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

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          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.

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          Most cited references88

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          CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture

          Enhanced agricultural production through innovative breeding technology is urgently needed to increase access to nutritious foods worldwide. Recent advances in CRISPR/Cas genome editing enable efficient targeted modification in most crops, thus promising to accelerate crop improvement. Here, we review advances in CRISPR/Cas9 and its variants and examine their applications in plant genome editing and related manipulations. We highlight base-editing tools that enable targeted nucleotide substitutions and describe the various delivery systems, particularly DNA-free methods, that have linked genome editing with crop breeding. We summarize the applications of genome editing for trait improvement, development of techniques for fine-tuning gene regulation, strategies for breeding virus resistance, and the use of high-throughput mutant libraries. We outline future perspectives for genome editing in plant synthetic biology and domestication, advances in delivery systems, editing specificity, homology-directed repair, and gene drives. Finally, we discuss the challenges and opportunities for precision plant breeding and its bright future in agriculture.
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            Evolution of crop species: genetics of domestication and diversification.

            Domestication is a good model for the study of evolutionary processes because of the recent evolution of crop species (<12,000 years ago), the key role of selection in their origins, and good archaeological and historical data on their spread and diversification. Recent studies, such as quantitative trait locus mapping, genome-wide association studies and whole-genome resequencing studies, have identified genes that are associated with the initial domestication and subsequent diversification of crops. Together, these studies reveal the functions of genes that are involved in the evolution of crops that are under domestication, the types of mutations that occur during this process and the parallelism of mutations that occur in the same pathways and proteins, as well as the selective forces that are acting on these mutations and that are associated with geographical adaptation of crop species.
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              Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops.

              Domesticated food crops are derived from a phylogenetically diverse assemblage of wild ancestors through artificial selection for different traits. Our understanding of domestication, however, is based upon a subset of well-studied 'model' crops, many of them from the Poaceae family. Here, we investigate domestication traits and theories using a broader range of crops. We reviewed domestication information (e.g. center of domestication, plant traits, wild ancestors, domestication dates, domestication traits, early and current uses) for 203 major and minor food crops. Compiled data were used to test classic and contemporary theories in crop domestication. Many typical features of domestication associated with model crops, including changes in ploidy level, loss of shattering, multiple origins, and domestication outside the native range, are less common within this broader dataset. In addition, there are strong spatial and temporal trends in our dataset. The overall time required to domesticate a species has decreased since the earliest domestication events. The frequencies of some domestication syndrome traits (e.g. nonshattering) have decreased over time, while others (e.g. changes to secondary metabolites) have increased. We discuss the influences of the ecological, evolutionary, cultural and technological factors that make domestication a dynamic and ongoing process. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 June 2020
                2020
                : 11
                : 789
                Affiliations
                [1] 1The Land Institute , Salina, KS, United States
                [2] 2Department of Geography, Birzeit University , Birzeit, Palestine
                [3] 3Donald Danforth Plant Science Center , St. Louis, MO, United States
                Author notes

                Edited by: Eric Von Wettberg, The University of Vermont, United States

                Reviewed by: Ashley DuVal, Mars, United States; Edward Marques, The University of Vermont, United States

                *Correspondence: Aubrey Streit Krug, streitkrug@ 123456landinstitute.org

                This article was submitted to Plant Breeding, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.00789
                7300247
                32595676
                6ef53c6f-e73e-4a33-b2d6-263ee96845f7
                Copyright © 2020 Van Tassel, Tesdell, Schlautman, Rubin, DeHaan, Crews and Streit Krug.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 06 January 2020
                : 18 May 2020
                Page count
                Figures: 2, Tables: 3, Equations: 0, References: 137, Pages: 16, Words: 0
                Categories
                Plant Science
                Hypothesis and Theory

                Plant science & Botany
                domestication,coevolution,gene editing,agronomy,cultural evolution,new crops
                Plant science & Botany
                domestication, coevolution, gene editing, agronomy, cultural evolution, new crops

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