Abstract
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.
Highlights
De novo domestication of new crops from currently wild plants could help solve a wide range of problems, including genetic and species diversification of agricultural systems (Fernie and Yan, 2019); expansion of agricultural production onto degraded sites, stressful environments, or regions highly vulnerable to climatic extremes (Zhang et al, 2018); improvement of the fit between crops and particular local ecological niches (Fernie and Yan, 2019); and intensification of the range of vital ecosystem services provided by crops (Weißhuhn et al, 2017)
We provide a practical framework that highlights and integrates multiple drivers of change (Figure 1) to conceptualize de novo domestication for communities of new crop domesticators, growers and consumers
Gene editing approaches to domestication using domestication genes” (DGs) risk portraying a misunderstanding of de novo crop domestication as something humans do to wild plants in a simple onetime event, in a single gene or generation, using increasingly cheap technology, and drawing from just a few scientific disciplines
Summary
De novo domestication of new crops from currently wild plants could help solve a wide range of problems, including genetic and species diversification of agricultural systems (Fernie and Yan, 2019); expansion of agricultural production onto degraded sites, stressful environments, or regions highly vulnerable to climatic extremes (Zhang et al, 2018); improvement of the fit between crops and particular local ecological niches (Fernie and Yan, 2019); and intensification of the range of vital ecosystem services provided by crops (Weißhuhn et al, 2017). The availability of new tools such as CRISPR, and the possibility of applying them toward de novo domestication of novel crops, could be misunderstood by society to mean that gene editing can produce domestication as a nearly instant and/or inexpensive event, failing to recognize the many years of foundational research that was required to characterize and identify candidate genes and develop transformation and tissue culture regeneration systems (Van Eck, 2018). Agronomic, and cultural change drive cycles of selective pressures that result in the fixation of domestication genes – and broad genetic changes, innovations in management, and social support may all be required to enable domestication processes to continue at different pivotal moments and for the long term across human generations and geographies (Table 1). To realize the ecological and social benefits that a new era of de novo food crop domestication could offer, it is necessary to recognize how genetic, agronomic, and cultural changes remain co-evolutionarily entangled (Figure 2)
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