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  1. Societal Impact Statement

    Fleshy fruits provide humans with many flavorful and nutritious crops. Understanding the diversity of these plants is fundamental to managing agriculture and food security in a changing world. This study surveyed fruit trait variation across species of tomato wild relatives and explored associations among color, size, shape, sugars, and acids. These wild tomato species native to South America can be interbred with the economically important cultivated tomato. Beyond its application to tomatoes, deepening our knowledge of how fruit traits evolve together is valuable to crop improvement efforts aimed at breeding more nutritious and appealing varieties of fruits.

    Summary

    Fleshy fruits display a striking diversity of traits, many of which are important for agriculture. The evolutionary drivers of this variation are not well understood, and most studies have relied on variation found in the wild. Few studies have explored this question on a fine‐grained scale with a group of recently diverged species while controlling for environmental effects.

    We developed the tomato clade as a novel system for fruit trait evolution research by presenting the first common garden‐based systematic survey of variation and phylogenetic signal in color, nutrition, and morphology traits across all 13 species of tomato wild relatives (Solanum sect.Lycopersicon). We laid the groundwork for further testing of potential evolutionary drivers by assessing patterns of clustering and correlation among disperser‐relevant fruit traits as well as historical climate variables.

    We found evidence of two distinct clusters of associated fruit traits defined by color, sugar type, and malic acid concentration. We also observed correlations between a fruit's external appearance and internal nutrient content that could function as honest signals to dispersers. Analyses of historical climate and soil variables revealed an association between red/orange/yellow fruits and high annual average temperature.

    Our results establish the tomato clade as a promising system for testing hypotheses on the drivers of divergence behind early‐stage fleshy fruit evolution, particularly selective pressure from frugivores.

     
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  2. Abstract

    Weedy rice (Oryzaspp.) 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 fromauscultivated 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 F2population derived from a cross between BHA weedy rice with an ancestralauscultivar. 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.

     
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    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. 
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  5. 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 nativeOryzaspecies, 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 oftemperate japonicacultivars, 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 theRcdomestication 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.

     
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  6. Societal Impact Statement

    Given the rapidly increasing drought and temperature stresses associated with climate change, innovative approaches for food security are imperative. One understudied opportunity is using feral crops—plants that have escaped and persisted without cultivation—as a source of genetic diversity, which could build resilience in domesticated conspecifics. In some cases, however, feral plants vigorously compete with crops as weeds, challenging food security. By bridging historically siloed ecological, agronomic, and evolutionary lines of inquiry into feral crops, there is the opportunity to improve food security and understand this relatively understudied anthropogenic phenomenon.

    Summary

    The phenomenon of feral crops, that is, free‐living populations that have established outside cultivation, is understudied. Some researchers focus on the negative consequences of domestication, whereas others assert that feral populations may serve as useful pools of genetic diversity for future crop improvement. Although research on feral crops and the process of feralization has advanced rapidly in the last two decades, generalizable insights have been limited by a lack of comparative research across crop species and other factors. To improve international coordination of research on this topic, we summarize the current state of feralization research and chart a course for future study by consolidating outstanding questions in the field. These questions, which emerged from the colloquium “Darwins' reversals: What we now know about Feralization and Crop Wild Relatives” at the BOTANY 2021 conference, fall into seven categories that span both basic and applied research: (1) definitions and drivers of ferality, (2) genetic architecture and pathway, (3) evolutionary history and biogeography, (4) agronomy and breeding, (5) fundamental and applied ecology, (6) collecting and conservation, and (7) taxonomy and best practices. These questions serve as a basis for ferality researchers to coordinate research in these areas, potentially resulting in major contributions to food security in the face of climate change.

     
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  7. Abstract

    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.

     
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