Assessing effective mechanical and chemical strategies for managing Eucosma giganteana (Lepidoptera: Tortricidae) in the perennial oilseed crop, Silphium integrifolium (Asteraceae: Heliantheae).

Eucosma giganteana (Riley) is a native specialist pest of silflower, Silphium integrifolium Michx., which is currently being domesticated as a perennial oilseeds crop. The larvae of this moth attack silflower capitula and root crowns, causing both seed damage and long-term degradation of plants. To determine methods to manage E. giganteana in silflower crop fields, we conducted a laboratory bioassay and 3 field experiments to assess the effects of a suite of organic, conventional, and mechanical treatments on E. giganteana mortality and colonization of flower heads. Pyrethroids (permethrin, cyfluthrin), chlorantraniliprole, and methoxyfenozide each had significant insecticidal effects on E. giganteana in at least 2 of the experiments conducted. Nematodes marginally increased larva mortality in the laboratory bioassay and could be further investigated as a soil-applied biological control. In 2 separate field experiments, trimming the top 15% of silflower plants to delay flowering did not alone reduce E. giganteana colonization of flower heads throughout the growing season. However, when trimming was paired with a single chlorantraniliprole application, colonization of capitula was reduced by 83% over untreated control plants. Collectively, these experiments provide evidence for several treatments that could be further tested and incorporated into an integrated pest management strategy for E. giganteana.

The next era of crop domestication starts now.

Current food systems are challenged by relying on a few input-intensive, staple crops. The prioritization of yield and the loss of diversity during the recent history of domestication has created contemporary crops and cropping systems that are ecologically unsustainable, vulnerable to climate change, nutrient poor, and socially inequitable. For decades, scientists have proposed diversity as a solution to address these challenges to global food security. Here, we outline the possibilities for a new era of crop domestication, focused on broadening the palette of crop diversity, that engages and benefits the three elements of domestication: crops, ecosystems, and humans. We explore how the suite of tools and technologies at hand can be applied to renew diversity in existing crops, improve underutilized crops, and domesticate new crops to bolster genetic, agroecosystem, and food system diversity. Implementing the new era of domestication requires that researchers, funders, and policymakers boldly invest in basic and translational research. Humans need more diverse food systems in the Anthropocene-the process of domestication can help build them.

Development of first linkage map for Silphium integrifolium (Asteraceae) enables identification of sporophytic self-incompatibility locus.

Silphium integrifolium (Asteraceae) has been identified as a candidate for domestication as a perennial oilseed crop and is assumed to have sporophytic self-incompatibility system-the genetic basis of which is not well understood in the Asteraceae. To address this gap, we sought to map the genomic location of the self-recognition locus (S-locus) in this species. We used a biparental population and genotyping-by-sequencing to create the first genetic linkage map for this species, which contained 198 SNP markers and resolved into the correct number of linkage groups. Then we developed a novel crossing scheme and set of analysis methods in order to infer S-locus genotypes for a subset of these individuals, allowing us to map the trait. Finally, we evaluated potential genes of interest using synteny analysis with the annual sunflower (Helianthus annuus) and lettuce (Lactuca sativa) genomes. Our results confirm that S. integrifolium does indeed have a sporophytic self-incompatibility system. Our method is effective and efficient, allowed us to map the S. integrifolium S-locus using fewer resources than existing methods, and could be readily applied to other species.

Weight Gain of Spodoptera frugiperda Larvae (Lepidoptera: Noctuidae) on Leaf and Floral Tissues of Silphium integrifolium (Asterales: Asteraceae) Differs by Plant Genotype.

Silflower (Silphium integrifolium (Michaux)) is a native North American relative of sunflower that is undergoing domestication as a perennial oilseed crop. As silflower incurs pest damage from multiple insect species, it is necessary to screen genotypes for their effect on insect performance such that more pest tolerant/resistant accessions can be incorporated into future silflower breeding programs. We present a bioassay protocol for silflower using the generalist herbivore fall armyworm (Spodoptera frugiperda (J. E. Smith)). In this study, fall armyworm larvae were placed on leaf and flower tissue from eleven silflower genotypes, one cup plant (Silphium perfoliatum (L.) (Asterales: Asteraceae)) genotype, and an inbred sunflower line (Helianthus annuus (L.) (Asterales: Asteraceae), HA89). Caterpillar weight gained during a 4-d feeding period significantly differed on leaf and floral tissue from different silflower genotypes, between the Silphium species (silflower and cup plant), and between Silphium genotypes and annual sunflower. Two wild silflower genotypes produced lower larval weight gain on both the floral and leaf tissue than all other genotypes, suggesting these genotypes have either lower nutrition or greater resistance to fall armyworm. However, nonsignificant correlations between larval growth on floral versus leaf tissue across all plant species tested and among all silflower accessions suggest insect performances on these tissue types in silflower are independent. Along with identifying germplasm of interest for silflower breeding programs, we established an easily replicable bioassay protocol using fall armyworm on silflower floral and leaf tissues.

Re-imagining crop domestication in the era of high throughput phenomics.

De novo domestication is an exciting option for increasing species diversity and ecosystem service functionality of agricultural landscapes. Genomic selection (GS), the application of genomic markers to predict phenotypic traits in a breeding population, offers the possibility of rapid genetic improvement, making GS especially attractive for modifying traits of long-lived species. However, for some wild species just entering the domestication pipeline, especially those with large and complex genomes, a lack of funding and/or prior genome characterization, GS is often out of reach. High throughput phenomics has the potential to augment traditional pedigree selection, reduce costs and amplify impacts of genomic selection, and even create new predictive selection approaches independent of sequencing or pedigrees.

Patterns of genetic variation in a prairie wildflower, Silphium integrifolium, suggest a non-prairie origin and locally adaptive variation.

PREMISE: Understanding the relationship between genetic structure and geography provides information about a species' history and can be used for breeding and conservation goals. The North American prairie is interesting because of its recent origin and subsequent fragmentation. Silphium integrifolium, an iconic perennial American prairie wildflower, is targeted for domestication, having undergone a few generations of improvement. We present the first application of population genetic data in this species to address the following goals: (1) improve breeding by characterizing genetic structure and (2) identify the species geographic origin and potential targets and drivers of selection during range expansion. METHODS: We developed a reference transcriptome as a genotyping reference for samples from throughout the species range. Population genetic analyses were used to describe patterns of genetic variation, and demographic modeling was used to characterize potential processes that shaped variation. Outlier scans for selection and associations with environmental variables were used to identify loci linked to putative targets and drivers of selection. RESULTS: Genetic variation partitioned samples into three geographic clusters. Patterns of variation and demographic modeling suggest that the species origin is in the American Southeast. Breeding program accessions are from the region with lowest observed genetic variation. CONCLUSIONS: This prairie species did not originate within the prairie. Breeding may be improved by including accessions from outside of the germplasm founding region. The geographic structuring and the identified targets and drivers of adaptation can guide collecting efforts toward populations with beneficial agronomic traits.

New Food Crop Domestication in the Age of Gene Editing: Genetic, Agronomic and Cultural Change Remain Co-evolutionarily Entangled.

The classic domestication scenario for grains and fruits has been portrayed as the lucky fixation of major-effect "domestication genes." Characterization of these genes plus recent improvements in generating novel alleles (e.g., by gene editing) have created great interest in de novo domestication of new crops from wild species. While new gene editing technologies may accelerate some genetic aspects of domestication, we caution that de novo domestication should be understood as an iterative process rather than a singular event. Changes in human social preferences and relationships and ongoing agronomic innovation, along with broad genetic changes, may be foundational. Allele frequency changes at many loci controlling quantitative traits not normally included in the domestication syndrome may be required to achieve sufficient yield, quality, defense, and broad adaptation. The environments, practices and tools developed and maintained by farmers and researchers over generations contribute to crop yield and success, yet those may not be appropriate for new crops without a history of agronomy. New crops must compete with crops that benefit from long-standing participation in human cultural evolution; adoption of new crops may require accelerating the evolution of new crops' culinary and cultural significance, the emergence of markets and trade, and the formation and support of agricultural and scholarly institutions. We provide a practical framework that highlights and integrates these genetic, agronomic, and cultural drivers of change to conceptualize de novo domestication for communities of new crop domesticators, growers and consumers. Major gene-focused domestication may be valuable in creating allele variants that are critical to domestication but will not alone result in widespread and ongoing cultivation of new crops. Gene editing does not bypass or diminish the need for classical breeding, ethnobotanical and horticultural knowledge, local agronomy and crop protection research and extension, farmer participation, and social and cultural research and outreach. To realize the ecological and social benefits that a new era of de novo domestication could offer, we call on funding agencies, proposal reviewers and authors, and research communities to value and support these disciplines and approaches as essential to the success of the breakthroughs that are expected from gene editing techniques.

Genetic Analysis of Domestication Parallels in Annual and Perennial Sunflowers (Helianthus spp.): Routes to Crop Development.

Parallels exist between the domestication of new species and the improvement of various crops through selection on traits which favor the sowing, harvest and retention of yield potential and the directed efforts to improve their agronomics, disease resistance and quality characteristics. Common selection pressures may result in the parallel selection of orthologs underlying these traits and homologies between crop species can be exploited by plant breeders to improve germplasm. Perennial grains and oilseeds are a class of proposed crops for improving the diversity and sustainability of agricultural systems. Maximilian sunflower (Helianthus maximiliani Schrad.) is a perennial crop wild relative of sunflower (Helianthus annuus L.) and a candidate perennial oilseed species. Understanding parallels between cultivated H. annuus and H. maximiliani may provide new tools for the development of Maximilian sunflower and other wild relatives of sunflower as crops to enhance functional diversity in cropping systems. F2 populations of Maximilian sunflower segregating for traits associated with the domestication ideotype of cultivated sunflower including branching architecture, capitulum morphology and flowering time were developed to investigate parallels between H. maximiliani and H. annuus. Genotype-by-sequencing (GBS) was employed to genotype novel Maximilian sunflower populations and perform quantitative-trait-loci (QTL) analysis. A total of 11 QTL in five regions were identified across 21 linkage groups using 4142 GBS derived single nucleotide polymorphism markers called using the sunflower reference genome as a guide. A major QTL on linkage group 17b, associated with aspects of floral development and apical dominance, was discovered and corresponds with a known domestication QTL hotspot in H. annuus and candidate genes were identified. This suggests the potential to exploit orthologs for neo-domestication of H. maximiliani for traits such as branching architecture, timing of anthesis, and capitulum size and morphology for the development of a perennial oilseed crop from wild relatives of cultivated sunflower.

Comparative Analysis of Early Life Stage Traits in Annual and Perennial Phaseolus Crops and Their Wild Relatives.

Herbaceous perennial species are receiving increased attention for their potential to provide both edible products and ecosystem services in agricultural systems. Many legumes (Fabaceae Lindl.) are of special interest due to nitrogen fixation carried out by bacteria in their roots and their production of protein-rich, edible seeds. However, herbaceous perennial legumes have yet to enter widespread use as pulse crops, and the response of wild, herbaceous perennial species to artificial selection for increased seed yield remains under investigation. Here we compare cultivated and wild accessions of congeneric annual and herbaceous perennial legume species to investigate associations of lifespan and cultivation with early life stage traits including seed size, germination, and first year vegetative growth patterns, and to assess variation and covariation in these traits. We use "cultivated" to describe accessions with a history of human planting and use, which encompasses a continuum of domestication. Analyses focused on three annual and four perennial species of the economically important genus Phaseolus. We found a significant association of both lifespan and cultivation status with seed size (weight, two-dimensional lateral area, length), node number, and most biomass traits (with cultivation alone showing additional significant associations). Wild annual and perennial accessions primarily showed only slight differences in trait values. Relative to wild forms, both cultivated annual and cultivated perennial accessions exhibited greater seed size and larger overall vegetative size, with cultivated perennials showing greater mean trait differences relative to wild accessions than cultivated annuals. Germination proportion was significantly lower in cultivated relative to wild annual accessions, while no significant difference was observed between cultivated and wild perennial germination. Regardless of lifespan and cultivation status, seed size traits were positively correlated with most vegetative traits, and all biomass traits examined here were positively correlated. This study highlights some fundamental similarities and differences between annual and herbaceous perennial legumes and provides insights into how perennial legumes might respond to artificial selection compared to annual species.

Useful insights from evolutionary biology for developing perennial grain crops.

Annual grain crops dominate agricultural landscapes and provide the majority of calories consumed by humanity. Perennial grain crops could potentially ameliorate the land degradation and off-site impacts associated with annual grain cropping. However, herbaceous perennial plants with constitutively high allocation to harvestable seeds are rare to absent in nature. Recent trade-off theory models suggest that rugged fitness landscapes may explain the absence of this form better than sink competition models. Artificial selection for both grain production and multiyear lifespan can lead to more rapid progress in the face of fitness and genetic trade-offs than natural selection but is likely to result in plant types that differ substantially from all current domestic crops. Perennial grain domestication is also likely to require the development of selection strategies that differ from published crop breeding methods, despite their success in improving long-domesticated crops; for this purpose, we have reviewed literature in the areas of population and evolutionary genetics, domestication, and molecular biology. Rapid domestication will likely require genes with large effect that are expected to exhibit strong pleiotropy and epistasis. Cryptic genetic variation will need to be deliberately exposed both to purge mildly deleterious alleles and to generate novel agronomic phenotypes. We predict that perennial grain domestication programs will benefit from population subdivision followed by selection for simple traits in each subpopulation, the evaluation of very large populations, high selection intensity, rapid cycling through generations, and heterosis. The latter may be particularly beneficial in the development of varieties with stable yield and tolerance to crowding.

Missing domesticated plant forms: can artificial selection fill the gap?

In the course of their evolution, the angiosperms have radiated into most known plant forms and life histories. Their adaptation to a recently created habitat, the crop field, produced a novel form: the plant that allocates an unprecedented 30-60% of its net productivity to sexual structures. Long-lived trees, shrubs and vines of this form evolved, as did annual herbs. Perennial herb forms with increased allocation to asexual reproduction evolved, but there are no examples of perennial herbs with high sexual effort. We suggest that sowing seed into annually tilled fields favored shorter-lived herbs because of trade-offs between first-year seed production and relative growth rate and/or persistence. By propagating cuttings, people quickly domesticated tuber crops and large woody plants. Perennial herbs were too small to be efficiently propagated by cuttings, and the association between longevity, allogamy and genetic load made rapid domestication by sexual cycles unlikely. Perennial grain crops do not exist because they could not have evolved under the original set of conditions; however, they can be deliberately developed today through artificial phenotypic and genotypic selection.