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The emerging bioeconomy will increase the need for plant biomass. We call for a third-generation of bioenergy crops, or biomass crops, to help move society towards a sustainable bioeconomy and global food security. Third-generation biomass crops should be capable of producing both food and raw materials. Such flexibility would allow farmers to respond to global markets and buffer global food security. At the same time, third-generation biomass crops need to increase the sustainability of agriculture. To reach such ambitious goals, new biomass crops have to develop de novo from promising perennial wild species.

International audience; De novo domestication has received recent attention because of the potential to produce new crop species with additional agroecosystem functions and useful products for climate-resilient agricultural systems of the future. However, there are often traits in wild species that make them difficult to domesticate. One key domestication trait selected by early farmers and modern plant breeders in many crops is the ability to self-pollinate. Benefits include higher seed set and more reliable seed production, as well as more efficient selection during breeding because it allows for unmasking of recessive traits and enforcement of favorable gene interactions. Similarly, interspecific hybridization has been used to add to the genetic diversity of many crop species. We evaluated self-pollination and interspecific hybridization in Silphium integrifolium and S. perfoliatum to learn the extent of possible gene flow between the species and its usefulness in cultivar development and the potential for fixation of favorable domestication genes by self-pollination. Our results indicate that Silphium interspecific hybrids can be easily developed, potentially facilitating movement of otherwise invariable traits from one species to another. Further, we showed, for the first time, that self-pollination is also possible in both species and their interspecific hybrids, but the rate varies among genotypes. This has profound implications in optimizing plant breeding methods for the study and improvement of these species and adds more evidence to our understanding of mating systems in Asteraceae, an underutilized family of plants with great potential for additional domesticated species.

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.

In the interest of diversifying the global food system, improving human nutrition, and making agriculture more sustainable, there have been many proposals to domesticate wild plants or complete the domestication of semidomesticated orphan crops. However, very few new crops have recently been fully domesticated. Many wild plants have traits limiting their production or consumption that could be costly and slow to change. Others may have fortuitous preadaptations that make them easier to develop or feasible as high-value, albeit low-yielding, crops. To increase success in contemporary domestication of new crops, we propose a pipeline approach, with attrition expected as species advance through the pipeline. We list criteria for ranking domestication candidates to help enrich the starting pool with more preadapted, promising species. We also discuss strategies for prioritizing initial research efforts once the candidates have been selected: developing higher value products and services from the crop, increasing yield potential, and focusing on overcoming undesirable traits. Finally, we present new-crop case studies that demonstrate that wild species’ limitations and potential (in agronomic culture, shattering, seed size, harvest, cleaning, hybridization, etc.) are often only revealed during the early phases of domestication. When nearly insurmountable barriers were reached in some species, they have been (at least temporarily) eliminated from the pipeline. Conversely, a few species have moved quickly through the pipeline as hurdles, such as low seed weight or low seed number per head, were rapidly overcome, leading to increased confidence, farmer collaboration, and program expansion. Fil: DeHaan, Lee R.. The Land Institute; Estados Unidos Fil: Van Tassel, David L.. The Land Institute; Estados Unidos Fil: Anderson, James A.. University of Minnesota; Estados Unidos Fil: Asselin, Sean R.. University of Manitoba; Canadá Fil: Barnes, Richard. University of Minnesota; Estados Unidos Fil: Baute, Gregory J.. University of British Columbia; Canadá Fil: Cattani, Douglas J.. University of Manitoba; Canadá Fil: Culman, Steve W.. Ohio State University; Estados Unidos Fil: Dorn, Kevin M.. University of Minnesota; Estados Unidos Fil: Hulke, Brent S.. United States Department of Agriculture. Agriculture Research Service; Estados Unidos Fil: Kantar, Michael. University of British Columbia; Canadá Fil: Larson, Steve. Forage and Range Research Laboratory; Estados Unidos Fil: David Marks, M.. University of Minnesota; Estados Unidos Fil: Miller, Allison J.. Saint Louis University; Estados Unidos Fil: Poland, Jesse. Kansas State University; Estados Unidos Fil: Ravetta, Damián Andrés. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Museo Paleontológico Egidio Feruglio; Argentina Fil: Rude, Emily. University of Wisconsin; Estados Unidos Fil: Ryan, Matthew R.. Cornell University; Estados Unidos Fil: Wyse, Don. University of Minnesota; Estados Unidos Fil: Zhang, Xiaofei. University of Minnesota; Estados Unidos

SummaryConcerns about soil health and stability are focusing attention on crops that deliver both agricultural products and ecological services. Deep rooted, perennial plants that build soil organic matter, support diverse below-ground microbial communities, and produce edible seeds are key components underpinning ecological intensification; however few perennial, herbaceous crops have been domesticated for food.To facilitate development of edible, perennial, herbaceous crops, including perennial grains, we constructed an online resource of wild, perennial, herbaceous species – the Perennial Agriculture Project Global Inventory (PAPGI; http://www.tropicos.org/Project/PAPGI). The first component of this project focuses on wild, perennial, herbaceous Fabaceae species. We extracted taxonomic names and descriptors from the International Legume Database and Information Service. Names were added to PAPGI, a special project within the botanical database TROPICOS, where they link to specimen records and ethnobotanical and toxicological data. PAPGI includes 6,644 perennial, herbaceous Fabaceae species. We built a searchable database of more than 60 agriculturally important traits. Here we highlight food and forage uses for 314 legume species, and toxicological data for 278 species.The novel contribution of PAPGI is its focus on wild, perennial herbaceous species that generally have not entered the domestication process but that hold promise for development as perennial food crops. By extracting botanical information relevant for agriculture we provide a dynamic resource for breeders and plant scientists working to advance ecological intensification of agriculture, and for conservation managers working to preserve wild species of potential agricultural importance.Societal Impact StatementAgroecosystems are constantly evolving to meet the needs of a growing population in a sustainable manner. Perennial, herbaceous crops deliver both agricultural products and ecological services. Until recently, edible, perennial, herbaceous crops, including perennial grains, were absent from agriculture. Perennial, herbaceous crops can be developed through wide hybridization between annual crops and perennial relatives or by de novo domestication of wild species. The diversity of wild, perennial, herbaceous legume species documented by the PAPGI increases resources available to breeders of perennial, herbaceous legumes, and raises awareness about previously untapped wild plant diversity in future crop development.

Climatic change will seriously impact Mediterranean areas. Palestine, which has given forth annual grain based agriculture, is particularly vulnerable given its political and economic situation. Research is needed to build climate adaptation and resilience into agroecosystems within the same landscape that gave forth agriculture. A primary step in achieving that adaptation is to develop polycultures composed of perennial crops to protect and rebuild the soil. Our preliminary research shows that agrobiodiversity and genetic material for this deep adaptation is already present within the landscape, and if developed could produce the new crops used to build perennial polycultures.

Silflower (Silphium integrifolium Michx.) is in the early stages of domestication as a perennial version of oilseed sunflower, its close relative. Grain crops with deep perennial root systems will provide farmers with new alternatives for managing soil moisture and limiting or remediating soil erosion, fertilizer leaching, and loss of soil biota. Several cycles of selection for increased seed production potential following initial germplasm evaluation in 2002 have provided opportunities to document the botany and ecology of this relatively obscure species, to compare agronomic practices for improving its propagation and management, and to evaluate the differences between semi-domesticated and wild accessions that have accrued over this time through intentional and unintentional genetic processes. Key findings include: domestication has increased aboveground biomass at seedling and adult stages; seed yield has increased more, achieving modest improvement in harvest index. Harvest index decreases with nitrogen fertilization. Silflower acquires nitrogen and water from greater depth than typical crops. In agricultural silflower stands within its native range, we found that Puccinia silphii (rust) and Eucosma giganteana (moth) populations build up to unacceptable levels, but we also found genetic variation for traits contributing to resistance or tolerance. Breeding or management for reduced height and vegetative plasticity should be top priorities for future silflower research outside its native range. Fil: Vilela, Alejandra Elena. Museo Paleontológico Egidio Feruglio; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: González Paleo, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Museo Paleontológico Egidio Feruglio; Argentina Fil: Turner, Kathryn. The Land Institute; Estados Unidos Fil: Peterson, Kelsey. The Land Institute; Estados Unidos Fil: Ravetta, Damián Andrés. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Museo Paleontológico Egidio Feruglio; Argentina Fil: Crews, Timothy E.. The Land Institute; Estados Unidos Fil: Van Tassel, David. The Land Institute; Estados Unidos

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.

Humanity depends on fewer than a dozen of the approximately 300,000 species of flowering plants for 80% of its caloric intake. And we capitalize on only a fraction of the genetic diversity that resides within each of these species. This is not enough to support our food system in the future. Food availability must double in the next 25 years to keep pace with population and income growth around the world. Already, food-production systems are precarious in the face of intensifying demand, climate change, soil degradation and water and land shortages. Farmers have saved the seeds of hundreds of crop species and hundreds of thousands of ‘primitive’ varieties (local domesticates called landraces), as well as the wild relatives of crop species and modern varieties no longer in use. These are stored in more than 1,700 gene banks worldwide. Maintaining the 11 international gene-bank collections alone costs about US$18 million a year.