropical japonica (approximately 150 kb) and indica (approximately 75 kb). LD extends over a shorter distance in O. rufipogon (<<40 kb) than in any of the O. sativa groups assayed here. The differences in the extent of LD among these groups are consistent with differences in outcrossing and recombination rate estimates. As well as heterogeneity between groups, our results suggest variation in LD patterns among genomic regions. We demonstrate the feasibility of genomewide association mapping in cultivated Asian rice using a modest number of SNPs.
The mechanisms by which weedy rice (Oryza sativa f. spontanea) has adapted to endure low‐temperature stress in northern latitudes remain unresolved. In this study, we assessed cold tolerance of 100 ...rice varieties and 100 co‐occurring weedy rice populations, which were sampled across a broad range of climates in China. A parallel pattern of latitude‐dependent variation in cold tolerance was detected in cultivated rice and weedy rice. At the molecular level, differential cold tolerance was strongly correlated with relative expression levels of CBF cold response pathway genes and with methylation levels in the promoter region of OsICE1, a regulator of this pathway. Among all methylated cytosine sites of the OsICE1 promoter, levels of CHG and CHH methylation were found to be significantly correlated with cold tolerance among accessions. Furthermore, within many of the collection locales, weedy rice shared identical or near‐identical OsICE1 methylation patterns with co‐occurring cultivated rice. These findings provide new insights on the possible roles that methylation variation in the OsICE1 promoter may play in cold tolerance, and they suggest that weedy rice can rapidly acquire cold tolerance via methylation patterns that are shared with co‐occurring rice cultivars.
PDF
