A derived weedy rice × ancestral cultivar cross identifies evolutionarily relevant weediness QTLs.

Weedy rice (Oryza spp.) is a weedy relative of the cultivated rice that competes with the crop and causes significant production loss. The BHA (blackhull awned) US weedy rice group has evolved from aus cultivated rice and differs from its ancestors in several important weediness traits, including flowering time, plant height and seed shattering. Prior attempts to determine the genetic basis of weediness traits in plants using linkage mapping approaches have not often considered weed origins. However, the timing of divergence between crossed parents can affect the detection of quantitative trait loci (QTL) relevant to the evolution of weediness. Here, we used a QTL-seq approach that combines bulked segregant analysis and high-throughput whole genome resequencing to map the three important weediness traits in an F2 population derived from a cross between BHA weedy rice with an ancestral aus cultivar. We compared these QTLs with those previously detected in a cross of BHA with a more distantly related crop, indica. We identified multiple QTLs that overlapped with regions under selection during the evolution of weedy BHA rice and some candidate genes possibly underlying the evolution weediness traits in BHA. We showed that QTLs detected with ancestor-descendant crosses are more likely to be involved in the evolution of weediness traits than those detected from crosses of more diverged taxa.

Variation in ripe fruit volatiles across the tomato clade: An evolutionary framework for studying fruit scent diversity in a crop wild relative.

PREMISE: The scents of volatile organic compounds (VOCs) are an important component of ripe fleshy fruit attractiveness, yet their variation across closely related wild species is poorly understood. Phylogenetic patterns in these compounds and their biosynthetic pathways offer insight into the evolutionary drivers of fruit diversity, including whether scent can communicate an honest signal of nutrient content to animal dispersers. We assessed ripe fruit VOC content across the tomato clade (Solanum sect. Lycopersicon), with implications for crop improvement since these compounds are key components of tomato flavor. METHODS: We analyzed ripe fruit volatiles from 13 species of wild tomato grown in a common garden. Interspecific variations in 66 compounds and their biosynthetic pathways were assessed in 32 accessions, and an accession-level phylogeny was constructed to account for relatedness. RESULTS: Wild tomato species can be differentiated by their VOCs, with Solanum pennellii notably distinct. Phylogenetic conservatism exists to a limited extent. Major cladewide patterns corresponded to divergence of the five brightly colored-fruited species from the nine green-fruited species, particularly for nitrogen-containing compounds (higher in colored-fruited) and esters (higher in green-fruited), the latter appearing to signal a sugar reward. CONCLUSIONS: We established a framework for fruit scent evolution studies in a crop wild relative system, showing that each species in the tomato clade has a unique VOC profile. Differences between color groups align with fruit syndromes that could be driven by selection from frugivores. The evolution of colored fruits was accompanied by changes in biosynthetic pathways for esters and nitrogen-containing compounds, volatiles important to tomato flavor.

Unraveling the genetics of tomato fruit weight during crop domestication and diversification.

KEY MESSAGE: Six novel fruit weight QTLs were identified in tomato using multiple bi-parental populations developed from ancestral accessions. Beneficial alleles at these loci arose in semi-domesticated subpopulations and were likely left behind. This study paves the way to introgress these alleles into breeding programs. The size and weight of edible organs have been strongly selected during crop domestication. Concurrently, human have also focused on nutritional and cultural characteristics of fruits and vegetables, at times countering selective pressures on beneficial size and weight alleles. Therefore, it is likely that novel improvement alleles for organ weight still segregate in ancestral germplasm. To date, five domestication and diversification genes affecting tomato fruit weight have been identified, yet the genetic basis for increases in weight has not been fully accounted for. We found that fruit weight increased gradually during domestication and diversification, and semi-domesticated subpopulations featured high phenotypic and nucleotide diversity. Columella and septum fruit tissues were proportionally increased, suggesting targeted selection. We developed twenty-one F2 populations with parents fixed for the known fruit weight genes, corresponding to putative key transitions from wild to fully domesticated tomatoes. These parents also showed differences in fruit weight attributes as well as the developmental timing of size increase. A subset of populations was targeted for QTL-seq, leading to the identification of six uncloned fruit weight QTLs. Three QTLs, located on chromosomes 1, 2 and 3, were subsequently validated by progeny testing. By exploring the segregation of the known fruit weight genes and the identified QTLs, we estimated that most beneficial alleles in the newly identified loci arose in semi-domesticated subpopulations from South America and were not likely transmitted to fully domesticated landraces. Therefore, these alleles could be incorporated into breeding programs using the germplasm and genetic resources identified in this study.

Natural Genetic Diversity in Tomato Flavor Genes.

Fruit flavor is defined as the perception of the food by the olfactory and gustatory systems, and is one of the main determinants of fruit quality. Tomato flavor is largely determined by the balance of sugars, acids and volatile compounds. Several genes controlling the levels of these metabolites in tomato fruit have been cloned, including LIN5, ALMT9, AAT1, CXE1, and LoxC. The aim of this study was to identify any association of these genes with trait variation and to describe the genetic diversity at these loci in the red-fruited tomato clade comprised of the wild ancestor Solanum pimpinellifolium, the semi-domesticated species Solanum lycopersicum cerasiforme and early domesticated Solanum lycopersicum. High genetic diversity was observed at these five loci, including novel haplotypes that could be incorporated into breeding programs to improve fruit quality of modern tomatoes. Using newly available high-quality genome assemblies, we assayed each gene for potential functional causative polymorphisms and resolved a duplication at the LoxC locus found in several wild and semi-domesticated accessions which caused lower accumulation of lipid derived volatiles. In addition, we explored gene expression of the five genes in nine phylogenetically diverse tomato accessions. In general, the expression patterns of these genes increased during fruit ripening but diverged between accessions without clear relationship between expression and metabolite levels.

Something old, something new: Evolution of Colombian weedy rice (Oryza spp.) through de novo de-domestication, exotic gene flow, and hybridization.

Weedy rice (Oryza spp.) is a worldwide weed of domesticated rice (O. sativa), considered particularly problematic due to its strong competition with the crop, which leads to reduction in yields and harvest quality. Several studies have established multiple independent origins for weedy rice populations in the United States and various parts of Asia; however, the origins of weedy rice in South America have not been examined in a global context. We evaluated the genetic variation of weedy rice populations in Colombia, as well as the contributions of local wild Oryza species, local cultivated varieties, and exotic Oryza groups to the weed, using polymorphism generated by genotyping by sequencing (GBS). We found no evidence for genomic contributions from local wild Oryza species (O. glumaepatula, O. grandiglumis, O. latifolia, and O. alta) to Colombian weedy rice. Instead, Colombian weedy rice has evolved from local indica cultivars and has also likely been inadvertently imported as an exotic pest from the United States. Additionally, weeds comprising de novo admixture between these distinct weedy populations now represent a large proportion of genomic backgrounds in Colombian weedy rice. Our results underscore the impressive ability of weedy rice to evolve through multiple evolutionary pathways, including in situ de-domestication, range expansion, and hybridization.

Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato.

Structural variants (SVs) underlie important crop improvement and domestication traits. However, resolving the extent, diversity, and quantitative impact of SVs has been challenging. We used long-read nanopore sequencing to capture 238,490 SVs in 100 diverse tomato lines. This panSV genome, along with 14 new reference assemblies, revealed large-scale intermixing of diverse genotypes, as well as thousands of SVs intersecting genes and cis-regulatory regions. Hundreds of SV-gene pairs exhibit subtle and significant expression changes, which could broadly influence quantitative trait variation. By combining quantitative genetics with genome editing, we show how multiple SVs that changed gene dosage and expression levels modified fruit flavor, size, and production. In the last example, higher order epistasis among four SVs affecting three related transcription factors allowed introduction of an important harvesting trait in modern tomato. Our findings highlight the underexplored role of SVs in genotype-to-phenotype relationships and their widespread importance and utility in crop improvement.

Identification of Novel QTL Conferring Sheath Blight Resistance in Two Weedy Rice Mapping Populations.

BACKGROUND: Rice sheath blight (ShB) disease, caused by the pathogenic fungus Rhizoctonia solani, causes significant yield losses globally. US weedy rice populations, which are de-domesticated forms of indica and aus cultivated rice, appear to be more resistant to ShB than local japonica cultivated rice. We mapped quantitative trait loci (QTL) associated with ShB resistance using two F8 recombinant inbred line populations generated from crosses of an indica crop variety, Dee-Geo-Woo-Gen (DGWG), with individuals representing the two major US weed biotypes, straw hull (SH) and black hull awned (BHA). RESULTS: We identified nine ShB resistance QTL across both mapping populations. Five were attributable to alleles that affect plant height (PH) and heading date (HD), two growth traits that are known to be highly correlated with ShB resistance. By utilizing an approach that treated growth traits as covariates in the mapping model, we were able to infer that the remaining four QTL are involved in ShB resistance. Two of these, qShB1-2 and qShB4, are different from previously identified ShB QTL and represent new candidates for further study. CONCLUSION: Our findings suggest that ShB resistance can be improved through favorable plant growth traits and the combined effects of small to moderate-effect resistance QTL. Additionally, we show that including PH and HD as covariates in QTL mapping models is a powerful way to identify new ShB resistance QTL.

Genomic Evidence for Complex Domestication History of the Cultivated Tomato in Latin America.

The process of plant domestication is often protracted, involving underexplored intermediate stages with important implications for the evolutionary trajectories of domestication traits. Previously, tomato domestication history has been thought to involve two major transitions: one from wild Solanum pimpinellifolium L. to a semidomesticated intermediate, S. lycopersicum L. var. cerasiforme (SLC) in South America, and a second transition from SLC to fully domesticated S. lycopersicum L. var. lycopersicum in Mesoamerica. In this study, we employ population genomic methods to reconstruct tomato domestication history, focusing on the evolutionary changes occurring in the intermediate stages. Our results suggest that the origin of SLC may predate domestication, and that many traits considered typical of cultivated tomatoes arose in South American SLC, but were lost or diminished once these partially domesticated forms spread northward. These traits were then likely reselected in a convergent fashion in the common cultivated tomato, prior to its expansion around the world. Based on these findings, we reveal complexities in the intermediate stage of tomato domestication and provide insight on trajectories of genes and phenotypes involved in tomato domestication syndrome. Our results also allow us to identify underexplored germplasm that harbors useful alleles for crop improvement.

Considering weed management as a social dilemma bridges individual and collective interests.

Weeds pose severe threats to agricultural and natural landscapes worldwide. One major reason for the failure to effectively manage weeds at landscape scales is that current Best Management Practice guidelines, and research on how to improve such guidelines, focus too narrowly on property-level management decisions. Insufficiently considered are the aggregate effects of individual actions to determine landscape-scale outcomes, or whether there are collective practices that would improve weed management outcomes. Here, we frame landscape-scale weed management as a social dilemma, where trade-offs occur between individual and collective interests. We apply a transdisciplinary system approach-integrating the perspectives of ecologists, evolutionary biologists and agronomists into a social science theory of social dilemmas-to four landscape-scale weed management challenges: (i) achieving plant biosecurity, (ii) preventing weed seed contamination, (iii) maintaining herbicide susceptibility and (iv) sustainably using biological control. We describe how these four challenges exhibit characteristics of 'public good problems', wherein effective weed management requires the active contributions of multiple actors, while benefits are not restricted to these contributors. Adequate solutions to address these public good challenges often involve a subset of the eight design principles developed by Elinor Ostrom for 'common pool social dilemmas', together with design principles that reflect the public good nature of the problems. This paper is a call to action for scholars and practitioners to broaden our conceptualization and approaches to weed management problems. Such progress begins by evaluating the public good characteristics of specific weed management challenges and applying context-specific design principles to realize successful and sustainable weed management.

Call of the wild rice: Oryza rufipogon shapes weedy rice evolution in Southeast Asia.

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.

The Role of Standing Variation in the Evolution of Weedines Traits in South Asian Weedy Rice (Oryza spp.).

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 questions about 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 five traits considered typical of or advantageous to weedy rice in weedy, cultivated and wild rice samples from South Asia. We establish that convergence among all three weed groups 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. We also examine polymorphism in five known domestication candidate genes, and find that Rc and Bh4 are associated with 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 at 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 trait in these weedy populations. Our characterization of weedy rice phenotypes in South Asia and their associated candidate genes contribute 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.

Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure.

While prokaryotic pan-genomes have been shown to contain many more genes than any individual organism, the prevalence and functional significance of differentially present genes in eukaryotes remains poorly understood. Whole-genome de novo assembly and annotation of 54 lines of the grass Brachypodium distachyon yield a pan-genome containing nearly twice the number of genes found in any individual genome. Genes present in all lines are enriched for essential biological functions, while genes present in only some lines are enriched for conditionally beneficial functions (e.g., defense and development), display faster evolutionary rates, lie closer to transposable elements and are less likely to be syntenic with orthologous genes in other grasses. Our data suggest that differentially present genes contribute substantially to phenotypic variation within a eukaryote species, these genes have a major influence in population genetics, and transposable elements play a key role in pan-genome evolution.

Signatures of adaptation in the weedy rice genome.

Crop domestication provided the calories that fueled the rise of civilization. For many crop species, domestication was accompanied by the evolution of weedy crop relatives, which aggressively outcompete crops and reduce harvests. Understanding the genetic mechanisms that underlie the evolution of weedy crop relatives is critical for agricultural weed management and food security. Here we use whole-genome sequences to examine the origin and adaptation of the two major strains of weedy rice found in the United States. We find that de-domestication from cultivated ancestors has had a major role in their evolution, with relatively few genetic changes required for the emergence of weediness traits. Weed strains likely evolved both early and late in the history of rice cultivation and represent an under-recognized component of the domestication process. Genomic regions identified here that show evidence of selection can be considered candidates for future genetic and functional analyses for rice improvement.

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

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.

Impact of volunteer rice infestation on yield and grain quality of rice.

BACKGROUND: Volunteer rice (Oryza sativa L.) grains may differ in physicochemical traits from cultivated rice, which may reduce the quality of harvested rice grain. To evaluate the effect of volunteer rice on cultivated rice, fields were surveyed in Arkansas in 2012. RESULTS: Cropping history that included hybrid cultivars in the previous two years (2010 and 2011) had higher volunteer rice infestation (20%) compared with fields planted previously with inbred rice (5.5%). The total grain yield of rice was reduced by 0.4% for every 1% increase in volunteer rice density. The grain quality did not change in fields planted with the same cultivar for three years. Volunteer rice density of at least 7.6% negatively impacted the head rice and when infestation reached 17.7%, it also reduced the rice grain yield. The protein and amylose contents of rice were not affected until volunteer rice infestation exceeded 30%. CONCLUSION: Crop rotation systems that include hybrid rice are expected to have higher volunteer rice infestation than systems without hybrid rice. It is predicted that, at 8% infestation, volunteer rice will start to impact head rice yield and will reduce total yield at 18% infestation. It could alter the chemical quality of rice grain at >30% infestation. © 2016 Society of Chemical Industry.

Population Structure in the Model Grass Is Highly Correlated with Flowering Differences across Broad Geographic Areas.

The small, annual grass (L.) Beauv., a close relative of wheat ( L.) and barley ( L.), is a powerful model system for cereals and bioenergy grasses. Genome-wide association studies (GWAS) of natural variation can elucidate the genetic basis of complex traits but have been so far limited in by the lack of large numbers of well-characterized and sufficiently diverse accessions. Here, we report on genotyping-by-sequencing (GBS) of 84 , seven , and three accessions with diverse geographic origins including Albania, Armenia, Georgia, Italy, Spain, and Turkey. Over 90,000 high-quality single-nucleotide polymorphisms (SNPs) distributed across the Bd21 reference genome were identified. Our results confirm the hybrid nature of the genome, which appears as a mosaic of -like and -like sequences. Analysis of more than 50,000 SNPs for the accessions revealed three distinct, genetically defined populations. Surprisingly, these genomic profiles are associated with differences in flowering time rather than with broad geographic origin. High levels of differentiation in loci associated with floral development support the differences in flowering phenology between populations. Genome-wide association studies combining genotypic and phenotypic data also suggest the presence of one or more photoperiodism, circadian clock, and vernalization genes in loci associated with flowering time variation within populations. Our characterization elucidates genes underlying population differences, expands the germplasm resources available for , and illustrates the feasibility and limitations of GWAS in this model grass.

Little White Lies: Pericarp Color Provides Insights into the Origins and Evolution of Southeast Asian Weedy Rice.

Weedy rice is a conspecific form of cultivated rice (Oryza sativa L.) that infests rice fields and results in severe crop losses. Weed strains in different world regions appear to have originated multiple times from different domesticated and/or wild rice progenitors. In the case of Malaysian weedy rice, a multiple-origin model has been proposed based on neutral markers and analyses of domestication genes for hull color and seed shattering. Here, we examined variation in pericarp (bran) color and its molecular basis to address how this trait evolved in Malaysian weeds and its possible role in weed adaptation. Functional alleles of the Rc gene confer proanthocyanidin pigmentation of the pericarp, a trait found in most wild and weedy Oryzas and associated with seed dormancy; nonfunctional rc alleles were strongly favored during rice domestication, and most cultivated varieties have nonpigmented pericarps. Phenotypic characterizations of 52 Malaysian weeds revealed that most strains are characterized by the pigmented pericarp; however, some weeds have white pericarps, suggesting close relationships to cultivated rice. Phylogenetic analyses indicate that the Rc haplotypes present in Malaysian weeds likely have at least three distinct origins: wild O. rufipogon, white-pericarp cultivated rice, and red-pericarp cultivated rice. These diverse origins contribute to high Rc nucleotide diversity in the Malaysian weeds. Comparison of Rc allelic distributions with other rice domestication genes suggests that functional Rc alleles may confer particular fitness benefits in weedy rice populations, for example, by conferring seed dormancy. This may promote functional Rc introgression from local wild Oryza populations.

Environmental niche variation and evolutionary diversification of the Brachypodium distachyon grass complex species in their native circum-Mediterranean range.

UNLABELLED: • PREMISE OF THE STUDY: We conducted environmental niche modeling (ENM) of the Brachypodium distachyon s.l. complex, a model group of two diploid annual grasses (B. distachyon, B. stacei) and their derived allotetraploid (B. hybridum), native to the circum-Mediterranean region. We (1) investigated the ENMs of the three species in their native range based on present and past climate data; (2) identified potential overlapping niches of the diploids and their hybrid across four Quaternary windows; (3) tested whether speciation was associated with niche divergence/conservatism in the complex species; and (4) tested for the potential of the polyploid outperforming the diploids in the native range.• METHODS: Geo-referenced data, altitude, and 19 climatic variables were used to construct the ENMs. We used paleoclimate niche models to trace the potential existence of ancestral gene flow among the hybridizing species of the complex.• KEY RESULTS: Brachypodium distachyon grows in higher, cooler, and wetter places, B. stacei in lower, warmer, and drier places, and B. hybridum in places with intermediate climatic features. Brachypodium hybridum had the largest niche overlap with its parent niches, but a similar distribution range and niche breadth.• CONCLUSIONS: Each species had a unique environmental niche though there were multiple niche overlapping areas for the diploids across time, suggesting the potential existence of several hybrid zones during the Pleistocene and the Holocene. No evidence of niche divergence was found, suggesting that species diversification was not driven by ecological speciation but by evolutionary history, though it could be associated to distinct environmental adaptations.

More than one way to evolve a weed: parallel evolution of US weedy rice through independent genetic mechanisms.

Many different crop species were selected for a common suite of 'domestication traits', which facilitates their use for studies of parallel evolution. Within domesticated rice (Oryza sativa), there has also been independent evolution of weedy strains from different cultivated varieties. This makes it possible to examine the genetic basis of parallel weed evolution and the extent to which this process occurs through shared genetic mechanisms. We performed comparative QTL mapping of weediness traits using two recombinant inbred line populations derived from crosses between an indica crop variety and representatives of each of the two independently evolved weed strains found in US rice fields, strawhull (S) and blackhull awned (B). Genotyping-by-sequencing provided dense marker coverage for linkage map construction (average marker interval <0.25 cM), with 6016 and 13 730 SNPs mapped in F5 lines of the S and B populations, respectively. For some weediness traits (awn length, hull pigmentation and pericarp pigmentation), QTL mapping and sequencing of underlying candidate genes confirmed that trait variation was largely attributable to individual loci. However, for more complex quantitative traits (including heading date, panicle length and seed shattering), we found multiple QTL, with little evidence of shared genetic bases between the S and B populations or across previous studies of weedy rice. Candidate gene sequencing revealed causal genetic bases for 8 of 27 total mapped QTL. Together these findings suggest that despite the genetic bottleneck that occurred during rice domestication, there is ample genetic variation in this crop to allow agricultural weed evolution through multiple genetic mechanisms.