Published November 21, 2019 RESEARCH Botanic Gardens Are Important Contributors to Crop Wild Relative Preservation Abby Meyer* and Nicholas Barton Botanic Gardens Conservation International US at at The Huntington ABSTRACT Library, Art Museum, and Botanical Gardens, 1151 Oxford Rd., San Humans rely on crop wild relatives (CWRs) for Marino, CA 91108. Received 2 June 2019. Accepted 11 Oct. 2019. sustainable agriculture and food security through *Corresponding author ([email protected]). Assigned to Associate augmentation of crop yield, disease resistance, Editor Joseph Robins. and climatic tolerance, among other important Abbreviations: BGCI, Botanic Gardens Conservation International; traits. Many CWRs are underrepresented in crop CWR, crop wild relative; GRIN, Germplasm Resources Information gene banks. With at least one-third of known Network. plant species maintained in botanic garden living collections, the botanic garden community serves as an important global ex situ network rop wild relatives (CWRs), plants that have “an indirect that supports plant conservation and research Cuse derived from its relatively close genetic relationship to a around the world. We sought to characterize crop,” provide important genetic diversity needed by breeders and botanic garden holdings of CWRs and demon- scientists to develop a wide range of crop plant adaptations (Maxted strate capacity for cross-sector coordination in et al., 2006, p. 2680). Benefits such as increased production, better support of CWR ex situ preservation. To do this, nutrition, drought tolerance, and pest and disease resistance have Botanic Gardens Conservation International been made possible through the use of CWRs and allowed for US (BGCI-US), in partnership with the United more consistent and sustainable yields of conventional crops for States Botanic Garden, used the BGCI Plant- Search database to conduct an ex situ survey of decades (Dempewolf et al., 2017; Guarino and Lobell, 2011; Hajjar CWRs maintained in botanic gardens. We found and Hodgkin, 2007; Maxted et al., 2006, 2012). Like many plant 28.6% of global priority CWR taxa and 75.4% species, CWRs face several threats including climate change, of US priority CWR taxa represented in botanic habitat fragmentation and degradation, invasive species, overex- gardens. By comparing with priority CWR ploitation, and agricultural expansion (Kell et al., 2012; Vincent holdings in crop gene banks, botanic gardens et al., 2013). Studies have found that significant ex situ gaps exist maintain 22 global priority and 108 US priority among crop gene bank collections of CWRs (Castañeda-Álvarez et CWR taxa not reported by crop gene banks. al., 2016; Khoury et al., 2019). Findings by Castañeda-Álvarez et al. A combination of crop gene bank and botanic (2016), for example, that nearly one-third of global CWRs have no garden holdings results in broader taxonomic ex situ germplasm accessions, and <5% are considered adequately coverage. Looking more closely at 10 US priority represented in crop gene banks, suggest that the current ability to CWR species, findings demonstrate that botanic adequately preserve CWRs in crop gene banks is lacking. gardens have the capacity to fill critical CWRs gaps in crop gene bank collections, and botanic Botanic garden holdings include the use of living plant speci- gardens maintain samples from wild popula- mens in traditional display beds indoors or outdoors, as well as tions not represented in crop gene banks. We nursery collections, common garden plantings, seed orchards, call on the crop gene bank and botanic garden or field gene banks, as well as a growing number of world-class communities to use an integrated collections development approach for further coordina- Published in Crop Sci. 59:2404–2412 (2019). tion, complementarity, and duplication of ex situ doi: 10.2135/cropsci2019.06.0358 CWR plant genetic resources. © 2019 The Author(s). This is an open access article distributed under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 2404 WWW.CROPS.ORG CROP SCIENCE, VOL. 59, NOVEMBER–DECEMBER 2019 facilities with preserved tissues and seed accessions. The with native distributions in the United States, many of which origin, or source, of plant material maintained in botanic have been assessed as threatened in the wild (Khoury et al., 2013). Both lists were aligned with synonyms based on Germ- gardens can vary broadly, from cultivated or horticul- plasm Resources Information Network (GRIN) Taxonomy tural origin, to documented wild origin. The PlantSearch (USDA-ARS-NPGS, 2018b) to ensure a comprehensive cross- database is used to network and connect >1100 botanic reference of botanic garden holdings. garden living plant, seed, and tissue collections around The Botanic Gardens Conservation International (BGCI) the world (BGCI, 2018). PlantSearch reveals that botanic PlantSearch database, a taxon-level, global repository of botanic gardens maintain at least 30% of all known plant species garden collections data, includes nearly 1.5 million collection in ex situ collections, including >41% of species assessed as records from >1100 botanic garden living plant, tissue, and seed globally threatened (Mounce et al., 2017). In the United bank collections worldwide. PlantSearch is used to track ex situ States, botanic gardens maintain an estimated 40% of conservation progress for threatened and priority plant taxa native threatened plant species (Kramer et al., 2011). (BGCI, 2018). PlantSearch also connects thousands of online While many botanic gardens maintain plant collections research requests for information and material to botanic garden with ornamental and aesthetic value for public enjoy- collection managers each year. Each taxon record reported by an institution to PlantSearch means that at least one accession ment, a growing number of botanic gardens around the and at least one living or viable specimen is present in that world collect and maintain genetically diverse and wild- garden’s collection. To assess representation of CWRs in living origin plant material to support research and conservation collections maintained in botanic gardens, the CWR lists were (Dosmann and Groover, 2012; Friedman et al., 2016). matched with plant names reported to PlantSearch as of May When combined, these collections form a metacollection 2018. The resulting inventory allowed us to analyze presence of plants that can be maintained, augmented, and shared and absence of priority CWRs maintained in botanic gardens. in coordinated and intentional ways to support research We also compared botanic garden holdings with crop gene and conservation (Griffith et al., 2019). bank holdings to assess complementarity and potential synergy The globally distributed network of botanic gardens between the botanic garden and crop gene bank communi- serves as an important safety net for wild plant genetic ties. To do this, we used a list of active accessions in Genesys, resources, as well as valuable contributors to ongoing a database of plant genetic resources for food and agriculture dialogues within the scientific community and the general maintained in gene banks worldwide (Genesys, 2019). We also sought to characterize infraspecific diversity public. The ex situ metacollection of wild species main- and documentation of botanic garden holdings of CWRs, so tained in botanic gardens likely includes CWR germplasm we selected 10 species from the US priority CWR list from valuable for the future of crop breeding and food security. Khoury et al. (2013) for a more detailed look at accessions Botanic gardens also offer world-class facilities and exper- provenance. The target species were selected to represent a tise in ex situ preservation and plant breeding and provide range of associated crops and uses, geographic distributions, valuable outreach opportunities to >500 million botanic growth habits, and presence ex situ collections. Botanic garden garden visitors and students each year on topics including holdings were identified for survey based on PlantSearch data, crop diversity and food security (Krishnan et al., 2019; and in July 2018, we contacted curatorial staff at 46 botanic Miller et al., 2015; O’Donnell and Sharrock, 2018). gardens via e-mail with a request for provenance data associated Given the gaps in gene bank CWR collections, and with all living accessions of the 10 target species. We compiled the capacity of botanic gardens to maintain such species, accession records from each botanic garden into standardized there appears to be significant potential for additional fields including provenance type, collection year, source, and country, municipality, county, and locality of origin. Using this collaboration and alignment of CWR preservation by information, we assessed approximate ex situ representation of the global crop gene bank and botanic garden communi- wild populations. To directly compare botanic garden holdings ties. To explore this potential, we set out to characterize with crop gene bank holdings, we mapped the historical natural the depth and breadth of botanic garden CWR holdings, range provided by Bartosh (personal communication, 2018) describe the level of documentation and types of CWR with wild origin collections for Juglans hindsii (Jeps.) R. E. Sm. collections maintained, and demonstrate current and reported by crop gene banks and botanic gardens. potential capacity for botanic garden living collections to support CWR preservation, breeding, and research. RESULTS