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Mobilizing Crop Biodiversity

2020; Elsevier BV; Volume: 13; Issue: 10 Linguagem: Inglês

10.1016/j.molp.2020.08.011

1674-2052

Susan R. McCouch, Zahra-Katy Navabi, Michael Abberton, Noelle L. Anglin, Rosa Lía Barbieri, Michaël Baum, Kirstin E. Bett, Helen M. Booker, Gerald L. Brown, Glenn J. Bryan, Luigi Cattivelli, David Charest, Kellye Eversole, Marcelo Freitas, Kioumars Ghamkhar, Dário Grattapaglia, Robert J Henry, Maria Cleria Valadares Inglis, Tofazzal Islam, Zakaria Kehel, Paul Kersey, Graham J.W. King, Stephen Kresovich, Emily Marden, Sean Mayes, Marie-Noëlle Ndjiondjop, Henry T. Nguyen, Samuel Rezende Paiva, Roberto Papa, Peter W.B. Phillips, Awais Rasheed, Christopher M. Richards, Mathieu Rouard, M. J. A. M. Sampaio, Uwe Scholz, Paul D. Shaw, Brad Sherman, S. Evan Staton, Nils Stein, Jan T. Svensson, Mark Tester, José Francisco Montenegro Valls, Rajeev K. Varshney, S. Visscher, Eric von Wettberg, Robbie Waugh, Peter Wenzl, Loren H. Rieseberg,

Conservation, Biodiversity, and Resource Management

Over the past 70 years, the world has witnessed extraordinary growth in crop productivity, enabled by a suite of technological advances, including higher yielding crop varieties, improved farm management, synthetic agrochemicals, and agricultural mechanization. While this “Green Revolution” intensified crop production, and is credited with reducing famine and malnutrition, its benefits were accompanied by several undesirable collateral effects (Pingali, 2012Pingali P.L. Green Revolution: impacts, limits, and the path ahead.Proc. Natl. Acad. Sci. U S A. 2012; 109: 12302-12308Crossref PubMed Scopus (1016) Google Scholar). These include a narrowing of agricultural biodiversity, stemming from increased monoculture and greater reliance on a smaller number of crops and crop varieties for the majority of our calories. This reduction in diversity has created vulnerabilities to pest and disease epidemics, climate variation, and ultimately to human health (Harlan, 1972Harlan J.R. Genetics of disaster.J. Environ. Qual. 1972; 1: 212-215Crossref Google Scholar). The value of crop diversity has long been recognized (Vavilov, 1992Vavilov N.I. Origin and Geography of Cultivated Plants. Cambridge University Press, New York, NY, USA1992Google Scholar). A global system of genebanks (e.g., www.genebanks.org/genebanks/) was established in the 1970s to conserve the abundant genetic variation found in traditional “landrace” varieties of crops and in crop wild relatives (Harlan, 1972Harlan J.R. Genetics of disaster.J. Environ. Qual. 1972; 1: 212-215Crossref Google Scholar). While preserving crop variation is a critical first step, the time has come to make use of this variation to breed more resilient crops. The DivSeek International Network (https://divseekintl.org/) is a scientific, not-for-profit organization that aims to accelerate such efforts. There are >1750 national and international genebanks worldwide. They house ∼7 million crop germplasm accessions (http://www.fao.org/3/i1500e/i1500e00.htm), including samples of diverse natural populations, with many more managed in situ. These accessions arguably represent one of humanity's greatest treasures, as they contain genetic variation that can be harnessed to create better-tasting, higher-yielding, disease/pest-resistant, and climate-resilient cultivars that require fewer agricultural inputs (Figure 1). Unfortunately, most genebank accessions are poorly characterized, and a small proportion have been utilized in breeding. Yet when a serious effort has been made to search genebanks for traits of interest, the effort has been highly rewarded. Examples include the discovery of a unique rice landrace used to breed submergence-tolerant varieties currently grown on tens of millions of acres (Mackill et al., 2012Mackill D.J. Ismail A.M. Singh U.S. Labios R.V. Paris T.R. Development and rapid adoption of submergence-tolerant (Sub1) rice varieties.Adv. Agron. 2012; 115: 299-352Crossref Scopus (136) Google Scholar) and durable resistance to late blight, a devastating disease of potato, derived from a wild relative (Bernal-Galeano et al., 2020Bernal-Galeano V.N.G. Ellis D. Anglin N.L. Hareau G. Smale M. Jamora N. Alwang J. Pradel W. The effect of Andean potato diversity conserved in the International Potato Center genebank helps develop agriculture in Uganda: the example of Victoria.Food Secur. J. 2020; https://doi.org/10.1007/s12571-020-01037-8Crossref Scopus (4) Google Scholar). Given the high value of the genetic diversity found in crop wild relatives and traditional landraces, why are these genetic resources not more widely used in breeding programs? One reason for the limited use of genebank holdings is the paucity of information about them, which increases the time, expense, and risk associated with mining genebank diversity. To address this deficiency, we support the development of digital catalogs that provide essential information about the genetic composition, phenotypic diversity, and phylogenetic relationships of genebank holdings, along with traditional passport data, images of whole plant morphology, growth habit, physiological data showing response to biotic/abiotic stress, nutrient profiles, and other information where available. Some genebanks have already begun building catalogs of their collections to improve the efficiency of genebank management, as well as to permit users to pre-screen for traits of interest, thereby facilitating variety development (König et al., 2020König P. Beier S. Basterrechea M. Schüler D. Arend D. Mascher M. Stein N. Scholz U. Lange M. Bridge—a visual analytics web tool for barley genebank genomics.Front. Plant Sci. 2020; 11: 701Crossref PubMed Scopus (18) Google Scholar). Another challenge to widespread use of genebank materials is the nature of genetic variation itself. Exotic germplasm often contains valuable cryptic variation, which is revealed only after crosses have been made with cultivated and elite breeding lines (Tanksley and McCouch, 1997Tanksley S.D. McCouch S.R. Seed banks and molecular maps: unlocking genetic potential from the wild.Science. 1997; 277: 1063-1066Crossref PubMed Scopus (1672) Google Scholar). For example, wild populations frequently carry alleles that increase seed, fruit, and tuber size or disease resistance when introduced into cultivars, but these are often masked by genes with opposing effects. Also, some traits that look promising in wild or landrace populations may not be expressed in adapted genetic backgrounds due to quantitative inheritance. In addition, strategies are needed to overcome crossing barriers and to ameliorate the impacts of genetic material that is inadvertently introduced into cultivars along with traits/alleles of interest (i.e., linkage drag). Even when crosses are successful, specific chromosomal segments may fail to introgress if they underlie hybrid incompatibilities or experience reduced recombination, further exacerbating linkage drag (Canady et al., 2006Canady M.A. Ji Y. Chetelat R.T. Homeologous recombination in Solanum lycopersicoides introgression lines of cultivated tomato.Genetics. 2006; 174: 1775-1788Crossref PubMed Scopus (60) Google Scholar). Finally, traits and alleles introgressed from wild germplasm may exhibit incomplete penetrance or unexpected epistatic interactions, forfeiting expected gains from introgressions (Lippman et al., 2007Lippman Z.B. Semel Y. Zamir D. An integrated view of quantitative trait variation using tomato interspecific introgression lines.Curr. Opin. Genet. Development. 2007; 17: 545-552Crossref PubMed Scopus (137) Google Scholar). Sorting through the myriad combinations of alleles generated in wild × elite crosses requires a systematic approach if it is to be productive. The use of structured populations, appropriate experimental designs, and effective use of reference varieties in combination with cost-effective genotyping, high throughput phenotyping, automated data capture, and appropriate analyses make it possible to link genotype with phenotype, identify valuable haplotypes, drive recombination, and make predictions about offspring phenotypes. Techniques that enhance recombination and mitigate crossability barriers offer additional means for accessing diversity from divergent wild relatives while reducing linkage drag (Fernandes et al., 2018Fernandes J.B. Séguéla-Arnaud M. Larchevêque C. Lloyd A.H. Mercier R. Unleashing meiotic crossovers in hybrid plants.Proc. Natl. Acad. Sci. U S A. 2018; 115: 2431-2436Crossref PubMed Scopus (81) Google Scholar). To address these challenges, we encourage communities of researchers to undertake systematic pre-breeding efforts to generate recombinant populations of introgressed lines in adapted cultivated backgrounds, evaluate them in diverse environments, and share the lines and associated information with breeders, farmers, researchers, and policy makers. The long time horizon and uncertainties associated with “pre-breeding” often impede investment from private breeding programs. Therefore, we urge increased investment from foundations and the public sector to support such efforts across major crop families, expanding on recent efforts by the Global Crop Diversity Trust, CGIAR, and other organizations. As products of pre-competitive research, pre-bred lines could be deposited into genetic stock centers and made available to both public and private breeding programs with explicit procedures to fulfill access and benefit-sharing obligations (see below). An alternative approach to pre-breeding involves the use of genome editing, which can be used to re-introduce favorable alleles from wild and exotic relatives into crop plants, purge deleterious alleles, break linkage drag, or create new alleles designed to enhance plant performance and resilience (Zsögön et al., 2018Zsögön A. Cermak T. Naves E. Notini M. Edel K. Weinl S. Freschi L. Voytas D. Kudla J. Peres L. De novo domestication of wild tomato using genome editing.Nat. Biotechnol. 2018; 36: 1211-1216Crossref Scopus (361) Google Scholar; Johnsson et al., 2019Johnsson M. Gaynor R.C. Jenko J. Gorjanc G. de Koning D.-J. Hickey J.M. Removal of alleles by genome editing (RAGE) against deleterious load.Genet. Select. Evol. 2019; 51: 14Crossref PubMed Scopus (30) Google Scholar). This approach allows researchers to explore natural variation as a key to resilience, and its application rests on a deep knowledge of the genetics and evolution of key traits and alleles. The use of genome editing also introduces a need for community and public discussion about regulatory requirements and international agreements to address the complex political, social, legal, and economic concerns surrounding the use of this technology (Lassoued et al., 2019Lassoued R. Macall D.M. Smyth S.J. Phillips P.W.B. Hesseln H. Risk and safety considerations of genome edited crops: expert opinion.Curr. Res. Biotechnol. 2019; 1: 11-21Crossref Scopus (26) Google Scholar). Finally, national and international policies related to benefit sharing derived from the use of plant genetic resources impact how such resources and associated information are collected, stored, regenerated, shared, studied, and used, potentially creating additional obstacles to research and the utilization of crop diversity (McCouch et al., 2013McCouch S. Baute G.J. Bradeen J. Bramel P. Bretting P.K. Buckler E. Burke J.M. Charest D. Cloutier S. Cole G. et al.Feeding the future.Nature. 2013; 499: 23-24Crossref PubMed Scopus (349) Google Scholar; Marden, 2018Marden E. International agreements may impact genomic technologies.Nat. Plants. 2018; 4: 2-4Crossref PubMed Scopus (9) Google Scholar). The International Treaty for Plant Genetic Resources in Food and Agriculture facilitates multi-lateral access to plant genetic resources under mutually agreed-upon terms. It currently covers 64 crops, but ambiguity regarding benefit-sharing requirements limits the use of genebank holdings by many plant breeders, researchers, and farmers (Sherman and Henry, 2020Sherman B. Henry R.J. The Nagoya Protocol and historical collections of plants.Nat. Plants. 2020; 6: 430Crossref PubMed Scopus (12) Google Scholar). There also are concerns that the benefit-sharing provisions of the Treaty somehow conflict with the long-accepted practice of providing open access to genetic sequence data (Marden, 2018Marden E. International agreements may impact genomic technologies.Nat. Plants. 2018; 4: 2-4Crossref PubMed Scopus (9) Google Scholar). In our view, open sharing of information about plant genetic resources represents one essential form of benefit sharing, and provides a critical foundation for capacity building strategies that help address UN sustainable development goals. It is important that those using genomic and phenomic information for crop research and breeding are fully aware of international treaties and comply with their requirements. The DivSeek International Network is a global, community-driven organization that facilitates the generation, integration, and sharing of information related to plant genetic resources, thereby empowering genebank managers, researchers, breeders, and farmers to more effectively utilize genetic variation for research, accelerated crop improvement, and sustainable production. DivSeek comprises ∼65 members from >30 countries, and includes a broad array of academic and research institutions, government agencies, and inter-governmental organizations (https://divseekintl.org/members/). To help achieve its goals, DivSeek has established several Working Groups to engage members and assist them in addressing issues of importance to the DivSeek Community. The activities undertaken by DivSeek's three current Working Groups are summarized below. DivSeek supports open-source genomic-assisted germplasm management and breeding, which represents a decentralized form of empowerment for genebanks and national breeding programs (Santantonio et al., 2020Santantonio N. Atanda S.A. Beyene Y. Varshney R.K. Olsen M. Jones E. Roorkiwal M. Gowda M. Bharadwaj C. Gaur P.M. et al.Strategies for effective use of genomic information in crop breeding programs serving Africa and South Asia.Frontiers in Plant Sci. 2020; 11: 353Crossref PubMed Scopus (23) Google Scholar). Similar to the revolution in information technology that invented the Internet and put cell phones in the hands of people throughout the world, open-source genomics tools, strategies, and datasets are being developed and shared internationally. The tools provide data and information to support decisions about germplasm management and variety development, and the use and iterative improvement of these tools by communities of practice has the power to accelerate the deployment of crop diversity in farmers' fields, helping to address several of the UN's Sustainable Development Goals. DivSeek promotes the use of new technologies for quantitative phenotypic evaluation of plant genetic resources across a network of test environments, and the application of community-based standards, ontologies, and data management practices that help make data findable, accessible, interoperable, and reusable (Pommier et al., 2019Pommier C. Michotey C. Cornut G. Roumet P. Duchêne E. Flores R. Lebreton A. Alaux M. Durand S. Kimmel E. et al.Applying FAIR principles to plant phenotypic data management in GnpIS.Plant Phenomics. 2019; 2019: 1671403Crossref Scopus (24) Google Scholar). Utilizing efficient and affordable technologies will be key to engaging genebanks and plant breeders in modern phenomics-based screening (Mir et al., 2019Mir R.R. Reynolds M. Pinto F. Khan M.A. Bhat M.A. High-throughput phenotyping for crop improvement in the genomics era.Plant Sci. 2019; 282: 60-72Crossref PubMed Scopus (109) Google Scholar). Integration of diverse datasets boosts the power of global efforts to document phenotypic variation found in both genebank accessions and in breeding populations (Roitsch et al., 2019Roitsch T. Cabrera-Bosquet L. Fournier A. et al.New sensors and data-driven approaches—A path to next generation phenomics.Plant Science. 2019; 282: 2-10Crossref PubMed Scopus (92) Google Scholar), and can greatly improve the accuracy of predictions about plant performance across environments. This is especially critical for accelerating the breeding of climate-resilient varieties in vulnerable environments. DivSeek aims to help members of the international plant community to understand the legal and policy framework for sharing information about plant genetic resources, lead discussions about the technological requirements for data sharing across constituencies, and share perspectives on benefit-sharing practices that are aligned with international treaties. All international agreements governing the utilization of plant genetic resources share the same basic objectives: conservation and sustainable use of resources, ease of access to them, and fair and equitable sharing of benefits derived from their use (https://www.cbd.int/; http://www.fao.org/plant-treaty/en/). However, rapid technological developments are changing the way scientists explore, utilize, and exchange information about plant genetic resources, creating new value for the information itself, and new opportunities for access and benefit sharing, while at the same time challenging existing agreements (Marden, 2018Marden E. International agreements may impact genomic technologies.Nat. Plants. 2018; 4: 2-4Crossref PubMed Scopus (9) Google Scholar). In particular, new breeding techniques that can take advantage of genomic and phenotypic data without accessing physical germplasm have led to a debate about open access to sequence data and the best ways to implement benefit-sharing requirements (Laird et al., 2020Laird S. Wynberg R. Rourke M. Humphries F. Muller M.R. Lawson C. Rethink the expansion of access and benefit sharing.Science. 2020; 367: 1200Crossref PubMed Google Scholar). International collaborative partnerships are essential for addressing global challenges, ranging from climate change to the control of pests and diseases to the conservation of biodiversity. DivSeek represents one such global partnership, focusing on the characterization and utilization of agricultural biodiversity and its impact on food and nutritional security. The success of DivSeek will depend on attracting a broad coalition of members, observers, and stakeholders dedicated to discussion and constructive exchange of ideas, perspectives, and expertise. We are pleased to invite the global agricultural science community to join the DivSeek International Network, either as members or observers (https://divseekintl.org/apply-to-join/). By joining forces, we can mobilize the value of crop diversity to sustainably improve yields in farmers' fields and ensure that the benefits of our efforts are equitably distributed across the globe. No conflict of interest declared.