REVIEW Genetic Resources (2021), 2 (4), 21–43 DOI: 10.46265/genresj.WJEU8358 https://www.genresj.org ISSN: 2708-3764 History and impact of a bean (Phaseolus spp., Leguminosae, Phaseoleae) collection Daniel G Debouck *, Marcela Santaella and Lúıs Guillermo Santos Genetic Resources Program, Alliance of Bioversity International and International Center for Tropical Agriculture (CIAT), Km 17 recta Cali-Palmira, Cali, AA 6713, Colombia Abstract: This work explains the reasons why a bean collection was established in 1973 at the International Center of Tropical Agriculture (CIAT) near Palmira in Colombia. It shows the impact of the collection on plant breeding and in agricultural development through the distribution of germplasm to the center’s bean breeding program, to successively find resistances to pests and diseases, adaptation to low phosphorus and drought, and more recently higher content of iron and zinc in seeds. The collection was also used to progress knowledge in biological sciences, as shown by a dozen of examples. A reason behind these successes was foresight and focus on diversity per se in the collection. The paper ends with a number of suggestions for the way ahead for the genetic resources conservation and management of these bean crops, and possible take-home lessons for curators in charge of other similar collections. Keywords: distribution, yield, biotic stress, abiotic stress, breeding, Phaseolus Citation: Debouck, D. G., Santaella, M., Santos, L. G. (2021). History and impact of a bean (Phaseolus spp., Leguminosae, Phaseoleae) collection. Genetic Resources 2 (4), 21–42. doi: 10.46265/genresj.WJEU8358. © Copyright 2021 the Authors. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The purpose for establishing a collection of genetic resources at CIAT Created in 1967, the International Center of Tropical Agriculture (CIAT for its Spanish acronym) was the third international center of agricultural research whose mandate was to increase the agricultural productivity in the tropics. Because of population growth a sure food availability crisis was anticipated and yields of key staple crops had to increase (Kastner et al, 2012) and, fortunately, this actually happened, namely in Asia (Evenson and Gollin, 2003). Although CIAT was originally designed to improve agricultural systems in the lowland tropics (the Center had a couple of animal production programs), it became clear that the level of human talents, physical and financial resources required for such a task was beyond the donors’ capacity and time frame, and these limits indicated to re-focus instead (Lynam and Byerlee, 2017). After the successful experience of the International Rice Research Institute ∗Corresponding author: Daniel G Debouck (d.debouck@cgiar.org) (IRRI) in Los Baños, Philippines, on rice and that of the Centro Internacional para el Mejoramiento del Máız y Trigo (CIMMYT) in El Batán, Mexico, on wheat, and as an outcome of international conferences (Hernández- Bravo, 1973; Rachie, 1973; Voysest-Voysest, 1983), CIAT moved from a Food Legumes Production Systems Program into a program focused on common bean, Phaseolus vulgaris L. (Hidalgo, 1991); the Bean Program initiated in January 1974 (Voysest-Voysest, 2000). Given the production problems faced for this crop (Hernández-Bravo, 1973; Singh, 1992), very often managed by small-holder farmers with limited access to inputs (Broughton et al, 2003), the next strategic decision was to increase productivity by transferring resistance to diseases and pests into target varieties. By then, the most severe diseases, out of more than one hundred affecting the crop (Zaumeyer and Thomas, 1957; Singh, 1999), often caused a 70-100% loss in yield (Sanders and Schwartz, 1980; Singh, 1999). The first cycle of breeding (which took about 8-10 years in beans in the 1960s) aimed at securing the potential yield of the landraces (Rachie, 1973). Thus, farmers would have a secure food stock at home and a surplus for Received: 25.06.2021 Accepted: 06.10.2021 Published online: 08.11.2021 https://www.genresj.org https://www.dx.doi.org/10.46265/genresj.WJEU8358 https://www.genresj.org https://www.dx.doi.org/10.46265/genresj.WJEU8358 mailto:d.debouck@cgiar.org 22 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Figure 1. Evolution of the breeding strategy in bush common bean in the tropics over the last decades. sale in local markets. This strategy was likely to work because in subsistence agriculture beans were planted in mixtures to where resistant genotypes would lower the disease pressure for the total crop (Clawson, 1985), and in market-oriented agriculture with fewer genotypes under cultivation a higher part of the production would be saved for sale. It was envisioned to tackle the next most limiting factor to productivity in a cumulative way, through the production and distribution of elite varieties, with the active participation of the national partners, who then would work with extension services for the diffusion of such a technological package. That participation was critical for impact, given the high number and regional variation of commercial seed types (Voysest-Voysest, 1983; Voysest and Dessert, 1991). Figure 1 shows how this strategic approach has worked for common bean over five decades. With each breeding cycle tackling a new challenge, the strategy had to be cumulative, because the entire production chain and the final users would hardly accept to go backwards. In this regard, it is worth noting that after fifty years, diseases and pests continue to be among the highest priorities of bean breeding, especially in Africa (Assefa et al, 2019). While the first breeding cycle was under way, improvements were introduced to agronomical prac- tices, taking into account planting density, plant- ing date versus water availability versus solar radi- ation/photoperiod, minimum of nitrogen-phosphorus- potassium fertilization, or pH correction by lime applica- tion (Thung, 1991). Once these improved agronomical practices were implemented, it was clear that progress in yield had to come from plant breeding (Borlaug, 1983), but there was a critically important assumption for the whole strategy to work: the immediate availability of well characterized and evaluated genetic resources, which would be the ultimate source of all desirable genes. Practically, because there were none at the Cen- ter, this meant assembling large collections of genetic resources of beans and evaluating such collections by multidisciplinary teams. In the early years of CIAT, that assumption had to quickly become reality for the effi- ciency and impact of the breeding efforts. The need for multiple sources for disease and pest resistance and abi- otic stress tolerance was also related to the wide diver- sity of conditions of deployment in the many countries benefiting from that technology. Note that apart from assembling collections, it was also the time of setting the founding principles of genebank management (Allard, 1970; Frankel and Hawkes, 1975). How the Phaseolus collection was assembled With the establishment of the CIAT Bean Program, the first introductions of bean collections from other insti- tutes (e.g. United States Department of Agriculture [USDA], Pullman, USA; Instituto Nacional de Investi- gación Agŕıcola, Chapingo, Mexico; Instituto de Ciencias y Tecnoloǵıa Agŕıcola, Chimaltenango, Guatemala; Cen- tro Agronómico Tropical de Investigación y Enseñanza [CATIE], Turrialba, Costa Rica) (Hernández-Xolocotzi, 1973; Vieira, 1973) were made thanks to the constant cooperation of the Instituto Colombiano Agropecuario, Palmira, Colombia on plant quarantine matters (Fig- ure 2). Accessions were registered as Germplasm num- bers (e.g. G4017 for ‘Carioca’, perhaps the most planted bean variety in the world; Voysest-Voysest (2000). Thanks to the support of the International Board for Plant Genetic Resources (IBPGR), Rome, Italy (estab- lished in 1974), several collecting missions were orga- nized for landraces and wild species. Before the entry into force of the Convention on Biological Diversity (CBD), these crop genetic resources were considered as common heritage of humankind, and there was free exchange of genetic resources for breeding and agricul- tural research purposes. After December 1993, acquisi- tion by introduction of copies of germplasm collections and explorations came to a halt (as experienced in other genebanks of the Consultative Group on International Agricultural Research (CGIAR); Halewood et al (2020). But in recent years, target explorations were carried out under the legal framework set by the International Treaty on Plant Genetic Resources for Food and Agricul- ture (FAO, 2002), for example in Costa Rica. Because beans as a staple are often associated with maize, collections of bean germplasm have been estab- lished across the tropics and subtropics, particularly in Latin America (e.g. in Chapingo in Mexico, Medelĺın in Figure 2. Increase in size of the bean collection introduced into the CIAT genebank. Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 23 Colombia or Campinas in Brazil) (Vieira, 1973), which could be introduced into CIAT. It was not rare for a maize breeder to pick up seeds of local bean landraces when visiting a farmer or a local market and give them to colleagues in charge of bean breeding. As a gen- eral practice in Latin America the maintenance of bean germplasm collections was a side activity of the bean breeders. Given this kind of attention, it is no surprise that the landraces of the market classes worked on by the breeders were well represented in the respec- tive collections. Retrospectively, this is positive because some of these collections were made in the 1940-1960s, just before massive rural transportation blurred the ori- gins of many local landraces. By that time, the vari- eties selected or bred over the last decade were starting to replace many landraces. This replacement was seen in small black and red-seeded bean varieties of Central America. Consequently, the most original genetic vari- ation in landraces that existed in the 1940s is by now either in genebanks or lost. Collecting today will only result in duplicates or in samples of bred materials. The focus on common bean and the need to find resistances for several market classes of beans as final targets influenced the makeup of the collection (Table 1). As the Bean Program was working with Central American countries and Brazil (Voysest-Voysest, 1983), many small-seeded collections were introduced, but because CIAT also worked together with Andean countries, large-seeded collections were included as well (both collections but particularly the last ones were important for Africa: Martin and Adams (1987). Cultivated P. vulgaris makes up the biggest part of the collection, the other cultivated species follow, with a total of 32,183 landraces and 2,797 improved varieties. The wild forms of the cultivated species and the wild species are represented by over 2,000 accessions (Table 1). The number of country depositors is 110. The top five countries that have contributed most are: Mexico (6,237 accessions), Colombia (3,927 accessions), Peru (3,798 accessions), Guatemala (2,853 accessions) and the United States (1,863 accessions), followed by Brazil, Ecuador, Turkey, Malawi and Costa Rica (with around 1,000 accessions each). Restoration of national bean diversity has been done for Bhutan, Chile, Costa Rica, India, Iran, and Mexico, based on institutional agreements. After partial safety duplications at CATIE and Centro Nacional de Pesquisa de Recursos Genéticos e Biotecnologia, Brasilia, it was decided in 1996 to make a complete backup at CIMMYT because extra space was kindly offered by Bent Skovmand then in charge of the wheat collection. This included a check for viability and absence of diseases of quarantine importance. By 2019, 92% of the bean collection had been safely duplicated at CIMMYT. When the Global Svalbard Seed Vault (GSSV, Longyearbyen, Norway) was opened in February 2008 (Fowler, 2016), a second safety backup was implemented there. By 2019, 94% of the bean Table 1. Accessions of the in-trust Phaseolus collection kept at CIAT Palmira (information also available in Genesys: https:// www.genesys-pgr.org/a/overview/v2ZW8lQwlep) Species Biological status No. accessions P. vulgaris, common bean cultivated (landraces, commercial varieties) 30,571 wild and weedy forms 1,804 P. lunatus, Lima bean cultivated (landraces, commercial varieties) 3,031 wild and weedy forms 274 P. coccineus, scarlet runner cultivated (landraces, commercial varieties) 760 wild and weedy forms 198 P. dumosus, year-bean cultivated (landraces) 475 wild and weedy forms 15 P. acutifolius, tepary cultivated (landraces, commercial varieties) 161 wild and weedy forms 165 Other species (411) wild forms only 484 1 This figure represents half of the number of species of the genus (Debouck, 2021). collection was safely duplicated at GSSV. In addition, CIAT safeguards in its vault the seed backups of the food legume collection of the International Institute of Tropical Agriculture (IITA), Ibadan, Nigeria, and the tropical forage legumes of the International Livestock Research Institute (ILRI), Addis Ababa, Ethiopia. The diversity in the bean collection and its use Given the breeding priorities (Figure 1), the bean collec- tions were evaluated by multidisciplinary teams in mul- tiple locations in Colombia, first in Palmira, in Quilichao since 1977 and in Popayán since 1978 (Cuellar, 2003). Resistances to several highly damaging diseases (e.g. anthracnose, angular leaf spot (ALS), bean common mosaic virus (BCMV), rust) were found (Table 2) and transferred as their mode of inheritance was pro- gressively defined (Singh, 1992; Beebe et al, 1997; Beebe, 2012). However, bean breeders soon realized that further genetic progress would be obtained only by screening the diversity outside the respective market classes, and that for many traits (e.g. Ascochyta blight, bean golden mosaic virus (BGMV), bean golden yellow mosaic virus (BGYMV), common bacterial blight, halo blight, web blight, white mold, bruchids and leafhop- pers) there were very few or no sources of workable resistance (Miklas et al, 2006; Singh and Schwartz, 2010; Beebe, 2012). In a copy of the USDA collection there were a few accessions of wild common bean from Mexico collected in the 1960s by Howard Scott Gen- try in which, later on, César Cardona and his team found bruchid resistance associated with a particular seed protein (Osborn et al, 1988). The screening for the right variants of that protein by electrophoresis https://www.genesys-pgr.org/a/overview/v2ZW8lQwlep https://www.genesys-pgr.org/a/overview/v2ZW8lQwlep 24 Debouck et al Genetic Resources (2021), 2 (4), 21–43 opened the way for marker assisted selection (Kelly and Miklas, 1999), widely applied in breeding for BGYMV resistance (Broughton et al, 2003), anthracnose resis- tance (Kelly, 2004) and other traits. The wide sec- ondary gene pool (e.g. P. coccineus, P. costaricensis, P. dumosus) has just started to be evaluated, and has already shown promise against Ascochyta blight (Schmit and Baudoin, 1992), angular leaf spot (Mahuku et al, 2003) and white mold (Singh et al, 2013). Such resis- tances were expected because the species of the sec- tion Phaseoli thrive in montane humid forests (Debouck, 2000) where these fungi diseases are frequent selec- tion pressures (Cattan-Toupance et al, 1998) and have likely been present over hundreds of thousands of years, given the age of these species (approximately 1 million years) (Delgado-Salinas et al, 2006; Rendón-Anaya et al, 2017). Once disease resistances were transferred to the pre- ferred varieties in the different market classes, yield came as the next challenge, in order to keep bean as a competitive (mono-)crop as compared to soybean, cow- pea or sorghum. An early approach, in line with the spirit of the Green Revolution in wheat (Donald, 1968), was to optimize the ideotype under favorable environ- ments (Adams, 1973). That breeding effort on plant architecture continued (Kelly, 2001), although with lim- ited success in the tropics (Beebe, 2012). An impor- tant outcome, however, has been the rise of growth habit 2 or bush erect indeterminate (race 3 of Evans (1973) for mechanical harvesting in bean improved germplasm, little present in traditional landraces of Latin America. This also offered opportunities to enrich the collection (Hidalgo et al, 1992). Another breed- ing goal was to combine the productivity of the small- seeded varieties with the grain size of the large-seeded ones, many of them demonstrated to be of Mesoamer- ican and Andean origin, respectively (Evans, 1976). Thus came the works evidencing the two major gene pools (Gepts et al, 1986; Singh et al, 1991b; Kwak and Gepts, 2009; Bitocchi et al, 2013), and the races within them (Singh et al, 1991a; Beebe et al, 2000b; Blair et al, 2007, 2012). The presence of races was a bit unexpected in an autogamous crop but could be explained by the role of outcrossing during early domes- tication (Chacón-Sánchez et al, 2021). Some genetic iso- lation and poor recombination have been shown to exist between the two major genepools (Singh and Gutiérrez, 1984) and since the wild state (Koinange and Gepts, 1992). But significant heterosis was demonstrated to exist (Nienhuis and Singh, 1986; Bannerot, 1989), espe- cially between races (Singh et al, 1993; Singh and Urrea, 1995), while genetic disorders between races were sometimes observed (Singh and Molina, 1996). The significant interactions with the environment, how- ever, have resulted in a narrow commercial applica- bility of this approach (Gutiérrez and Singh, 1985; Nienhuis and Singh, 1986). Another strategy inspired from the quantitative developments in tomato breed- ing (Tanksley et al, 1996) was the advanced back- cross QTL analysis using a wild form. The accessions of wild P. vulgaris G12947 (Acosta-Gallegos et al, 2007), G19892 (Buend́ıa et al, 2003), G24404 (Blair et al, 2006) and G24423 (Kelly, 2004) were found to con- tribute a significant QTL for yield (a 27% increase as compared to the recurrent parent in the last example). In some cases, the use of weedy types would help reduce the number of backcrosses needed to recover the appro- priate seed size (Acosta-Gallegos et al, 2007). Another innovative approach has been the use of lines coming from crosses with the year-bean (for transfer of high iron in the grain) or with tepary (for transfer of bacterial blight resistance) in order to bring more monocarpism into common bean (Klaedtke et al, 2012; Mej́ıa-Jiménez et al, 1994). The bean crop with exceptions in growth habits 1 and 2 still has the ancestral trait of continuing shoot production and lateral flowering, while the first pods already enter into maturity. In the wild it makes all sense, but not in a crop aimed at mechanical har- vesting. The desert ephemerals of the genus such as P. acutifolius A. Gray, P. filiformis Benth, or P. microcar- pus Mart. (Freytag and Debouck, 2002) invest much less in profuse branching but soon move all photosynthesis products into their seeds. Thus, under heat or drought stress, it makes sense to quickly redirect such products to the only part that will be harvested (Rao et al, 2013; Suárez et al, 2020). One outcome of the increase in size of the collection and the first phase of germplasm evaluations at CIAT was the establishment of core collections (along the concept introduced by Frankel and Brown (1984). The CIAT common bean core collection was established by use of Geographic Information Systems maximizing the environmental diversity of landraces, and a few morpho-agronomic descriptors (Tohme et al, 1995a). The core collection, consisting of 1,556 accessions, has been used for the identification of germplasm tolerant to low phosphorus (Beebe, 1997) or containing high levels of micronutrients (Islam et al, 2002). For both traits less than 10% of the total collection had been evaluated at that time (Beebe et al, 2000b,a), explaining the recourse to the core collection. Using core collections was, in part, the consequence of internal duplication or redundancy in general collections, which for cultivated common bean has been estimated at 50% across the major genebanks (Lyman, 1984). This figure is perhaps on the high side but reflects the amount of commercial and breeding materials kept in genebanks as compared to primary sources of variation (landraces, wild species). As mentioned, the management of germplasm collections was often a side activity of bean breeders who would hesitate to eliminate all variants close to the target market class. Given the cost of keeping accessions versus the cost of tracking down internal copies (this was then achieved by multi-site characterization, in addition to passport data) (Koo et al, 2004), the problem was not given high priority in the past. With the development of SNP genotyping technology, this issue should be revisited, Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 25 Table 2. Bean accessions from the CIAT collection used as sources of resistance to diseases and pests. Trait Material used References Diseases angular leaf spot G10613 from Guatemala Pastor-Corrales et al (1998) interspecific hybrids with P. coccineus; G4691 Pastor-Corrales et al (1998); Islam et al (2002); Mahuku et al (2003) angular leaf spot and anthracnose G3991 from Costa Rica Schwartz et al (1982) anthracnose Aliya G02333 Young and Kelly (1996) Kaboon G1588; Cornell 49-242 G5694 Melotto and Kelly (2000) interspecific hybrids with P. coccineus G35252 Mahuku et al (2002) Ascochyta blight P. dumosus G35369 from Costa Rica Schmit and Baudoin (1992) P. dumosus G35182 from Guatemala Garzón et al (2011) bacterial wilt wild P. vulgaris G12883 from Mexico Urrea and Harveson (2014) Bean Golden Yellow Mosaic Virus (BGYMV) P. coccineus G35172 from Rwanda Beaver et al (2005) Bean Common Mosaic Virus (BCMV) Porillo Sintético G04495, Royal Red G04450 Singh et al (2000) beet curly top virus California Pink G06222, Red Mexican G05507 Larsen and Miklas (2004) Porillo Sintético G04495, Burtner, Tio Canela 75 Singh and Schwartz (2010) common bacterial blight interspecific hybrids with acutifolius VAX4, MBE7 Zapata et al (1985); Singh and Muñoz (1999); Michaels et al (2006); Navabi et al (2012) Montana No. 5; PI 207262 Miklas et al (2003, 2006) halo blight Montcalm G06416, ICA Tundama G14016 Beaver (1999) Palomo G12669 Schwartz (1989) Pinto US 14 G18105 Singh and Schwartz (2010) Wis HBR 72 G03954 Taylor et al (1996) Fusarium root rot Porillo Sintético G04495; wild P. vulgaris G12947 Beebe et al (1981); Acosta-Gallegos et al (2007) Pythium root rot PI 311987 G02323 Beebe et al (1981) Rhizoctonia solani rot N203 G00881 Beebe et al (1981) rust Compuesto Negro Chimaltenango G05711 Stavely (1984) Ecuador 299 G05653 Stavely and Pastor-Corrales (1989) Redlands Pioneer G05747 Liebenberg et al (2006) PI 260418 Singh and Schwartz (2010) web blight BAT 93; Flor de Mayo G14241 Beaver et al (2002) white mold P. coccineus PI 175829 from Turkey Abawi et al (1978) P. dumosus PI 417603 from Mexico Hunter et al (1982) interspecific hybrids with P. coccineus G35172 Singh et al (2009) interspecific hybrids with P. costaricensis G40604 Singh et al (2013) Pests Acanthoscelides weevil wild P. vulgaris from western Mexico G12952; QUES van Schoonhoven et al (1983); Zaugg et al (2013) Apion godmani pod weevil Amarillo 154 G03982; G03578 Beebe et al (1993); Garza et al (2001) Empoasca leafhoppers Turrialba 1 G03712 Galwey (1983) California Dark Red Kidney, from USA G17638 Schaafsma et al (1998) Ophiomyia bean fly P. coccineus G35023 and G35075, and interspecific hybrids Kornegay and Cardona (1991) whiteflies Aleyrodidae DOR 303 Blair and Beaver (1992) Zabrotes weevil wild P. vulgaris from Chiapas, Mexico G24582 Acosta-Gallegos et al (1998) 26 Debouck et al Genetic Resources (2021), 2 (4), 21–43 with the merging of near identical accessions and the review of the core collection (as already suggested for the USDA core collection by Kuzay et al (2020). The most significant costs ahead are likely to be about regeneration and evaluation, not the chasing of internal copies helped by robotics! Distribution of the bean collection Since being established in August 1977 as an inter- nal service unit (Hidalgo, 1991), the genebank has distributed to the Bean Program and the Biotechnol- ogy Research Unit of CIAT a total of 318,148 samples (or 69.4 % of the total distributed) (Figure 3). Exter- nally, the genebank has distributed 140,109 samples (or 30.6% of the total) to users in 105 countries. The total distributed was 458,257 samples of 37,657 accessions, or 99% of the bean collection. These figures indicate that: i) the collection has been studied and used ini- tially by the scientists of CIAT, ii) the number of coun- tries benefiting from the conservation work through dis- tribution almost matches with the number of country depositors, and iii) the collection has been distributed almost entirely (this percentage could be even higher since some accessions have not been distributed due to lack of seeds). One should note that apart from CIAT programs, the most important users were national agricultural research services, universities and research institutes. The shares of farmers, commercial companies and non-governmental organizations in the distribution were low in comparison. Assuming farmers are aware of the existence of germplasm collections, reasons for the low number of requests might be related to the farmers’ access to on-line request processes (mail requests were honored), as well as the capacity to deal with phytosan- itary regulations in the respective countries. As dry bean breeding has been mostly carried out by public institu- tions, requests of genetic diversity by the private sec- tor were few, often related to specific sources of varia- tion for snap bean breeding (e.g. sources of resistance to anthracnose). The purposes of distribution have generally followed the breeding priorities shown in Figure 1: interest in resistances to diseases and pests, nutritional quality and more recently tolerance to abiotic stresses such as drought and high temperature. As discussed below and shown in Figure 4, a significant part of the distribution has been for the purpose of advancing knowledge. In Figure 4, breeding activities (38.9%) and applied research (e.g. in pathology or entomology: 37.1%) were the top purposes for seed requests, followed by agronomy (11.7%) and basic research (e.g. in genetics or evolutionary studies: 9.6%). The variation in number of distributed samples from one year to another can be significant, namely if the core collection with over 1,500 accessions was requested and sent. The peak in distribution in the period 1978- 1996 practically matches with that of the activities of CIAT Bean Program (Voysest-Voysest, 2000). For the period 1973-2019, the top five recipient countries were: USA (26,093 samples), Colombia (18,444 samples), Brazil (9,198 samples), Guatemala (7,430 samples) and Mexico (6,787 samples). The term ‘samples’ is preferred over ‘accessions’ as a country recipient could ask for a specific accession more than once. Apart from germplasm, the genebank also distributed information related to the in-trust collections. An indicator of this service is given by the number of consultations of the genebank website (https://ciat.cgia r.org/what-we-do/crop-conservation-and-use/) to have access to data (Figure 5). Statistics about access to genebank information and services in recent years show that most of the visi- tors (81%) reach the genebank website directly, indi- cating a user knowledge and confidence that relevant information can be found there, while 19% of visi- tors find the website through a browser search or are referred to it through another link. Users also benefit from specialized technical information currently consist- ing of 658 documents (including articles, book chapters, conference proceedings, germplasm exploration reports, posters and presentations). These documents can be accessed through the genebank website or the institu- tional document repository CGSpace (https://cgspace.c giar.org/handle/10568/35697), that registered 27,278 downloads in 2017-2019. Impact of the bean genetic resources collection The 225 varieties released in 17 countries of Latin America and the 88 varieties released in 14 countries of Africa in 1974-1999 by the Bean Program (Voysest- Voysest, 2000), the check of BGYMV in Central America (Beebe, 2012), as well as the yield gain from 688 kg/ha to 782 kg/ha in eastern Africa (Lynam and Byerlee, 2017) eventually have their origin in the CIAT genebank. Once the interesting traits were identified (Table 2); (Hidalgo and Beebe, 1997), through different breeding schemes, elite varieties were produced, tested and released via international nurseries such as the International Bean Yield and Adaptation Nursery (Voysest-Voysest, 1983; Beebe, 2012), generating significant economic and social benefits (Johnson et al, 2003). In this last work, over the period of analysis, and because of the varieties involved, some countries of Latin America and the Caribbean were net beneficiaries (Argentina, Brazil), while others were net contributors (Mexico, El Salvador). Overall, and over the duration, however, it seems that all countries benefit from conservation and unrestricted international exchange of germplasm (Johnson et al, 2003). As an example of changing context over time, the gene gy. originating from Peru and conferring an intense and sustained yellow color (Bassett et al, 2002) was used since 1978 in northwestern Mexico (Lépiz-Ildefonso and Navarro-Sandoval, 1983), because it gave a premium price as compared to the fading color in yellow- seeded traditional landraces. It ended up in the variety ‘Azufrado Peruano 87’ (Voysest-Voysest, 2000) and also https://ciat.cgiar.org/what-we-do/crop-conservation-and-use/ https://ciat.cgiar.org/what-we-do/crop-conservation-and-use/ https://cgspace.cgiar.org/handle/10568/35697 https://cgspace.cgiar.org/handle/10568/35697 Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 27 Figure 3. Number of samples distributed in the period 1973-2019. Important recipients were the Bean and Biotechnology Programs of CIAT, the national agricultural research services (NARS), universities and research institutes. an undue patent granting (genetically dissected in great detail by Pallottini et al (2004). It is because the in-trust collection was rich in yellow-seeded accessions from Mexico and Peru, and because the CIAT genebank kept past records such as old catalogs of varieties (Hedrick, 1931), it was possible to demonstrate ample prior art, and the patent was turned down in 2008. Legumes have been called the ’meat of the poor’ (Heiser, 1990) and in many parts of Latin Amer- ica (e.g. Brazil, Mexico, Cuba) people with low income eat beans daily. Similarly, the highest consumption rates per capita are currently registered in eastern Africa (OECD, 2015). Given this, it was becoming evident that improved varieties should also fight the ‘hidden hunger’ or the deficiency in minor minerals such as iron and zinc where the diet is not sufficiently diverse. Using the core collection, the evaluation to find accessions with high iron and zinc was expanded (Islam et al, 2002), and good sources were identified (G21242, G23818, G23834) (Blair et al, 2011), primarily from the Andean region. Nothing on the seed aspect indi- cates high values in these micronutrients. Likewise, G14519, an old landrace named ‘Hickman Pole Bean’ from the United States and belonging to the Mesoamer- ican genepool, also has shown potential (Blair et al, 2010). From the start, the genebank had interest in assembling variation for any future need, and this is precisely the wide scope that made biofortification pos- sible thirty years later and with a lasting impact where it is today most needed, e.g. in East Africa (Sellitti et al, 2020). With changing context of bean production over the last forty years, for example, common bean being pushed towards the west in the Plains of the USA or in the Canadian prairie, the northwest in Mexico and the northeast in Brazil (Singh, 2001), new challenges like drought, cold, heat or low phosphorus are set for breeding. Some drought tolerance can be found in the ‘Durango’ race (Singh, 2007; Beebe et al, 2013), in other landraces such as G21212 (Beebe et al, 2008) and in wild forms (Cortés and Blair, 2018). Root architectural and physiological traits identified in an Andean landrace, G19833, may contribute to phosphorus acquisition (Beebe et al, 2006). 28 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Figure 4. Number of samples distributed annually to users in the period 1973-2019, according to the purposes of requests. Figure 5. Number of consultations of the CIAT genebank website (https://ciat.cgiar.org/what-we-do/crop-conservation -and-use/) in the period 2009-2019. The impact of the bean germplasm collection has also been through the direct adoption of genebank accessions by farmers after the screening of international nurseries. No less than thirty-four accessions have been registered in national catalogs of varieties in thirty-eight countries in 1974-1999 (Voysest-Voysest, 2000), or 13% of the total of improved genetic materials distributed by CIAT. This figure may not look impressive, but bean varieties produced by breeding have been released in the same geographic areas since the 1940s. That said, it is anticipated that apart from the use of landraces for specific niche markets (see popping beans below), for specialized studies for example in pathology (e.g. disease differential sets) or for servicing gardeners, a significant coming impact of genetic resources will materialize through libraries of genetic stocks (van https://ciat.cgiar.org/what-we-do/crop-conservation-and-use/ https://ciat.cgiar.org/what-we-do/crop-conservation-and-use/ Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 29 Treuren and van Hintum, 2014), targeted diversity panels (Cichy et al, 2015; Moghaddam et al, 2016), and sequence tagged traits (Lobaton et al, 2018). But in order to allow the ‘molecular’ breeder to do advanced searches throughout the collection substantial changes must be brought to databases (McCouch et al, 2012; Byrne et al, 2018). Learning from experience, the design should be for use by non-database experts, modular and scalable, moving from passport data into accession traits and ending into annotated genes. Somehow, this focus re-emphasizes the role of genebanks as keepers of the primary genetic variation, and perhaps less of all allelic combinations of that variation (i.e. the sister lines of simple crosses), since tools now exist to recombine that variation to better meet human needs or agricultural contexts (towards precision agriculture for instance). Appraising that variation by curators might be difficult (what should be kept in the genebank remains a cornerstone and recurrent question), although they will be helped by sequence information. From a pragmatic perspective genebanks may keep interest in old landraces since these have been tested over long durations in farmers’ fields. For similar efficiencies in breeding, genebanks might be interested in keeping recombinants between gene pools, for example from southern Europe (Gioia et al, 2013), part of the Guarani area in Brazil (Burle et al, 2010) or the northern Andes (Chacón-Sánchez et al, 2021), especially if they represent novelties in agronomic or nutritional attributes. The other impact: the contribution to knowledge The in-trust collections, because of the open access set forth by FAO in the early years and then the facilitated access approved by the parties to the International Treaty (FAO, 2002), have helped increase knowledge in many fields of biological sciences (Dudnik et al, 2001). Conversely, the increased knowledge contributed tremendously to the efficiency of the breeding and varietal deployment efforts. This was particularly applicable to the mandate crops of CIAT, since with the exception of rice, not much basic biology and genetics was known in the late 1960s when crop improvement efforts were launched. For instance, the ancestry of common bean became firmly established at a time not far away from the founding of CIAT (Burkart and Brücher, 1953; Gentry, 1969). The double domestication of common bean became obvious only in 1986 (Gepts et al, 1986), and that of Lima bean in 1989 (Debouck et al, 1989), and the existence of a fifth case of domestication in the genus was clarified as late as 1991 (Schmit and Debouck, 1991)! Such increased knowledge also helped to better define what should be conserved in genebanks; for example, studies on the founder effect due to bean domestications have stressed the importance of wild forms for accessing the total genetic diversity of three bean crops (Sonnante et al, 1994; Mart́ınez-Castillo et al, 2015; Mina-Vargas et al, 2016). As expected, that founder effect was less marked in the scarlet runner (Guerra-Garćıa et al, 2017). That knowledge also helped in the development of disease indexing methods for the safe movement of germplasm (Kumar et al, 2021). Some examples are provided in Table 3 (by tracking accessions distributed in 1973-2019). The breadth of disciplines, evidenced by the diversity of peer-reviewed journal titles and linked to genebank accessions, is striking but just reflecting the diversity of the collection. No less important are the opportunities of scientific collaborations around ‘problems’ set up by the bean crops and materials provided by the genebank, as reflected by the institutions and countries of authorships. Knowledge often overlooked, although associated with crop germplasm for millennia Because germplasm collections were assembled at CIAT primarily in relation to breeding, traditional knowledge associated with specific accessions was rarely documented. As the first phase of breeding was focused on resistance to diseases and pests, with systematic inoculation of known strains, there were often no incentives for a time-consuming effort to document vernacular names, culinary and other folk practices. One such example is that of popping beans consumed toasted (National Research Council, 1989). That group of landraces still exists in the Andes, from Cajamarca in Peru down to Chuquisaca in Bolivia (Tohme et al, 1995b). Elder farmers in the countryside will tell which variety can pop, while migrants to urban areas one generation after will simply process them all in water cooking, even with a slight increase in digestibility (van Beem et al, 1992). Documenting this property by the genebank is doubly important. First, consumer preferences change over time (Voysest-Voysest, 2000) and, in contrast to the 1960s, there is a renewed interest nowadays in local gastronomy that can provide a better income to mountain farmers (Zimmerer, 1992). Second, water and fossil energy might become expensive inputs to food processing or transportation, as it is still the case in many parts of rural eastern Africa. In pre-ceramic times in the Andes, these two inputs (excepting fire) were either difficult to carry or to access. Producing a hot surface with the help of solar energy might not be an excessively difficult or expensive technology to implement in the Andes or in eastern Africa. In altitude, this kind of germplasm and the unique way to make it ready for human consumption may also contribute to reduce deforestation for fuel wood, while montane forests usually occupy a small acreage (National Research Council, 1989). Finally, it is worth noting that this group has a high number of phaseolin types (Tohme et al, 1995b), indicating a high diversity in contrast to other Andean landraces (Beebe et al, 2001). Evaluation of popping beans is continuing in Peru (Cruz-Balarezo et al, 2009) and Colombia (Otálora et al, 2006), while 30 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Table 3. Examples of impact of CIAT bean in-trust collection for the advance of knowledge. Field Output, problem solved References Botany new species described Salcedo-Castaño et al (2011) Plant taxonomy taxonomic status of bean species re-assessed Schmit et al (1996) review of the genus and species Freytag and Debouck (2002) Agricultural botany founder effect of bean domestication Schinkel and Gepts (1988) definition of a 3rd gene pool in Lima bean Motta-Aldana et al (2010) fifth case of domestication in the genus Schmit and Debouck (1991) Crop evolution recombination between gene pools Gioia et al (2013) Phylogeography past trans-isthmic migrations of wild bean Chacón-Sánchez et al (2007) Plant breeding gene pools/ races of common bean defined Singh et al (1991a) Plant pathology inheritance of ANT/ALS resistance genes Gonçalves-Vidigal et al (2011) coevolution of ALS in bean gene pools Guzmán et al (1995) Plant virology resistance to Clover yellow vein virus Hart and Griffiths (2014) Entomology resistance to bean bruchids Cardona et al (1990) resistance to bean weevil Kamfwa et al (2018) Plant genetics common bean genomic map Schmutz et al (2014) common bean genome history & evolution Rendón-Anaya et al (2017) inheritance of pod dehiscence Parker et al (2020) inheritance of leaf mutation Garrido et al (1991) Plant biotechnology genetic transformation in tepary bean Dillen et al (1997) Plant physiology flowering response to daylength White and Laing (1989) identification of phosphorus-efficient genotypes Beebe et al (1997) low phosphorus tolerance in bean Rao (2001) variation in photosynthetic activity Lynch et al (1992) Plant root physiology tolerance to NaCl salinity in early growth Bayuelo-Jiménez et al (2002) Plant microbiology coevolution of Rhizobium etli Aguilar et al (2004) Human nutrition content in micronutrients such as iron Beebe et al (2000a) phaseolin type and digestibility Montoya et al (2008) Archaeology crop domestication and ancient diet Piperno and Dillehay (2008) Intellectual Property Protection rebuttal of an undue crop utility patent Pallottini et al (2004) the inheritance of the trait is being investigated (Campa et al, 2011; Yuste-Lisbona et al, 2012). Serving the breeders community and beyond As shown in Figure 3 and Table 3, distribution has been significant to a high diversity of users, going beyond CIAT breeding activities in Colombia and in eastern Africa. The trend that in some countries dry bean consumption is declining (Khoury et al, 2014) (contradictory to health and global environment benefits: Foyer et al (2016) may mean fewer requests for that kind of germplasm but an increased interest into snap bean, often of Andean origin (Myers and Baggett, 1999). With the development of urban gardening, snap bean might be on the rise, either through the planting of old heirloom varieties (Kaplan and Kaplan, 1992; Zeven, 1997) or new ones. In CIAT, the priority was on dry bean, little on snap bean for the tropics, but with possibilities of using a wide range of resistance sources developed for the former commodity (Silbernagel et al, 1991). The changing fate of the popping beans, even in countries of origin over the last forty years, shows the ever-changing nature of markets. Thus, examples of unpredictability abound, indicating for the genebank to focus on diversity per se, independently from immediate and local interests. This example of success brings a strong message to focus scarce resources, at a time when there is risk of repeating previous work because many disciplinary continuums have been broken. Thus, it seems of paramount importance to document at accession level what is already known: phaseolin type, alleles of allozyme, RAPD markers, SCARs, SSRs, also evaluation data (trait, location, strain as applicable). Individual accessions should be linked with references and supporting documents. Keeping in mind that one third of the collection has not been evaluated, there is still a lot of work for pathologists, entomologists and virologists. Evaluations were done on up to 23,000 accessions only for anthracnose, angular leaf spot and common bacterial blight; for the other limiting pests the figures are much lower (Hidalgo and Beebe, 1997). The reaction should be reported at each accession level, and not restricted to the best performers. Evaluation Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 31 should obviously capitalize on knowledge generated by previous protocols. For example, on bruchids, it is likely that evaluation of the rest of cultivated common bean germplasm will lead to nowhere (van Schoonhoven and Cardona, 1982), because domestication occurred elsewhere (Chacón-Sánchez et al, 2005; Bitocchi et al, 2013; Kwak et al, 2009). But the right arcelin can be picked by screening for the protein or the gene(s) involved instead of testing thousands of accessions in contact with the insects. From previous experience, it seems likely that genebanks will face periodic shortages in skilled, highly specialized staff (a challenge also mentioned by Fu (2017). This is a recurrent limitation for germplasm evaluation (thus resulting in limited use of the collection in the future). Sending the core collection or more accessions abroad for specialized evaluations is an option, although perhaps not as fast as having it evaluated by a multidisciplinary team as done at CIAT in the 1970s. Incidentally, blocks of resistance genes (Gonçalves-Vidigal et al, 2020) that can be traced by molecular markers are giving an unexpected support to that approach. But in view of complex traits such as heat or drought tolerance, for which just a fraction of the entire collection has been evaluated, multi site evaluation of thousands of accessions seems extremely time-consuming and expensive. New evaluation schemes have to be designed and are a true challenge at the organ level (Zhao et al, 2019), but not impossible when focused for example on pulvini-caused movements of leaflets in relation to solar radiation avoidance (Thomas et al, 1983). For location-related abiotic stresses, geographical approaches (targeted towards the surviving germplasm where the stress has been present for thousands of years, and thus logically the wild forms) may help. But these GIS approaches did not pick up outstanding wild forms under low phosphorus stress (eighteen accessions tested, Beebe et al (1997), while there seems some promise for drought tolerance (eighty-six accessions tested, Cortés and Blair (2018). Internally, these approaches requires the genebank to be strict on passport data accuracy (van Hintum et al, 2011). However, this is not always possible; for example, accession G40001 with promise for heat tolerance is from a market in Veracruz (Suárez et al, 2020). Given some intrinsic limitations of common bean, coming heat and drought stress in the tropics and subtropics (Battisti and Naylor, 2009; Beebe et al, 2011) may be the opportunity to re-balance the collection towards the tepary and Lima bean, more hardy crops in this regard (Freeman, 1913; Rachie, 1973), respectively). Eventually, bean breeders may realize that they have five crops instead of one, each one with a different ecological head start (Debouck, 1992). With the advances in marker assisted selection and genetic maps, it might be faster to correct a shortcoming in seed or growth habit in tepary than expecting the common bean to fully change its ecological background. Discussion The afore-mentioned facts suggest the following points for discussion. First, one can ask whether this bean germplasm collection meets the expectations for which it was established. Many sources of disease resistance were found (Table 2), and one should note that in many cases the findings were unpredicted, and largely independent of geographic origin or gene pool. As well noted by Harlan (1978), page 351) “resistance is where you find it”. For those diseases where no good sources of resistance have been found, in the light of a similar experience with the USDA collection (e.g. the case of white mold: Schwartz and Singh (2013), it seems more a deficiency of the common bean crop species itself than a severe lack of representativeness. Thus, the breeders turned logically to the wild forms and the secondary gene pools (Debouck, 1999), where the collection provided some solutions but also means for the needed preliminary studies in taxonomy and wide crossing. This links with a second point: given the above evidence of return on investment and incompleteness of the task (Hidalgo and Beebe, 1997), it might be important to continue with evaluation, namely for abiotic stresses such as drought or heat caused by global warming, as these will impact on yield (Lobell and Gourdji, 2012; Beebe et al, 2013). In view of the numbers of accessions and facing the need for developing novel evaluation schemes for abiotic stresses including a network of well characterized (climate, soil) experimental plots, it might be cost effective to cooperate with other bean germplasm repositories (e.g. Instituto Nacional de Investigaciones Forestales, Agŕıcolas y Pecuarias, Tepatitlán, Mexico; Institut für Pflanzengenetik und Kulturpflanzenforschung, Gatersleben, Germany; USDA, USA). Incidentally, this cooperation might also include a reciprocative safety backup and the development of a novel database because it is a shared concern. Third, to the question whether the genebank has made any impact, the answer came from bean breeding but also many actors in the global community. The figures of germplasm distribution for applied and basic research (Table 3 and Figure 4) have shown a vibrant research community worldwide adding value to the collection. They invite the genebank to a permanent capacity to respond to requests (because of the ‘on-line shopping syndrome’) but also to document these impacts. The question whether the collection will make any impact in the future should also consider technological innovations such as transgenesis and gene editing (e.g. using CRISPR-Cas9) (Doudna and Charpentier, 2014). These approaches of genetic engineering bring new light on using diversity, as they have the potential to add a new function such as herbicide tolerance or improve an existing one, such as seed protein quality, beyond the trait offer of the primary gene pool (Gepts, 2002). Transformation in common bean has proven to be particularly difficult (Jacobsen, 1999), and with limited success (Aragão et al, 1998, 2002; Estrada-Navarrete et al, 2007). Transformation seems 32 Debouck et al Genetic Resources (2021), 2 (4), 21–43 quite possible in tepary bean (Zambre et al, 2005), but apparently little exploited for tepary improvement. The CRISPR technology in soybean aims at editing genes involved in a biosynthetic pathway for seed oil quality, for herbicide tolerance, or changing photoperiod sensitivity (Bandyopadhyay et al, 2020; Xu et al, 2020). New technologies will continue to appear, but under currently available evidence and costs they seem likely to contribute to a wider and/or faster use of the collection rather than to replace it. Finally, in this context, in order to continue to meet the broader expectations of human societies, the genebanks should fill gaps which were identified early on, in terms of geography, e.g. the northern Andes: (Hidalgo and Beebe, 1997; Beebe and Debouck, 2019); or in terms of biological coverage (Ramı́rez-Villegas et al, 2010, 2020). Wild forms and wild species should thus be better represented in the collection, with due consideration to the regeneration capacity and disclosure of the potential. There are two points here: first, given the possibilities opened by comparative mapping in the Phaseoleae (Schmutz et al, 2014; Vlasova et al, 2016; Garcia et al, 2021; Moghaddam et al, 2021) and by gene editing (Bhatta and Malla, 2020; Ku and Ha, 2020), it may be time to think beyond direct interspecific hybridization for the use of alien germplasm. In that sense, species of clade A that may represent half of the genus (Delgado-Salinas et al, 2006; Porch et al, 2013; Debouck, 2021) may be opportunities of genes to imitate and/or to regulate differently instead of genes to transfer. But given the speed of the technological development in breeding (Hickey et al, 2019), the action should be initiated now with the most threatened habitats (Williams et al, 2007), species (Goettsch et al, 2021), or unpredictable conditions, or time- consuming work. This leads to a second point, as forsaking millenary crops (Mamidi et al, 2011) does not improve humankind’s food security. The four other bean crops mean four more opportunities for plant breeding. Following the diversity criteria prevailing during the establishment of the common bean collection, similar efforts should be carried out for these bean crops. The change experienced by soybean from an oriental soy sauce in North America in 1767 into an animal feeding and agro-industrial crop in just one hundred years (Hymowitz and Bernard, 1991) is a strong message to not lose options. Along the concept of a societal insurance provided by crop genetic resources (Gepts, 2006), keeping more crops alive goes in line with productive, sustainable and locally adapted agriculture and, as a consequence, with reducing rural poverty and increasing appreciation towards indigenous cultures. More than ever before, genebanks should continue to be the reserve of all options. Concluding remarks Figure 1 presented breeding challenges in Latin America in a time sequence, which were largely met by use of genetic resources assembled and evaluated over the last fifty years. The same germplasm collections allowed inheritance studies and the improvement of bean breeding methods, when looking for combining ability, tolerance to abiotic stress or tagging a resistance. The coming storms in areas of bean production (e.g. increased demand due to demography in eastern Africa, extinction of crop wild relatives in Mesoamerica, drought in 60% of bean growing areas worldwide) are resetting the timing to meet all breeding challenges at once and soon, but they also involve the genebanks to have the genetic solutions ready on the shelf or on the screen (or both). The contributions of the bean collections to advance knowledge on the nature, structure and evolution of Phaseolus genetic resources can now help the genebanks to check two extinctions: the extinction of populations in the wild, and the extinction of knowledge about cultivated diversity. Buying time on these two fronts will be difficult for genebanks, but the continuing improvement of conservation methods and efficiencies will contribute to find and enable the human talents for these daunting tasks. The above history shows many ways forward to ensure global food security in uncertain times. Acknowledgments The authors warmly thank the following individu- als for providing or confirming specific data about introduction and/or distribution of accessions: Sandra Albarraćın, Alejandro Borrero, Juan Carlos Guerrero, Ángela Hernández, Rigoberto Hidalgo, Dimary Libreros, Celia Lima, Carmenza Llano, Josefina Mart́ınez, Daniel Eduardo Salazar, Orlando Toro (deceased), Alba Marina Torres and Eliana Urquijo. The invitation by Peter Wenzl to the first author to write down a few mem- ories is fully acknowledged. The first author expresses deep gratitude to the following institutions for sup- port during four decades: Administration Générale de la Coopération au Développement, Bundesministerium für Wirtschaftliche Zusammenarbeit und Entwicklung, the Department for International Development, Euro- pean Union, Global Crop Diversity Trust, International Board for Plant Genetic Resources, International Cen- ter for Tropical Agriculture, United States Agency for International Development, United States Department of Agriculture, and the World Bank. The agricultural research services of the following countries are fully acknowledged for support in the field work and sub- sequent germplasm introduction: Argentina, Bolivia, Chile, Colombia, Costa Rica, Ecuador, El Salvador, Guatemala, Mexico, Panama and Peru. Author contributions DGD conceptualized and wrote the paper. DGD collated the data about use and impact for the first period of the genebank, while MS covered the most recent period. LGS compiled the data about germplasm distribution. MS and LGS re-checked the data of accession numbers. All authors read, revised and approved the manuscript. Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 33 Conflict of interest statement The first author has been responsible of CIAT genebank, as Head of the Genetic Resources Unit (1996-2009) and as Leader of the Genetic Resources Program (2009- 2016), with over seventy Staff members operating in five experimental stations and three labs, for three germplasm collections (bean, cassava and tropical forages) of over 67,000 accessions. The second author has been responsible for all genebank operations in 2017 to date, which include the regeneration of bean and tropical forages collections in the experimental stations and the conservation in the labs. The third author has been responsible since 2009 for all operations related to seed conservation of the bean and tropical forages collections, which include germplasm distribution. References Abawi, G. S., Provvidenti, R., Crosier, D. C., and Hunter, J. E. (1978). Inheritance of resistance to white mold disease in Phaseolus coccineus. J. Hered 69, 200–202. doi: https://doi.org/10.1093/ oxfordjournals.jhered.a108926 Acosta-Gallegos, J. A., Kelly, J. D., and Gepts, P. (2007). Prebreeding in common bean and use of genetic diversity from wild germplasm. Crop Sci 47, 44–59. doi: https://doi.org/10.2135/cropsci2007.04. 0008IPBS Acosta-Gallegos, J. A., Quintero, C., Vargas, J., Toro, O., Tohme, J., and Cardona, C. (1998). A new variant of arcelin in wild common bean, Phaseolus vulgaris L., from southern Mexico. Genet. Resources & Crop Evol 45, 235–242. doi: https://doi.org/10.1023/A: 1008636132108 Adams, M. W. (1973). Plant architecture and physiological efficiency in the field bean. In Potential of field beans and other food legumes in Latin America, ed. Wall, D., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 266-278. Aguilar, O. M., Riva, O., and Peltzer, E. (2004). Analysis of Rhizobium etli and its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc. Natl. Acad. Sci. USA 101, 13548–13553. doi: https://doi.org/10.1073/ pnas.0405321101 Allard, R. W. (1970). Problems of maintenance. In Genetic resources in plants: their exploration and conservation, ed. Frankel, O. H. and Bennett, E., (Oxford, United Kingdom: Blackwell Scientific Publications), 491-499. Aragão, F. J. L., Ribeiro, S. G., Barros, L. M. G., Brasileiro, A. C. M., Maxwell, D. P., Rech, E. L., and Faria, J. C. (1998). Transgenic beans (Phaseolus vulgaris L.) engineered to express viral antisense RNAs show delayed and attenuated symptoms to bean golden mosaic geminivirus. Molec. Breed 4, 491–499. doi: https://doi.org/10.1023/A:1009613607559 Aragão, F. J. L., Vianna, G. R., Albino, M. M. C., and Rech, E. L. (2002). Transgenic dry bean tolerant to the herbicide glufosinate ammonium. Crop Sci 42, 1298–1302. doi: https://doi.org/10.2135/ cropsci2002.1298 Assefa, T., Assibi-Mahama, A., Brown, A. V., Cannon, E. K. S., Rubyogo, J. C., Rao, I. M., Blair, M. W., and Cannon, S. B. (2019). A review of breeding objectives, genomic resources, and marker-assisted methods in common bean (Phaseolus vulgaris L.). Mol. Breeding 39, 1–23. doi: https://doi.org/10.1007/s11032-018- 0920-0 Bandyopadhyay, A., Kancharla, N., Javalkote, V. S., Dasgupta, S., and Brutnell, T. P. (2020). CRISPR- Cas12a (Cpf1): a versatile tool in the plant genome editing tool box for agricultural advancement. Front. Plant Sci 11(584151), 1–17. doi: https://doi.org/10. 3389/fpls.2020.584151 Bannerot, H. (1989). The potential of hybrid beans. Current topics in breeding of com- mon bean 111-134. url: http://ciat-library. ciat.cgiar.org/Articulos Ciat/Digital/SB327. C87 International Bean Breeding Workshop 1988, Cali, Colombia. Current topics in bree.pdf. Bassett, M. J., Lee, R., Otto, C., and Mcclean, P. E. (2002). Classical and molecular genetic studies of the strong greenish yellow seedcoat color in ’Wagenaar’ and ’Enola’ common bean. J. Amer. Soc. Hort. Sci 127, 50–55. doi: https://doi.org/10.21273/JASHS.127.1. 50 Battisti, D. S. and Naylor, R. L. (2009). Historical warn- ings of future food insecurity with unprecedented sea- sonal heat. Science 323, 240–244. doi: https://doi. org/10.1126/science.1164363 Bayuelo-Jiménez, J., Debouck, D. G., and Lynch, J. (2002). Salinity tolerance in Phaseolus species during early vegetative growth. Crop Sci 42, 2184–2192. doi: https://doi.org/10.2135/cropsci2002.2184 Beaver, J. S. (1999). Improvement of large-seeded race Nueva Granada cultivars. In Common bean improvement in the twenty first century, ed. Singh, S. P., (Dordrecht, The Netherlands: Kluwer Academic Publishers), 275-288. Beaver, J. S., Godoy, G., Rosas, J. C., and Steadman, J. (2002). Estrategias para seleccionar frijol común con mayor resistencia a Mustia hilachosa. Agron. Mesoamer 13, 67–72. url: http://www.redalyc.org/ articulo.oa?id=43713113. Beaver, J. S., Muñoz-Perea, C. G., Osorno, J. M., Ferwerda, F. H., and Miklas, P. N. (2005). Registration of Bean Golden Yellow Mosaic Virus resistant dry bean germplasm lines PR9771-3-2, PR0247-49, and PR0157-4-1. Crop Sci 45. doi: https://doi.org/10. 2135/cropsci2004.0487 Beebe, S., Lynch, J., Galwey, N., Tohme, J., and Ochoa, I. (1997). A geographical approach to identify phosphorus-efficient genotypes among landraces and wild ancestors of common bean. Euphytica 95, 325– 336. doi: https://doi.org/10.1023/A:1003008617829 Beebe, S., Rengifo, J., Gaitán, E., Duque, M. C., and Tohme, J. (2001). Diversity and origin of Andean https://doi.org/10.1093/oxfordjournals.jhered.a108926 https://doi.org/10.1093/oxfordjournals.jhered.a108926 https://doi.org/10.2135/cropsci2007.04.0008IPBS https://doi.org/10.2135/cropsci2007.04.0008IPBS https://doi.org/10.1023/A:1008636132108 https://doi.org/10.1023/A:1008636132108 https://doi.org/10.1073/pnas.0405321101 https://doi.org/10.1073/pnas.0405321101 https://doi.org/10.1023/A:1009613607559 https://doi.org/10.2135/cropsci2002.1298 https://doi.org/10.2135/cropsci2002.1298 https://doi.org/10.1007/s11032-018-0920-0 https://doi.org/10.1007/s11032-018-0920-0 https://doi.org/10.3389/fpls.2020.584151 https://doi.org/10.3389/fpls.2020.584151 http://ciat-library.ciat.cgiar.org/Articulos_Ciat/Digital/SB327.C87_International_Bean_Breeding_Workshop_1988,_Cali,_Colombia._Current_topics_in_bree.pdf http://ciat-library.ciat.cgiar.org/Articulos_Ciat/Digital/SB327.C87_International_Bean_Breeding_Workshop_1988,_Cali,_Colombia._Current_topics_in_bree.pdf http://ciat-library.ciat.cgiar.org/Articulos_Ciat/Digital/SB327.C87_International_Bean_Breeding_Workshop_1988,_Cali,_Colombia._Current_topics_in_bree.pdf http://ciat-library.ciat.cgiar.org/Articulos_Ciat/Digital/SB327.C87_International_Bean_Breeding_Workshop_1988,_Cali,_Colombia._Current_topics_in_bree.pdf https://doi.org/10.21273/JASHS.127.1.50 https://doi.org/10.21273/JASHS.127.1.50 https://doi.org/10.1126/science.1164363 https://doi.org/10.1126/science.1164363 https://doi.org/10.2135/cropsci2002.2184 http://www.redalyc.org/articulo.oa?id=43713113 http://www.redalyc.org/articulo.oa?id=43713113 https://doi.org/10.2135/cropsci2004.0487 https://doi.org/10.2135/cropsci2004.0487 https://doi.org/10.1023/A:1003008617829 34 Debouck et al Genetic Resources (2021), 2 (4), 21–43 landraces of common bean. Crop Sci 41, 854–862. doi: https://doi.org/10.2135/cropsci2001.413854x Beebe, S. E. (1997). La colección núcleo del fŕıjol y la búsqueda de genes útiles: el caso de tolerancia a bajo fósforo. In Taller de mejoramiento de fŕıjol para el siglo XXI: bases para una estrategia para América Latina, ed. Singh, S. P. and Voysest, O., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 3-8. (in Spanish). Beebe, S. E. (2012). Common bean breeding in the tropics. Plant Breeding Reviews 36, 357–426. doi: https://doi.org/10.1002/9781118358566.ch5 Beebe, S. E., Bliss, F. A., and Schwartz, H. F. (1981). Root rot resistance in common bean germplasm of Latin American origin. Plant Disease 65, 485–489. doi: https://doi.org/10.1094/PD-65-485 Beebe, S. E., Cardona, C., D́ıaz, O., Rodŕıguez, F., Mancia, E., and Asquejay, S. (1993). Development of common bean (Phaseolus vulgaris L.) lines resistant to the pod weevil, Apion godmani Wagner, in Central America. Euphytica 69, 83–88. doi: https://doi.org/ 10.1007/BF00021729 Beebe, S. E. and Debouck, D. G. (2019). Common beans and Lima beans in the northern Andes: evolutionary riddles and potential utility. Annu. Rept Bean Improvement Coop. (USA) 62, xxii–xxxi. url: https: //hdl.handle.net/10568/101566. Beebe, S. E., González, A. V., and Rengifo, J. (2000a). Research on trace minerals in the common bean. Food & Nutrition Bull 21, 387–391. doi: https://doi.org/10. 1177/156482650002100408 Beebe, S. E., Ramı́rez, J., Jarvis, A., Rao, I. M., Mosquera, G., Bueno, J. M., and Blair, M. (2011). Genetic improvement of common beans and the challenges of climate change. In Crop adaptation to climate change, ed. Yadav, S. S., Redden, R. J., Hatfield, J. L., Lotze- Campen, H., and Hall, A. E. (John Wiley & Sons Ltd. and Blackwell Publishing Ltd), 356-369. Beebe, S. E., Rao, I. M., Blair, M. W., and Acosta- Gallegos, J. A. (2013). Phenotyping common beans for adaptation to drought. Front. Physiol 4, 1–20. doi: https://doi.org/10.3389/fphys.2013.00035 Beebe, S. E., Rao, I. M., Cajiao, C., and Grajales, M. (2008). Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Sci 48, 582–592. doi: https://doi.org/10.2135/cropsci2007.07.0404 Beebe, S. E., Rojas-Pierce, M., Yan, X., Blair, M. W., Pedraza, F., Muñoz, F., Tohme, J., and Lynch, J. P. (2006). Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46, 413–423. doi: https: //doi.org/10.2135/cropsci2005.0226 Beebe, S. E., Skroch, P. W., Tohme, J., Duque, M. C., Pedraza, F., and Nienhuis, J. (2000b). Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD. Crop Sci 40, 264–273. doi: https: //doi.org/10.2135/cropsci2000.401264x Bhatta, B. P. and Malla, S. (2020). Improving horticul- tural crops via CRISPR/ Cas9: current successes and prospects. Plants 9, 1–19. doi: https://doi:10.3390/ plants9101360 Bitocchi, E., Bellucci, E., Giardini, A., Rau, D., Rodŕıguez, M., Biagetti, E., Santilocchi, R., Spagnoletti-Zeuli, P., Gioia, T., Logozzo, G., Attene, G., Nanni, L., and Papa, R. (2013). Molecular analysis of the parallel domestication of the common bean (Phaseolus vulgaris) in Mesoamerica and the Andes. New Phytol 197, 303–313. doi: https://doi.org/10.1111/j.1469- 8137.2012.04377.x Blair, M. W., Astudillo, C., Rengifo, J., Beebe, S. E., and Graham, R. (2011). QTL analyses for seed iron and zinc concentrations in an intra-genepool population of Andean common beans (Phaseolus vulgaris L.). Theor. Appl. Genet 122, 511–521. doi: https://doi.org/doi: 10.1007/s00122-010-1465-8 Blair, M. W. and Beaver, J. S. (1992). Resistance to the sweet potato whitefly (Bemisia tabaci), the vector of Bean Golden Mosaic Virus in dry beans (Phaseolus vulgaris). Annu. Rept. Bean Improvement Coop. (USA) 35, 154–155. url: https://naldc.nal.usda. gov/download/IND50000040/PDF. Blair, M. W., D́ıaz, J. M., Hidalgo, R., D́ıaz, L. M., and Duque, M. C. (2007). Microsatellite characterization of Andean races of common bean (Phaseolus vulgaris L.). Theor. Appl. Genet 116, 29–43. doi: https://doi. org/10.1007/s00122-007-0644-8 Blair, M. W., Iriarte, G., and Beebe, S. (2006). QTL analysis of yield traits in an advanced backcross population derived from a cultivated Andean x wild common bean (Phaseolus vulgaris L.) cross. Theor. Appl. Genet 112, 1149–1163. doi: https://doi.org/doi: 10.1007/s00122-010-1465-8 Blair, M. W., Medina, J. I., Astudillo, C., Rengifo, J., Beebe, S. E., Machado, G., and Graham, R. (2010). QTL for seed iron and zinc concentration and content in a Mesoamerican common bean (Phaseolus vulgaris L.) population. Theor. Appl. Genet 121, 1059–1070. doi: https://doi.org/10.1007/s00122-010-1371-0 Blair, M. W., Soler, A., and Cortés, A. J. (2012). Diversification and population structure in common beans (Phaseolus vulgaris L.). PLoS ONE 7, 1–12. doi: https://doi.org/10.1371/journal.pone.0049488 Borlaug, N. E. (1983). Contributions of conventional plant breeding to food production. Science 219, 689– 693. doi: https://doi.org/10.1126/science.219.4585. 689 Broughton, W. J., Hernández, G., Blair, M., Beebe, S., Gepts, P., and Vanderleyden, J. (2003). Beans (Phaseolus spp.) - model food legumes. Plant & Soil 252, 55–128. doi: https://doi.org/10.1023/A: 1024146710611 Buend́ıa, H. F., Beebe, S., Blair, M., Terán, H., and Pedraza, F. (2003). Identificaci ón de marcadores moleculares asociados a genes de rendimiento en una poblaci ón R.C2F3.7 de fŕıjol común Phaseolus vulgaris https://doi.org/10.2135/cropsci2001.413854x https://doi.org/10.1002/9781118358566.ch5 https://doi.org/10.1094/PD-65-485 https://doi.org/10.1007/BF00021729 https://doi.org/10.1007/BF00021729 https://hdl.handle.net/10568/101566 https://hdl.handle.net/10568/101566 https://doi.org/10.1177/156482650002100408 https://doi.org/10.1177/156482650002100408 https://doi.org/10.3389/fphys.2013.00035 https://doi.org/10.2135/cropsci2007.07.0404 https://doi.org/10.2135/cropsci2005.0226 https://doi.org/10.2135/cropsci2005.0226 https://doi.org/10.2135/cropsci2000.401264x https://doi.org/10.2135/cropsci2000.401264x https://doi:10.3390/plants9101360 https://doi:10.3390/plants9101360 https://doi.org/10.1111/j.1469-8137.2012.04377.x https://doi.org/10.1111/j.1469-8137.2012.04377.x https://doi.org/doi:10.1007/s00122-010-1465-8 https://doi.org/doi:10.1007/s00122-010-1465-8 https://naldc.nal.usda.gov/download/IND50000040/PDF https://naldc.nal.usda.gov/download/IND50000040/PDF https://doi.org/10.1007/s00122-007-0644-8 https://doi.org/10.1007/s00122-007-0644-8 https://doi.org/doi:10.1007/s00122-010-1465-8 https://doi.org/doi:10.1007/s00122-010-1465-8 https://doi.org/10.1007/s00122-010-1371-0 https://doi.org/10.1371/journal.pone.0049488 https://doi.org/10.1126/science.219.4585.689 https://doi.org/10.1126/science.219.4585.689 https://doi.org/10.1023/A:1024146710611 https://doi.org/10.1023/A:1024146710611 Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 35 L. (DOR390 x G19892). Fitotecnia Colombiana 1, 57– 64. (in Spanish). Burkart, A. and Brücher, H. (1953). Phaseolus aborig- ineus Burkart, die mutmaßliche andine Stammform der Kulturbohne. Züchter 23, 65–72. doi: https://doi. org/10.1007/BF00712180 Burle, M. L., Fonseca, J. R., Kami, J. A., and Gepts, P. (2010). Microsatellite diversity and genetic structure among common bean (Phaseolus vulgaris L.) landraces in Brazil, a secondary center of diversity. Theor. Appl. Genet 121, 801–813. doi: https://doi.org/ 10.1007/s00122-010-1350-5 Byrne, P. F., Volk, G. M., Gardner, C., Gore, M. A., Simon, P. W., and Smith, S. (2018). Sustaining the future of plant breeding: the critical role of the USDA- ARS national plant germplasm system. Crop Sci 58, 451–468. doi: https://doi.org/10.2135/cropsci2017. 05.0303 Campa, A., Pañeda, A., Pérez-Vega, E., Giraldez, R., and Ferreira, J. J. (2011). Mapping and use of seed protein loci for marker-assisted selection of growth habit and photoperiod response in Nuña bean (Phaseolus vulgaris L.). Euphytica 179, 383–391. doi: https:// doi.org/10.1007/s10681-010-0320-y Cardona, C., Kornegay, J., Posso, C. E., Morales, F., and Ramı́rez, H. (1990). Comparative value of four arcelin variants in the development of dry bean lines resistant to the Mexican bean weevil. Entomol. Exp. Appl 56, 197–206. doi: https://doi.org/10.1111/j.1570-7458. 1990.tb01397.x Cattan-Toupance, I., Michalakis, Y., and Neema, C. (1998). Genetic structure of wild bean populations in their South-Andean centre of origin. Theor. Appl. Genet 96, 844–851. doi: https://doi.org/10.1007/ s001220050811 Chacón-Sánchez, M. I., Mart́ınez-Castillo, J., Duitama, J., and Debouck, D. G. (2021). Gene flow in Phaseolus beans and its role as a plausible driver of ecological fitness and expansion of cultigens. Front. Ecol. Evol 9, 1–25. doi: https://doi.org/10.3389/fevo.2021. 618709 Chacón-Sánchez, M. I., Pickersgill, B., and Debouck, D. G. (2005). Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theor. Appl. Genet 110, 432–444. doi: https://doi.org/10. 1007/s00122-004-1842-2 Chacón-Sánchez, M. I., Pickersgill, B., Debouck, D. G., and Salvador-Arias, J. (2007). Phylogeographic analysis of the chloroplast DNA variation in wild common bean (Phaseolus vulgaris L.) in the Americas. Pl. Syst. Evol 266, 175–195. doi: https://doi.org/10. 1007/s00606-007-0536-z Cichy, K. A., Porch, T. G., Beaver, J. S., Cregan, P., Fourie, D., Glahn, R. P., Grusak, M. A., Kamfwa, K., Katuuramu, D. N., Mcclean, P., Mndolwa, E., Nchimbi- Msolla, S., Pastor-Corrales, M. A., and Miklas, P. N. (2015). A Phaseolus vulgaris diversity panel for Andean bean improvement. Crop Sci 55, 2149–2160. doi: https://doi.org/10.2135/cropsci2014.09.0653 Clawson, D. L. (1985). Harvest security and intraspe- cific diversity in traditional tropical agriculture. Econ. Bot 39, 56–67. doi: https://doi.org/10.1007/ BF02861175 Cortés, A. J. and Blair, M. W. (2018). Genotyping by sequencing and genome-environment associations in wild common bean predict widespread divergent adaptation to drought. Front. Plant Sci 9, 1–13. doi: https://doi.org/10.3389/fpls.2018.00128 Cruz-Balarezo, J., Camarena-Mayta, F., Baudoin, J. P., Huaringa-Joaqúın, A., and Blas-Sevillano, R. (2009). Evaluación agromorfológica y caracterización molec- ular de la ñuña (Phaseolus vulgaris L.). Idesia (Chile) 27, 29–40. (in Spanish). doi: https://doi.org/10. 4067/S0718-34292009000100005 Cuellar, J. (2003). Estaciones experimentales de Quilichao y Popayán: 25 años de investigación. (Cali, Colombia: Centro Internacional de Agricultura Tropical), 1-8, (in Spanish). Debouck, D. G. (1992). Frijoles, Phaseolus spp. In Bermejo, E. H. and León, J., Cultivos marginados: otra perspectiva de 1492, Food and Agriculture Organization of the United Nations, 92-97. Debouck, D. G. (1999). Diversity in Phaseolus species in relation to the common bean. In Common bean improvement in the twenty-first century, ed. Singh, S. P., (Dordrecht, the Netherlands: Kluwer Academic Publishers), 25-52. Debouck, D. G. (2000). Biodiversity, ecology and genetic resources of Phaseolus beans - Seven answered and unanswered questions. In Wild legumes , ed. Oono, K., (Tsukuba, Ibaraki, Japan: Ministry of Agriculture, Forestry and Fisheries, and National Institute of Agrobiological Resources), 95-123. Debouck, D. G. (2021). Phaseolus beans (Leguminosae, Phaseoleae): a checklist and notes on their taxonomy and ecology. J. Bot. Res. Inst. Texas 15, 73–111. doi: https://doi.org/10.17348/jbrit.v15.i1.1052 Debouck, D. G., Maquet, A., and Posso, C. E. (1989). Biochemical evidence for two different gene pools in Lima beans (Phaseolus lunatus L.). Annu. Rept. Bean Improvement Coop. (USA) 32, 58– 59. url: https://naldc.nal.usda.gov/naldc/download. xhtml?id=IND89038220&content=PDF. Delgado-Salinas, A., Bibler, R., and Lavin, M. (2006). Phylogeny of the genus Phaseolus (Leguminosae): a recent diversification in an ancient landscape. Syst. Bot 31. doi: https://10.1600/036364406779695960 Dillen, W., Clercq, J. D., Goossens, A., Montagu, M. V., and Angenon, G. (1997). Agrobacterium-mediated transformation of Phaseolus acutifolius A. Gray. Theor. Appl. Genet 94, 151–158. doi: https://doi.org/10. 1007/s001220050394 Donald, C. M. (1968). The breeding of crop ideotypes. Euphytica 17, 385–403. doi: https://doi.org/10.1007/ BF00056241 https://doi.org/10.1007/BF00712180 https://doi.org/10.1007/BF00712180 https://doi.org/10.1007/s00122-010-1350-5 https://doi.org/10.1007/s00122-010-1350-5 https://doi.org/10.2135/cropsci2017.05.0303 https://doi.org/10.2135/cropsci2017.05.0303 https://doi.org/10.1007/s10681-010-0320-y https://doi.org/10.1007/s10681-010-0320-y https://doi.org/10.1111/j.1570-7458.1990.tb01397.x https://doi.org/10.1111/j.1570-7458.1990.tb01397.x https://doi.org/10.1007/s001220050811 https://doi.org/10.1007/s001220050811 https://doi.org/10.3389/fevo.2021.618709 https://doi.org/10.3389/fevo.2021.618709 https://doi.org/10.1007/s00122-004-1842-2 https://doi.org/10.1007/s00122-004-1842-2 https://doi.org/10.1007/s00606-007-0536-z https://doi.org/10.1007/s00606-007-0536-z https://doi.org/10.2135/cropsci2014.09.0653 https://doi.org/10.1007/BF02861175 https://doi.org/10.1007/BF02861175 https://doi.org/10.3389/fpls.2018.00128 https://doi.org/10.4067/S0718-34292009000100005 https://doi.org/10.4067/S0718-34292009000100005 https://doi.org/10.17348/jbrit.v15.i1.1052 https://naldc.nal.usda.gov/naldc/download.xhtml?id=IND89038220&content=PDF https://naldc.nal.usda.gov/naldc/download.xhtml?id=IND89038220&content=PDF https://10.1600/036364406779695960 https://doi.org/10.1007/s001220050394 https://doi.org/10.1007/s001220050394 https://doi.org/10.1007/BF00056241 https://doi.org/10.1007/BF00056241 36 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Doudna, J. A. and Charpentier, E. (2014). The new frontier of genome engineering with CRISPR-Cas9. Science 346(6213), 1258097. doi: https://doi.org/10. 1126/science.1258096 Dudnik, N. S., Thormann, I., and Hodgkin, T. (2001). The extent of use of plant genetic resources in research: a literature survey. Crop Sci 41. doi: https: //doi.org/10.2135/cropsci2001.4116 Estrada-Navarrete, G., Alvarado-Affantranger, X., Oli- vares, J. E., Guillén, G., D́ıaz-Camino, C., Campos, F., Quinto, C., Gresshoff, P. M., and Sánchez, F. (2007). Fast, efficient and reproducible genetic transforma- tion of Phaseolus spp. by Agrobacterium rhizogenes. Nature Protocols 2, 1819–1824. doi: https://doi.org/ 10.1038/nprot.2007.259 Evans, A. M. (1973). I. Commentary upon: plant architecture and physiological efficiency in the field bean. In Wall, D., Potential of field beans and other food legumes in Latin America, Centro Internacional de Agricultura Tropical, 279-286. Evans, A. M. (1976). Beans - Phaseolus spp. (Leguminosae - Papilionatae). In Evolution of crop plants, ed. Simmonds, N. W., (London, United Kingdom: Longman), 168-172. Evenson, R. E. and Gollin, D. (2003). Assessing the impact of the Green Revolution, 1960 to 2000. Science 300, 758–762. doi: https://doi.org/10.1126/science. 1078710 FAO (2002). The International Treaty on Plant Genetic Resources for Food and Agriculture (Rome, Italy: Food and Agriculture Organization of the United Nations), 1-45. url: http://www.fao.org/3/a-i0510e.pdf Fowler, C. (2016). Seeds on ice: Svalbard and the global seed vault (Westport, Connecticut, USA: Prospecta Press), 1-161. Foyer, C. H., Lam, H. M., Nguyen, H. T., Siddique, K. H. M., Varshney, R. K., Colmer, T. D., Cowling, W., Bramley, H., Mori, T. A., Hodgson, J. M., Cooper, J. W., Miller, A. J., Kunert, K., Vorster, J., Cullis, C., Ozga, J. A., Wahlqvist, M. L., Liang, Y., Shou, H., ..., and Considine, M. J. (2016). Neglecting legumes has compromised human health and sustainable food production. Nature Plants 2, 1–10. doi: https://doi. org/10.1038/NPLANTS.2016.112 Frankel, O. H. and Brown, A. H. D. (1984). Plant genetic resources today: a critical appraisal. In Crop genetic resources: conservation and evaluation, ed. Holden, J. H. W. and Williams, J. T., (London, England: George Allen & Unwin Publishers Ltd), 249-257. Frankel, O. H. and Hawkes, J. G. (1975). Crop genetic resources for today and tomorrow, ed. Frankel, O. H. and Hawkes, J. G. (Cambridge, United Kingdom: Cambridge University Press), 492p. Freeman, G. F. (1913). The tepary, a new cultivated legume from the Southwest. Bot. Gaz 56, 395–417. doi: https://doi.org/10.1086/331183 Freytag, G. F. and Debouck, D. G. (2002). Taxon- omy, distribution, and ecology of the genus Phaseo- lus (Leguminosae-Papilionoideae) in North America, Mexico and Central America . SIDA Bot. Misc 23, 1– 300. doi: https://doi.org/10568/54291 Fu, Y. B. (2017). The vulnerability of plant genetic resources conserved ex situ. Crop Sci 57, 2314–2328. doi: https://doi.org/10.2135/cropsci2017.01.0014 Galwey, N. W. (1983). Characteristics of the common bean, Phaseolus vulgaris, associated with resistance to the leafhopper Empoasca kraemeri. Ann. Appl. Biol 102, 161–175. doi: https://doi.org/10.1111/j.1744- 7348.1983.tb02677.x Garcia, T., Duitama, J., Smolenski-Zullo, S., Gil, J., Ariani, A., Dohle, S., Palkovic, A., Skeen, P., Bermudez-Santana, C. I., Debouck, D. G., Mart́ınez- Castillo, J., Gepts, P., and Chacón-Sánchez, M. I. (2021). Comprehensive genomic resources related to domestication and crop improvement traits in Lima bean. Nature Communic 12, 1–17. doi: https://doi/ org/10.1038/s41467-021-20921-1 Garrido, B., Nodari, R., Debouck, D. G., and Gepts, P. (1991). Uni-2 - A dominant mutation affect- ing leaf development in Phaseolus vulgaris. J. Hered 82, 181–183. doi: https://doi.org/10.1093/ oxfordjournals.jhered.a111059 Garza, R., Vera, J., Cardona, C., Barcenas, N., and Singh, S. P. (2001). Hypersensitive response of beans to Apion godmani (Coleoptera: Cucurlionidae). J. Econ. Entomol 94, 958–962. doi: https://doi.org/10.1603/ 0022-0493-94.4.958 Garzón, G. L. N., Blair, M. W., Jara, C., Castellanos, G., Mosquera, G., Cajiao, C., Beebe, S., Ligarreto, G. A., Oliveros, G. O. A., and Villarraga, P. (2011). Disease response of interspecific common bean (Phaseolus vulgaris) x scarlet runner or year-long bean (P. coccineus and P. dumosus) breeding lines for Ascochyta blight resistance. Annu. Rept. Bean Improvement Coop. (USA) 54, 122–123. Gentry, H. S. (1969). Origin of the common bean, Phaseolus vulgaris. Econ. Bot 23, 55–69. url: https: //www.jstor.org/stable/4253014 Gepts, P. (2002). A comparison between crop domestication, classical plant breeding, and genetic engineering. Crop Sci 42, 1780–1790. doi: https: //doi.org/10.2135/cropsci2002.1780 Gepts, P. (2006). Plant genetic resources conservation and utilization: the accomplishments and future of a societal insurance policy. Crop Sci 46, 2278– 2292. doi: https://doi.org/10.2135/cropsci2006.03. 0169gas Gepts, P., Osborn, T. C., Rashka, K., and Bliss, F. A. (1986). Phaseolin protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris L.): evidence for multiple centers of domestication. Econ. Bot 40, 451–468. doi: https: //doi.org/10.1007/BF02859659 Gioia, T., Logozzo, G., Attene, G., Bellucci, E., Benedet- telli, S., Negri, V., Papa, R., and Zeuli, P. S. (2013). Evidence for introduction bottleneck and extensive inter-gene pool (Mesoamerica x Andes) hybridization in the European common bean (Phaseolus vulgaris L.) https://doi.org/10.1126/science.1258096 https://doi.org/10.1126/science.1258096 https://doi.org/10.2135/cropsci2001.4116 https://doi.org/10.2135/cropsci2001.4116 https://doi.org/10.1038/nprot.2007.259 https://doi.org/10.1038/nprot.2007.259 https://doi.org/10.1126/science.1078710 https://doi.org/10.1126/science.1078710 http://www.fao.org/3/a-i0510e.pdf https://doi.org/10.1038/NPLANTS.2016.112 https://doi.org/10.1038/NPLANTS.2016.112 https://doi.org/10.1086/331183 https://doi.org/10568/54291 https://doi.org/10.2135/cropsci2017.01.0014 https://doi.org/10.1111/j.1744-7348.1983.tb02677.x https://doi.org/10.1111/j.1744-7348.1983.tb02677.x https://doi/org/10.1038/s41467-021-20921-1 https://doi/org/10.1038/s41467-021-20921-1 https://doi.org/10.1093/oxfordjournals.jhered.a111059 https://doi.org/10.1093/oxfordjournals.jhered.a111059 https://doi.org/10.1603/0022-0493-94.4.958 https://doi.org/10.1603/0022-0493-94.4.958 https://www.jstor.org/stable/4253014 https://www.jstor.org/stable/4253014 https://doi.org/10.2135/cropsci2002.1780 https://doi.org/10.2135/cropsci2002.1780 https://doi.org/10.2135/cropsci2006.03.0169gas https://doi.org/10.2135/cropsci2006.03.0169gas https://doi.org/10.1007/BF02859659 https://doi.org/10.1007/BF02859659 Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 37 germplasm. PLoS ONE 8(e75974), 1–14. doi: https: //doi.org/10.1371/journal.pone.0075974 Goettsch, B., Urquiza-Haas, T., Koleff, P., Acevedo- Gasman, F., Aguilar-Meléndez, A., Alavez, V., Alejandre-Iturbide, G., Aragón-Cuevas, F., Azurdia- Pérez, C., Carr, J. A., Castellanos-Morales, G., Cerén, G., Contreras-Toledo, A. R., Correa-Cano, M. E., Cruz-Larios, L. D. L., Debouck, D. G., Delgado-Salinas, A., Gómez-Ruiz, E. P., González-Ledesma, M., ..., and Jenkins, R. K. B. (2021). Extinction risk of Mesoamer- ican crop wild relatives. Plants, People, Planet 3(6), 775–795. doi: https://doi.org/10.1002/ppp3.10225 Gonçalves-Vidigal, M. C., Cruz, A. S., Garcia, A., Kami, J., Vidigal-Filho, P. S., Sousa, L. L., Mcclean, P., Gepts, P., and Pastor-Corrales, M. A. (2011). Linkage mapping of the Phg-1 and Co-14 genes for resistance to angular leaf spot and anthracnose in the common bean cultivar AND 277. Theor. Appl. Genet. 112, 893– 903. doi: https://doi.org/10.1007/s00122-010-1496- 1 Gonçalves-Vidigal, M. C., Gilio, T. A. S., Valentini, G., Vaz-Bisneta, M., Vidigal-Filho, P. S., Song, Q., Oblessuc, P. R., and Melotto, M. (2020). New Andean source of resistance to anthracnose and angular leaf spot: fine-mapping of disease-resistance genes in California Dark Red Kidney common bean cultivar. PLoS ONE 15, 1–19. doi: https://doi.org/10.1371/ journal.pone.0235215 Guerra-Garćıa, A., Suárez-Atilano, M., Mastretta-Yanes, A., Delgado-Salinas, A., and Piñero, D. (2017). Domestication genomics of the open-pollinated scarlet runner bean (Phaseolus coccineus L.). Front. Plant Sci 8(1891), 1–15. doi: https://doi.org/10.3389/fpls. 2017.01891 Gutiérrez, J. A. and Singh, S. P. (1985). Heterosis and inbreeding depression in dry bush beans, Phaseolus vulgaris L. Can. J. Plant Sci 65, 243–249. doi: https: //doi.org/10.4141/cjps85-036 Guzmán, P., Gilbertson, R. L., Nodari, R., Johnson, W. C., Temple, S. R., Mandala, D., Mkandawire, A. B. C., and Gepts, P. (1995). Characterization of variability in the fungus Phaeoisariopsis griseola suggests coevo- lution with the common bean (Phaseolus vulgaris). Phytopathology 85, 600–607. doi: https://doi.org/10. 1094/Phyto-85-600 Halewood, M., Jamora, N., López-Noriega, I., Anglin, N. L., Wenzl, P., Payne, T., Ndjiondjop, M. N., Guarino, L., Kumar, P. L., Yazbek, M., Muchugi, A., Azevedo, V., Tchamba, M., Jones, C. S., Venuprasad, R., Roux, N., Rojas, E., and Lusty, C. (2020). Germplasm acquisition and distribution by CGIAR genebanks. Plants 9(10), 1–29. doi: https://doi.org/10.3390/plants9101296 Harlan, J. R. (1978). Sources of genetic defense. Ann. N.Y. Acad. Sci 287, 345–356. doi: https://doi.org/10. 1111/j.1749-6632.1977.tb34252.x Hart, J. P. and Griffiths, P. D. (2014). Resistance to Clover yellow vein virus in common bean germplasm. Crop Sci 54, 2609–2618. doi: https://doi.org/10. 2135/cropsci2014.03.0263 Hedrick, U. P. (1931). The vegetables of New York volume 1 part 2. (Albany, New York: New York Agricultural Experiment Station. JB Lyon Company Printers), 82-83. Heiser, C. B. (1990). Seed to civilization - The story of food (Cambridge, Massachusetts, USA: Harvard University Press), 228p. Hernández-Bravo, G. (1973). Potentials and problems of production of dry beans in the lowland tropics. In Potentials of field beans and other food legumes in Latin America, ed. Wall, D., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 144-150. Hernández-Xolocotzi, E. (1973). Commentary upon plant introduction and germplasm of Phaseolus vulgaris and other food legumes. In Potentials of field beans and other food legumes in Latin America, ed. Wall, D., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 253-258. Hickey, L. T., Hafeez, A. N., Robinson, H., Jackson, S. A., Leal-Bertioli, S. C. M., Tester, M., Gao, C., Godwin, I. D., Hayes, B. J., and Wulff, B. B. H. (2019). Breeding crops to feed 10 billion. Nature Biotechnol 37, 744– 754. doi: https://doi.org/10.1038/s41587-019-0152- 9 Hidalgo, R. (1991). CIAT’s world Phaseolus collection. In Common beans: research for crop improvement, ed. van Schoonhoven, A. and Voysest, O., (Wallingford, United Kingdom: CABI), 163-197. Hidalgo, R. and Beebe, S. (1997). Phaseolus beans. In Biodiversity in trust - Conservation and use of plant genetic resources in CGIAR Centres, ed. Fuccillo, D., Sears, L., and Stapleton, P., (Cambridge, United Kingdom: Cambridge University Press), 139-155. Hidalgo, R., Rubiano, H., and Toro, O. (1992). Catálogo de germoplasma de fŕıjol común Phaseolus vulgaris L., ed. Hidalgo, R., Rubiano, H., and Toro, O. (Cali, Colombia: Centro Internacional de Agricultura Tropical), 450p. url: http://ciat-library.ciat.cgiar.org/ ciat digital/CIAT/books/historical/028.1.pdf Hunter, J. E., Dickson, M. H., Boettger, M. A., and Cigna, J. A. (1982). Evaluation of plant introductions of Phaseolus spp. for resistance to white mold. Plant Dis 66, 320–322. doi: https://doi.org/10.1094/PD- 66-320 Hymowitz, T. and Bernard, R. L. (1991). Origin of the soybean and germplasm introduction and development in North America. In Use of plant introductions in cultivar development part 1, ed. Shands, H. L. and Wiesner, L. E. volume 17 of Crop Science Society of America Special Publication, 147-164. Islam, F. M. A., Basford, K. E., Jara, C., Redden, R. J., and Beebe, S. (2002). Seed compositional and disease resistance differences among gene pools in cultivated common bean. Genet. Resources & Crop Evol 49, 285– 293. doi: https://doi.org/10.1023/A:1015510428026 Jacobsen, H. J. (1999). Genetic transformation. In Common bean improvement in the twenty first-century, ed. Singh, S., (Dordrecht, The Netherlands: Kluwer Academic Publishers), 125-132. https://doi.org/10.1371/journal.pone.0075974 https://doi.org/10.1371/journal.pone.0075974 https://doi.org/10.1002/ppp3.10225 https://doi.org/10.1007/s00122-010-1496-1 https://doi.org/10.1007/s00122-010-1496-1 https://doi.org/10.1371/journal.pone.0235215 https://doi.org/10.1371/journal.pone.0235215 https://doi.org/10.3389/fpls.2017.01891 https://doi.org/10.3389/fpls.2017.01891 https://doi.org/10.4141/cjps85-036 https://doi.org/10.4141/cjps85-036 https://doi.org/10.1094/Phyto-85-600 https://doi.org/10.1094/Phyto-85-600 https://doi.org/10.3390/plants9101296 https://doi.org/10.1111/j.1749-6632.1977.tb34252.x https://doi.org/10.1111/j.1749-6632.1977.tb34252.x https://doi.org/10.2135/cropsci2014.03.0263 https://doi.org/10.2135/cropsci2014.03.0263 https://doi.org/10.1038/s41587-019-0152-9 https://doi.org/10.1038/s41587-019-0152-9 http://ciat-library.ciat.cgiar.org/ciat_digital/CIAT/books/historical/028.1.pdf http://ciat-library.ciat.cgiar.org/ciat_digital/CIAT/books/historical/028.1.pdf https://doi.org/10.1094/PD-66-320 https://doi.org/10.1094/PD-66-320 https://doi.org/10.1023/A:1015510428026 38 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Johnson, N. L., Pachico, D., and Voysest, O. (2003). The distribution of benefits from public international germplasm banks: the case of beans in Latin America. Agricult. Econ 29, 277–286. doi: https://doi.org/10. 1016/S0169-5150(03)00055-0 Kamfwa, K., Beaver, J. S., Cichy, K. A., and Kelly, J. D. (2018). QTL mapping of resistance to bean weevil in common bean. Crop Sci 58, 2370–2378. doi: https: //doi.org/10.2135/cropsci2018.02.0106 Kaplan, L. and Kaplan, L. N. (1992). Beans of the Americas. In Chillies to chocolate – Food the Americas gave the world, ed. Foster, N. and Cordell, L. S., (Tucson, Arizona, USA: The University of Arizona Press), 61-79. Kastner, T., Ibarrola-Rivas, M. J., Koch, W., and Nonhebel, S. (2012). Global changes in diets and the consequences for land requirements for food. Proc. Natl. Acad. Sci. USA 109, 6868–6872. doi: http://dx. doi.org/10.1073/pnas.1117054109 Kelly, J. D. (2001). Remaking bean plant architecture for efficient production. Adv. Agron 71, 109–143. doi: https://doi.org/10.1016/S0065-2113(01)71013-9 Kelly, J. D. (2004). Advances in common bean improvement: some case histories with broader applications. Acta Horticulturae 637, 99–122. doi: https://doi.org/10.17660/ActaHortic.2004.637.11 Kelly, J. D. and Miklas, P. N. (1999). Marker-assisted selection. In Common bean improvement in the twenty-first century, ed. Singh, S. P. (Kluwer Academic Publishers), 93-123. Khoury, C. K., Bjorkman, A. D., Dempewolf, H., Ramirez- Villegas, J., Guarino, L., Jarvis, A., Rieseberg, L. H., and Struik, P. C. (2014). Increasing homogeneity in global food supplies and the implications for food security. Proc. Natl. Acad. Sci. USA 111, 4001–4006. doi: https://doi.org/10.1073/pnas.1313490111 Klaedtke, S. M., Cajiao, C., Grajales, M., Polańıa, J., Borrero, G., Guerrero, A., Rivera, M., Rao, I., Beebe, S. E., and León, J. (2012). Photosynthate remobi- lization capacity from drought-adapted common bean (Phaseolus vulgaris L.) lines can improve yield poten- tial of interspecific populations within the secondary gene pool. J. Plant Breed. & Crop Sci 4, 49–61. doi: https://doi.org/10.5897/JPBCS11.087 Koinange, E. M. K. and Gepts, P. (1992). Hybrid weakness in wild Phaseolus vulgaris L. J. Hered 83, 135–139. doi: https://doi.org/10.1093/ oxfordjournals.jhered.a111173 Koo, B. W., Pardey, P. G., and Debouck, D. G. (2004). CIAT genebank. In Saving seeds - The economics of conserving crop genetic resources ex situ in the Future Harvest Centres of the CGIAR, ed. Koo, B. W., Pardey, P. G., and Wright, B. D., (Wallingford, United Kingdom: CABI Publishing), volume 13, 105-125. Kornegay, J. and Cardona, C. (1991). Breeding for insect resistance in beans. In Common beans: research for crop improvement, ed. van Schoonhoven, A. and Voysest, O., (Wallingford, United Kingdom: CABI), 619-648. Ku, H. K. and Ha, S. H. (2020). Improving nutritional and functional quality by genome editing of crops: status and perspectives. Front. Plant Sci 11, 1–14. doi: https://doi/10.3389/fpls.2020.577313 Kumar, P. L., Cuervo, M., Kreuze, J. F., Muller, G., Kulkarni, G., Kumari, S. G., Massart, S., Mezza- lama, M., Alakonya, A., Muchugi, A., Graziosi, I., Ndjiondjop, M. N., Sharma, R., and Teressa-Negayo, A. (2021). Phytosanitary interventions for safe global germplasm exchange and the prevention of trans- boundary pest spread: the role of CGIAR germplasm health units. Plants 10, 1–29. doi: https://doi.org/10. 3390/plants10020328 Kuzay, S., Hamilton-Conaty, P., Palkovic, A., and Gepts, P. (2020). Is the USDA core collection of common bean representative of genetic diversity of the species, as assessed by SNP diversity? Crop Sci 60, 1398–1414. doi: https://doi.org/10.1002/csc2.20032 Kwak, M. and Gepts, P. (2009). Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theor. Appl. Genet 118, 979–992. doi: https://doi.org/10.1007/s00122- 008-0955-4 Kwak, M., Kami, J. A., and Gepts, P. (2009). The putative Mesoamerican domestication center of Phaseolus vulgaris is located in the Lerma-Santiago basin of Mexico. Crop Sci 49, 554–563. doi: https://doi.org/ 10.2135/cropsci2008.07.0421 Larsen, R. C. and Miklas, P. N. (2004). Generation and molecular mapping of a sequence characterized amplified region marker linked with the Bct gene for resistance to Beet Curly Top Virus in common bean. Phytopathology 94, 320–325. doi: https://doi.org/10. 1094/PHYTO.2004.94.4.320 Lépiz-Ildefonso, R. and Navarro-Sandoval, F. J. (1983). Fŕıjol en el noroeste de México (tecnoloǵıa de producción). Instituto Nacional de Investigaciones Agŕıcolas. Secretaŕıa de Agricultura y Recursos Hidráulicos, Culiacán, Sinaloa, México, 1-69. Liebenberg, M. M., Mienie, C. M. S., and Pretorius, Z. A. (2006). The occurrence of rust resistance gene Ur-13 in common bean cultivars and lines. Euphytica 150, 365–386. doi: https://doi.org/10.1007/s10681-006- 9123-6 Lobaton, J. D., Miller, T., Gil, J., Ariza, D., Hoz, J. F. D. L., Soler, A., Beebe, S., Duitama, J., Gepts, P., and Raatz, B. (2018). Resequencing of common bean identifies regions of inter-gene pool introgression and provides comprehensive resources for molecular breeding. The Plant Genome 11, 1–21. doi: https://doi.org/10.3835/ plantgenome2017.08.0068 Lobell, D. B. and Gourdji, S. M. (2012). The influence of climate change on global crop productivity. Plant Physiol 160, 1686–1697. doi: https://doi.org/10. 1104/pp.112.208298 Lyman, J. (1984). Progress and planning for germplasm conservation of major food crops. FAO/IBPGR Plant Genet. Resources Newsl 60, 3–21. https://doi.org/10.1016/S0169-5150(03)00055-0 https://doi.org/10.1016/S0169-5150(03)00055-0 https://doi.org/10.2135/cropsci2018.02.0106 https://doi.org/10.2135/cropsci2018.02.0106 http://dx.doi.org/10.1073/pnas.1117054109 http://dx.doi.org/10.1073/pnas.1117054109 https://doi.org/10.1016/S0065-2113(01)71013-9 https://doi.org/10.17660/ActaHortic.2004.637.11 https://doi.org/10.1073/pnas.1313490111 https://doi.org/10.5897/JPBCS11.087 https://doi.org/10.1093/oxfordjournals.jhered.a111173 https://doi.org/10.1093/oxfordjournals.jhered.a111173 https://doi/10.3389/fpls.2020.577313 https://doi.org/10.3390/plants10020328 https://doi.org/10.3390/plants10020328 https://doi.org/10.1002/csc2.20032 https://doi.org/10.1007/s00122-008-0955-4 https://doi.org/10.1007/s00122-008-0955-4 https://doi.org/10.2135/cropsci2008.07.0421 https://doi.org/10.2135/cropsci2008.07.0421 https://doi.org/10.1094/PHYTO.2004.94.4.320 https://doi.org/10.1094/PHYTO.2004.94.4.320 https://doi.org/10.1007/s10681-006-9123-6 https://doi.org/10.1007/s10681-006-9123-6 https://doi.org/10.3835/plantgenome2017.08.0068 https://doi.org/10.3835/plantgenome2017.08.0068 https://doi.org/10.1104/pp.112.208298 https://doi.org/10.1104/pp.112.208298 Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 39 url:http://pascal-francis.inist.fr/vibad/index.php? action=getRecordDetail&idt=9218230 Lynam, J. and Byerlee, D. (2017). Forever pioneers - CIAT: 50 years contributing to a sustainable food future . . . and counting. CIAT Publication No. 444. International Center for Tropical Agriculture (CIAT), Cali, Colombia, 1-140. Lynch, J., González, A., Tohme, J., and Garćıa, J. (1992). Variation in characters related to leaf photosynthesis in wild bean populations. Crop Sci 32, 633–640. doi: https://doi.org/10.2135/cropsci1992. 0011183X003200030012x Mahuku, G. S., Jara, C., Cajiao, C., and Beebe, S. (2002). Sources of resistance to Colletotrichum lindemuthianum in the secondary gene pool of Phaseolus vulgaris and in crosses of primary and secondary gene pools. Plant Dis 86, 1383–1387. doi: https://doi.org/10.1094/PDIS.2002.86.12.1383 Mahuku, G. S., Jara, C., Cajiao, C., and Beebe, S. (2003). Sources of resistance to angular leaf spot (Phaeoisariopsis griseola) in common bean core collection, wild Phaseolus vulgaris and secondary gene pool. Euphytica 130, 303–313. doi: https://doi. org/10.1094/PDIS.2002.86.12.1383 Mamidi, S., Rossi, M., Annam, D., Moghaddam, S., Lee, R., Papa, R., and McClean, P. (2011). Investigation of the domestication of common bean (Phaseolus vulgaris) using multilocus sequence data. Functional Plant Biol 38, 953–967. doi: https://doi.org/10.1071/ FP11124 Martin, G. B. and Adams, M. W. (1987). Landraces of Phaseolus vulgaris (Fabaceae) in northern Malawi. 1. Regional variation. Econ. Bot 41, 190–203. doi: https://doi.org/10.1007/BF02858965 Mart́ınez-Castillo, J., Andueza-Noh, R., and Chacón- Sánchez, M. I. (2015). Recent advances in the study of the evolution of Lima bean (Phaseolus lunatus L.) in Mexico. In Phaseolus lunatus: diversity, growth and production, ed. de Araujo, A. S. F., de Almeida Lopes, A. C., and Gomes, R. L. F., (New York, USA: Nova Science Publishers, Inc), 43-62. McCouch, S. R., McNally, K. L., Wang, W., and Sackville- Hamilton, R. (2012). Genomics of gene banks: a case study in rice. Amer. J. Bot 99, 407–423. doi: https://doi.org/10.3732/ajb.1100385 Mej́ıa-Jiménez, A., Muñoz, C., Jacobsen, H. J., Roca, W. M., and Singh, S. P. (1994). Interspecific hybridization between common bean and tepary bean: increased hybrid embryo growth, fertility, and efficiency of hybridization through recurrent and congruity backcrossing. Theor. Appl. Genet 88, 324– 331. doi: https://doi.org/10.1007/BF00223640 Melotto, M. and Kelly, J. D. (2000). An allelic series at the Co-1 locus conditioning resistance to anthracnose in common bean of Andean origin. Euphytica 116, 143–149. doi: https://doi.org/10. 1023/A:1004005001049 Michaels, T. E., Smith, T. H., Larsen, J., Beattie, A. D., and Pauls, K. P. (2006). OAC Rex common bean. Can. J. Plant Sci 86, 733–736. doi: https://doi.org/ 10.4141/P05-128 Miklas, P. N., Coyne, D. P., Grafton, K. F., Mutlu, N., Reiser, J., Lindgren, D. T., and Singh, S. P. (2003). A major QTL for common bacterial blight resistance derives from the common bean Great Northern landrace cultivar Montana No. 5. Euphytica 131, 137– 146. doi: https://doi.org/10.1023/A:1023064814531 Miklas, P. N., Kelly, J. D., Beebe, S. E., and Blair, M. W. (2006). Common bean breeding for resistance against biotic and abiotic stresses: from classical to MAS breeding. Euphytica 147, 105–131. doi: https://doi. org/10.1007/978-94-015-9211-6\ 11 Mina-Vargas, A. M., Mckeown, P. C., Flanagan, N. S., Debouck, D. G., Kilian, A., Hodkinson, T. R., and Spillane, C. (2016). Origin of year-long bean (Phaseolus dumosus Macfady., Fabaceae) from reticulated hybridization events between multiple Phaseolus species. Ann. Bot 118, 957–969. doi: https: //doi.org/10.1093/aob/mcw138 Moghaddam, S. M., Mamidi, S., Osorno, J. M., Lee, R., Brick, M., Kelly, J., Miklas, P., Urrea, C., Song, Q., Cregan, P., Grimwood, J., Schmutz, J., and McClean, P. E. (2016). Genome-wide association study identifies candidate loci underlying agronomic traits in a Middle American diversity panel of common bean. The Plant Genome 9, 1–21. doi: https://doi.org/ 10.3835/plantgenome2016.02.0012 Moghaddam, S. M., Oladzad, A., Koh, C., Ramsay, L., Hart, J. P., Mamidi, S., Hoopes, G., Sreedasyam, A., Wiersma, A., Zhao, D., Grimwood, J., Hamilton, J. P., Jenkins, J., Vaillancourt, B., Wood, J. C., Schmutz, J., Kagale, S., Porch, T., Bett, K. E., Buell, C. R., and Mcclean, P. E. (2021). The tepary bean genome provides insight into evolution and domestication under heat stress. Nature Communic 12, 1–14. doi: https://doi.org/10.1038/s41467-021-22858-x Montoya, C. A., Leterme, P., Victoria, N. F., Toro, O., Souffrant, W. B., Beebe, S., and Lallès, J. P. (2008). Susceptibility of phaseolin to in vitro proteolysis is highly variable across common bean varieties (Phaseolus vulgaris). J. Agric. Food Chem 56, 2183– 2191. doi: https://doi.org/10.1021/jf072576e Motta-Aldana, J. R., Serrano-Serrano, M. L., Hernández- Torres, J., Castillo-Villamizar, G., Debouck, D. G., and Chacón-Sánchez, M. I. (2010). Multiple origins of Lima bean landraces in the Americas: evidence from chloroplast and nuclear DNA polymorphisms. Crop Sci 50, 1773–1787. doi: https://doi.org/10.2135/ cropsci2009.12.0706 Myers, J. R. and Baggett, J. R. (1999). Improvement of snap bean. In Common bean improvement in the twenty-first century, ed. Singh, S. P., (Dordrecht, The Netherlands: Kluwer Academic Publishers), 289-329. National Research Council (1989). Lost crops of the Incas: little-known plants of the Andes with promise for worldwide cultivation (Washington, D.C., USA: National Academy Press), 415p. doi: https://doi.org/ 10.17226/1398 http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=9218230 http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=9218230 https://doi.org/10.2135/cropsci1992.0011183X003200030012x https://doi.org/10.2135/cropsci1992.0011183X003200030012x https://doi.org/10.1094/PDIS.2002.86.12.1383 https://doi.org/10.1094/PDIS.2002.86.12.1383 https://doi.org/10.1094/PDIS.2002.86.12.1383 https://doi.org/10.1071/FP11124 https://doi.org/10.1071/FP11124 https://doi.org/10.1007/BF02858965 https://doi.org/10.3732/ajb.1100385 https://doi.org/10.1007/BF00223640 https://doi.org/10.1023/A:1004005001049 https://doi.org/10.1023/A:1004005001049 https://doi.org/10.4141/P05-128 https://doi.org/10.4141/P05-128 https://doi.org/10.1023/A:1023064814531 https://doi.org/10.1007/978-94-015-9211-6\_11 https://doi.org/10.1007/978-94-015-9211-6\_11 https://doi.org/10.1093/aob/mcw138 https://doi.org/10.1093/aob/mcw138 https://doi.org/10.3835/plantgenome2016.02.0012 https://doi.org/10.3835/plantgenome2016.02.0012 https://doi.org/10.1038/s41467-021-22858-x https://doi.org/10.1021/jf072576e https://doi.org/10.2135/cropsci2009.12.0706 https://doi.org/10.2135/cropsci2009.12.0706 https://doi.org/10.17226/1398 https://doi.org/10.17226/1398 40 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Navabi, A., Burt, A., Rupert, T., Smith, T. H., Gillard, C., and Pauls, K. P. (2012). Contribution of genetic improvement in yield increase and disease resistance in Navy beans released in central Canada since 1930’s. Annu. Rept. Bean Improvem. Coop. (USA) 55, 113–114. Nienhuis, J. and Singh, S. P. (1986). Combining ability analyses and relationships among yield, yield components, and architectural traits in dry bean. Crop Sci 26, 21–27. doi: https://doi.org/10.2135/ cropsci1986.0011183X002600010005x OECD (2015). Consensus document on compositional considerations for new varieties of common bean (Phaseolus vulgaris L.): key food and feed nutrients, anti-nutrients and other constituents. volume 27 of Series on the Safety of Novel Foods and Feeds. (Paris, France) 1-49. url: https://www.oecd.org/ officialdocuments/publicdisplaydocumentpdf/?cote= env/jm/mono(2015)49&doclanguage=en Osborn, T. C., Alexander, D. C., Sun, S. S. M., Cardona, C., and Bliss, F. A. (1988). Insecticidal activity and lectin homology of arcelin seed protein. Science 240, 207–210. doi: https://doi.org/10.1126/science.240. 4849.207 Otálora, J. M., Ligarreto, G. A., and Romero, A. (2006). Comportamiento de fŕıjol común (Phaseolus vulgaris L.) tipo reventón por caracteŕısticas agronómicas y de calidad de grano. Agron. Colomb 24, 7–16. (in Spanish). Pallottini, L., Garcia, E., Kami, J., Barcaccia, G., and Gepts, P. (2004). The genetic anatomy of a patented yellow bean. Crop Sci 44, 968–977. doi: https://doi. org/10.2135/cropsci2004.9680 Parker, T. A., Terán, B. M. Y., Palkovic, J. C., Jernstedt, A., Gepts, J., and P (2020). Pod indehiscence is a domestication and aridity resilience trait in common bean. New Phytol 225, 558–570. doi: https://doi.org/ 10.1111/nph.16164 Pastor-Corrales, M. A., Jara, C., and Singh, S. P. (1998). Pathogenic variation in, sources of, and breeding for resistance to Phaeoisariopsis griseola causing angular leaf spot in common bean. Euphytica 103, 161–171. doi: https://doi.org/10.1023/A:1018350826591 Piperno, D. L. and Dillehay, T. D. (2008). Starch grains on human teeth reveal early broad crop diet in northern Peru. Proc. Natl. Acad. Sci. USA 105 19622-19627. doi: https://doi.org/10.1073/ pnas.0808752105 Porch, T. G., Beaver, J. S., Debouck, D. G., Jackson, S., Kelly, J. D., and Dempewolf, H. (2013). Use of wild relatives and closely related species to adapt common bean to climate change. Agronomy 3, 433–461. doi: https://doi.org/10.3390/agronomy3020433 Rachie, K. O. (1973). Relative agronomic merits of various food legumes for the lowland tropics. In Potentials of field beans and other food legumes in Latin America, ed. Wall, D., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 123-139. Ramı́rez-Villegas, J., Khoury, C., Achicanoy, H. A., Mendez, A. C., Diaz, M. V., Sosa, C. C., Debouck, D. G., Kehel, Z., and Guarino, L. (2020). A gap analysis modelling framework to prioritize collecting for ex situ conservation of crop landraces. Diversity & Distributions 26, 730–742. doi: https://doi.org/10. 1111/ddi.13046 Ramı́rez-Villegas, J., Khoury, C., Jarvis, A., Debouck, D. G., and Guarino, L. (2010). A gap analysis methodology for collecting crop genepools: a case study with Phaseolus beans. PLoS ONE Biology 5, 1– 18. Rao, I., Beebe, S., Polańıa, J., Ricaurte, J., Cajiao, C., Garćıa, R., and Rivera, M. (2013). Can tepary bean be a model for improvement of drought resistance in common bean? Afric Crop Sci. J 21, 265–281. url: https://www.ajol.info/index.php/acsj/ article/view/95291 Rao, I. M. (2001). Role of physiology in improving crop adaptation to abiotic stresses in the tropics: the case of common bean and tropical forages. In Handbook of plant and crop physiology, ed. Pessarakli, M., (New York, USA: Marcel Dekker, Inc). 2 edition. Rendón-Anaya, M., Montero-Vargas, J. M., Saburido- Alvarez, S., Vlasova, A., Capella-Gutiérrez, S., Ordaz- Ortiz, J. J., Aguilar, O. M., Vianello-Brondani, R. P., Santalla, M., Delaye, L., Gabaldón, T., Gepts, P., Winkler, R., Guigó, R., Salinas, A. D., and Herrera- Estrella, A. (2017). Genomic history of the origin and domestication of common bean unveils its closest sister species. Genome Biol 18, 1–17. doi: https://doi. org/10.1186/s13059-017-1190-6 Salcedo-Castaño, J., Araya-Villalobos, R., Castañeda- Alvarez, N., Toro-Chica, O., and Debouck, D. G. (2011). Phaseolus hygrophilus (Leguminosae- Papilionoideae), a new wild bean species from the wet forests of Costa Rica, with notes about section Bre- vilegumeni. J. Bot. Res. Inst. Texas 5, 53–65. url: https: //journals.brit.org/jbrit/article/download/953/871/ Sanders, J. H. and Schwartz, H. F. (1980). La producción de fŕıjol y limitaciones impuestas por las plagas en América Latina. In Problemas de producción del fŕıjol: enfermedades, insectos, limitaciones edáficas y climáticas de Phaseolus vulgaris, ed. Schwartz, H. F. and Gálvez, G. E., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 1-14. Schaafsma, A. W., Cardona, C., Kornegay, J. L., Wylde, A. M., and Michaels, T. E. (1998). Resistance of common bean lines to the potato leafhopper (Homoptera: Cicadellidae). J. Econ. Entomol 91, 981– 986. doi: https://doi.org/10.1093/jee/91.4.981 Schinkel, C. and Gepts, P. (1988). Phaseolin diversity in the tepary bean Phaseolus acutifolius A. Gray. Plant Breeding 101, 292–301. doi: https://doi.org/10. 1111/j.1439-0523.1988.tb00301.x Schmit, V. and Baudoin, J. P. (1992). Screening for resistance to Ascochyta blight in populations of Phaseolus coccineus L. and P. polyanthus Greenman. Field Crops Res 30, 155–165. doi: https://doi.org/10. 1016/0378-4290(92)90064-G https://doi.org/10.2135/cropsci1986.0011183X002600010005x https://doi.org/10.2135/cropsci1986.0011183X002600010005x https://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2015)49&doclanguage=en https://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2015)49&doclanguage=en https://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2015)49&doclanguage=en https://doi.org/10.1126/science.240.4849.207 https://doi.org/10.1126/science.240.4849.207 https://doi.org/10.2135/cropsci2004.9680 https://doi.org/10.2135/cropsci2004.9680 https://doi.org/10.1111/nph.16164 https://doi.org/10.1111/nph.16164 https://doi.org/10.1023/A:1018350826591 https://doi.org/10.1073/pnas.0808752105 https://doi.org/10.1073/pnas.0808752105 https://doi.org/10.3390/agronomy3020433 https://doi.org/10.1111/ddi.13046 https://doi.org/10.1111/ddi.13046 https://www.ajol.info/index.php/acsj/article/view/95291 https://www.ajol.info/index.php/acsj/article/view/95291 https://doi.org/10.1186/s13059-017-1190-6 https://doi.org/10.1186/s13059-017-1190-6 https://journals.brit.org/jbrit/article/download/953/871/ https://journals.brit.org/jbrit/article/download/953/871/ https://doi.org/10.1093/jee/91.4.981 https://doi.org/10.1111/j.1439-0523.1988.tb00301.x https://doi.org/10.1111/j.1439-0523.1988.tb00301.x https://doi.org/10.1016/0378-4290(92)90064-G https://doi.org/10.1016/0378-4290(92)90064-G Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 41 Schmit, V. and Debouck, D. G. (1991). Observations on the origin of Phaseolus polyanthus Greenman. Econ. Bot 45, 345–364. doi: https://doi.org/10.1007/ BF02887077 Schmit, V., Debouck, D. G., and Baudoin, J. P. (1996). Biogeographical and molecular observations on Phaseolus glabellus (Fabaceae, Phaseolinae) and its taxonomic status. Taxon 45, 493–501. doi: https: //doi.org/10.2307/1224141 Schmutz, J., Mcclean, P. E., Mamidi, S., Wu, G. A., Cannon, S. B., Grimwood, J., Jenkins, J., Shu, S., Song, Q., Chavarro, C., Torres-Torres, M., Geffroy, V., Moghaddam, S. M., Gao, D., Abernathy, B., Barry, K., Blair, M., Brick, M. A., Chovatia, M., ..., and Jackson, S. A. (2014). A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genet 46, 707–713. doi: https://doi.org/10. 1038/ng.3008 Schwartz, H. F. (1989). Halo blight. In Bean production problems in the tropics, ed. Schwartz, H. F. and Pastor- Corrales, M. A., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 285-301. 2 edition. Schwartz, H. F., Pastor-Corrales, M. A., and Singh, S. P. (1982). New sources of resistance to anthracnose and angular leaf spot of beans (Phaseolus vulgaris L.). Euphytica 31, 741–754. doi: https://doi.org/10.1007/ BF00039213 Schwartz, H. F. and Singh, S. P. (2013). Breeding common bean for resistance to white mold: a review. Crop Sci 53, 1832–1844. doi: https://doi.org/10. 2135/cropsci2013.02.0081 Sellitti, S., Vaiknoras, K., Smale, M., Jamora, N., Andrade, R., Wenzl, P., and Labarta, R. (2020). The contribution of the CIAT genebank to the development of iron-biofortified bean varieties and well-being of farm households in Rwanda. Food Security 12, 975–991. doi: https://doi.org/10.1007/s12571-020- 01038-7 Silbernagel, M. J., Janssen, W., Davis, J. H. C., and Oca, G. M. D. (1991). Snap bean production in the tropics: implications for genetic improvement. In Common beans: research for crop improvement, ed. van Schoonhoven, A. and Voysest, O., (Wallingford, United Kingdom: CABI), 835-862. Singh, S. P. (1992). Common bean improvement in the tropics. Plant Breeding Reviews 10, 199–269. doi: https://doi.org/10.1002/9780470650011 Singh, S. P. (1999). Production and utilization. In Common bean improvement in the twenty-first century, ed. Singh, S. P., (Dordrecht, The Netherlands: Kluwer Academic Publishers), 1-24. Singh, S. P. (2001). Broadening the genetic base of com- mon bean cultivars: a review. Crop Sci 41, 1659–1675. doi: https://doi.org/10.2135/cropsci2001.1659 Singh, S. P. (2007). Drought resistance in the race Durango dry bean landraces and cultivars. Agron. J 99, 1219–1225. doi: https://doi.org/10. 2134/agronj2006.0301 Singh, S. P., Gepts, P., and Debouck, D. G. (1991a). Races of common bean (Phaseolus vulgaris, Fabaceae). Econ. Bot 45, 379–396. doi: https://doi.org/10.1007/BF02887079 Singh, S. P. and Gutiérrez, J. A. (1984). Geographical distribution of the DL1 and DL2 genes causing hybrid dwarfism in Phaseolus vulgaris L., their association with seed size, and their significance to breeding. Euphytica 33, 337–345. doi: https://doi.org/10.1007/ BF02887079 Singh, S. P. and Molina, A. (1996). Inheritance of crippled trifoliolate leaves occurring in interracial crosses of common bean and its relationship with hybrid dwarfism. J. Hered 87, 464–469. doi: https: //doi.org/10.1093/oxfordjournals.jhered.a023039 Singh, S. P., Molina, A., Urrea, C. A., and Gutiérrez, J. A. (1993). Use of interracial hybridization in breeding the race Durango common bean. Can. J. Plant Sci 73, 785–793. doi: https://doi.org/10.4141/cjps93-101 Singh, S. P., Morales, F. J., Miklas, P. N., and Terán, H. (2000). Selection for Bean Golden Mosaic resistance in intra- and interracial bean populations. Crop Sci 40, 1565–1572. doi: https://doi.org/10.2135/ cropsci2000.4061565x Singh, S. P. and Muñoz, C. G. (1999). Resis- tance to common bacterial blight among Phase- olus species and common bean improvement. Crop Sci 39, 80–89. doi: https://doi.org/10.2135/ cropsci1999.0011183X003900010013x Singh, S. P., Nodari, R., and Gepts, P. (1991b). Genetic diversity in cultivated common bean: 1. Allozymes. Crop Sci 31, 19–29. doi: https://doi.org/10.2135/ cropsci1991.0011183X003100010004x Singh, S. P. and Schwartz, H. F. (2010). Breeding common bean for resistance to diseases: a review. Crop Sci 50, 2199–2223. doi: https://doi.org/10. 1007/s10681-006-4600-5 Singh, S. P., Terán, H., Schwartz, H. F., Otto, K., Debouck, D. G., Roca, W., and Lema, M. (2013). White mold-resistant, interspecific common bean breeding line VRW32 derived from Phaseolus costaricensis. J. Plant Registr 7, 95–99. doi: https://doi.org/10.3198/ jpr2012.02.0131crg Singh, S. P., Terán, H., Schwartz, H. F., Otto, K., and Lema, M. (2009). Introgressing white mold resistance from Phaseolus species of the secondary gene pool into common bean. Crop Sci 49, 1629–1637. doi: https://doi.org/10.2135/cropsci2008.08.0508 Singh, S. P. and Urrea, C. A. (1995). Inter- and intraracial hybridization and selection for seed yield in early generations of common bean, Phaseolus vulgaris L. Euphytica 81, 131–137. doi: https://doi.org/10. 1007/BF00025424 Sonnante, G., Stockton, T., Nodari, R. O., Becerra- Velásquez, V. L., and Gepts, P. (1994). Evolution of genetic diversity during the domestication of common bean (Phaseolus vulgaris L.). Theor. Appl. Genet 89, 629–635. doi: https://doi.org/10.1007/BF00222458 https://doi.org/10.1007/BF02887077 https://doi.org/10.1007/BF02887077 https://doi.org/10.2307/1224141 https://doi.org/10.2307/1224141 https://doi.org/10.1038/ng.3008 https://doi.org/10.1038/ng.3008 https://doi.org/10.1007/BF00039213 https://doi.org/10.1007/BF00039213 https://doi.org/10.2135/cropsci2013.02.0081 https://doi.org/10.2135/cropsci2013.02.0081 https://doi.org/10.1007/s12571-020-01038-7 https://doi.org/10.1007/s12571-020-01038-7 https://doi.org/10.1002/9780470650011 https://doi.org/10.2135/cropsci2001.1659 https://doi.org/10.2134/agronj2006.0301 https://doi.org/10.2134/agronj2006.0301 https://doi.org/10.1007/BF02887079 https://doi.org/10.1007/BF02887079 https://doi.org/10.1007/BF02887079 https://doi.org/10.1093/oxfordjournals.jhered.a023039 https://doi.org/10.1093/oxfordjournals.jhered.a023039 https://doi.org/10.4141/cjps93-101 https://doi.org/10.2135/cropsci2000.4061565x https://doi.org/10.2135/cropsci2000.4061565x https://doi.org/10.2135/cropsci1999.0011183X003900010013x https://doi.org/10.2135/cropsci1999.0011183X003900010013x https://doi.org/10.2135/cropsci1991.0011183X003100010004x https://doi.org/10.2135/cropsci1991.0011183X003100010004x https://doi.org/10.1007/s10681-006-4600-5 https://doi.org/10.1007/s10681-006-4600-5 https://doi.org/10.3198/jpr2012.02.0131crg https://doi.org/10.3198/jpr2012.02.0131crg https://doi.org/10.2135/cropsci2008.08.0508 https://doi.org/10.1007/BF00025424 https://doi.org/10.1007/BF00025424 https://doi.org/10.1007/BF00222458 42 Debouck et al Genetic Resources (2021), 2 (4), 21–43 Stavely, J. R. (1984). Pathogenic specialization in Uromyces phaseoli in the United States and rust resistance in beans. Plant Dis 68, 95–99. doi: https: //doi.org/10.1094/PD-68-95 Stavely, J. R. and Pastor-Corrales, M. A. (1989). Rust. In Bean production problems in the tropics, ed. Schwartz, H. F. and Pastor-Corrales, M. A., (Cali, Colombia: Centro Internacional de Agricultura Tropical), 159- 194. 2 edition. Suárez, J. C., Polańıa, J. A., Contreras, A. T., Rodŕıguez, L., Machado, L., Ordoñez, C., Beebe, S., and Rao, I. M. (2020). Adaptation of common bean lines to high temperature conditions: genotypic differences in phenological and agronomic performance. Euphytica 216, 28–47. doi: https://doi.org/10.1007/s10681- 020-2565-4 Tanksley, S. D., Grandillo, S., Fulton, T. M., Zamir, D., Eshed, Y., Petiard, V., Lopez, J., and Beck-Bunn, T. (1996). Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor. Appl. Genet 92, 213–224. doi: https://doi.org/10.1007/BF00223378 Taylor, J. D., Teverson, D. M., and Davis, J. H. C. (1996). Sources of resistance to Pseudomonas syringae pv. phaseolicola races in Phaseolus vulgaris. Plant Pathol 45, 479–485. doi: https://doi.org/10.1046/j.1365- 3059.1996.d01-148.x Thomas, C. V., Manshardt, R. M., and Waines, J. G. (1983). Teparies as a source of useful traits for improving common beans. Desert Plants 5, 43–48. url: http://hdl.handle.net/10150/552200 Thung, M. (1991). Bean agronomy in monoculture. In Common beans: research for crop improvement, ed. van Schoonhoven, A. and Voysest, O., (Wallingford, UK: CABI), 737-834. Tohme, J., Jones, P., Beebe, S., and Iwanaga, M. (1995a). The combined use of agroecological and characterization data to establish the CIAT Phaseolus vulgaris core collection. In Core collection of plant genetic resources, ed. Hodgkin, T., Brown, A. H. D., van Hintum, T. J. L., and Morales, E. A. V., (Chichester, UK: John Wiley and Sons), 95-107. Tohme, J., Toro-Chica, O., Vargas, J., and Debouck, D. G. (1995b). Variability in Andean nuña common bean (Phaseolus vulgaris, Fabaceae). Econ. Bot 49, 78–95. doi: https://doi.org/10.1007/BF02862280 Urrea, C. A. and Harveson, R. M. (2014). Identification of sources of bacterial wilt resistance in common bean (Phaseolus vulgaris). Plant Dis 98, 973–976. doi: http://dx.doi.org/10.1094/PDIS-04-13-0391-RE van Beem, J., Kornegay, J., and Lareo, L. (1992). Nutri- tive value of the nuña popping bean. Econ. Bot 46, 164–170. doi: https://doi.org/10.1007/BF02930631 van Hintum, T., Menting, F., and van Strien, E. (2011). Quality indicators for passport data in ex situ genebanks. Plant Genet. Resour. Character. Utiliz 9, 478–485. doi: https://doi.org/10.1017/ S1479262111000682 van Schoonhoven, A. and Cardona, C. (1982). Low levels of resistance to the Mexican bean weevil in dry beans. J. Econ. Entomol 75, 567–569. doi: https: //doi.org/10.1093/jee/75.4.567 van Schoonhoven, A., Cardona, C., and Valor, J. (1983). Resistance to the bean weevil and the Mexican bean weevil (Coleoptera: Bruchidae) in non cultivated common bean accessions. J. Econ. Entomol 76, 1255– 1259. doi: https://doi.org/10.1093/jee/76.6.1255 van Treuren, R. and van Hintum, T. J. L. (2014). Next-generation genebanking: plant genetic resources management and utilization in the sequencing era. Plant Genet. Resour. Charact. Utiliz 12, 298–307. doi: https://doi.org/10.1017/S1479262114000082 Vieira, C. (1973). Plant introduction and germplasm of Phaseolus vulgaris and other food legumes. In Wall, D., Potentials of field beans and other food legumes in Latin America, Centro Internacional de Agricultura Tropical, 239-252. Vlasova, A., Capella-Gutiérrez, S., Rendón-Anaya, M., Hernández-Oñate, M., Minoche, A. E., Erb, I., Câmara, F., Prieto-Barja, P., Corvelo, A., Sanseverino, W., Westergaard, G., Dohm, J. C., Pappas, G. J., Saburido- Alvarez, S., Kedra, D., Gonzalez, I., Cozzuto, L., Gómez-Garrido, J., Aguilar-Morón, M. A., ..., and Guigó, R. (2016). Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biol 17, 1–18. doi: https://doi.org/10.1186/s13059-016-0883-6 Voysest, O. and Dessert, M. (1991). Bean cultivars: classes and commercial seed types. In Common beans: research for crop improvement, ed. van Schoonhoven, A. and Voysest, O., (Wallingford, UK: CABI), 119-162. Voysest-Voysest, O. (1983). Variedades de frijol en América Latina y su origen (Cali, Colombia: Centro Internacional de Agricultura Tropical), 87p, (in Spanish). Voysest-Voysest, O. (2000). Mejoramiento genético del frijol (Phaseolus vulgaris L.) - Legado de variedades de América Latina 1930-1999 (Cali, Colombia: Centro Internacional de Agricultura Tropical), 195p. White, J. W. and Laing, D. R. (1989). Photope- riod response of flowering in diverse genotypes of common bean (Phaseolus vulgaris). Field Crops Res 22, 113–128. doi: https://doi.org/10.1016/0378- 4290(89)90062-2 Williams, J. W., Jackson, S. T., and Kutzbach, J. E. (2007). Projected distributions of novel and disappearing climates by 2100 AD. Proc. Natl. Acad. Sci. USA 104, 5738–5742. doi: https://doi.org/10. 1073/pnas.0606292104 Xu, H., Zhang, L., Zhang, K., and Ran, Y. (2020). Progresses, challenges, and prospects of genome editing in soybean (Glycine max). Front. Plant Sci 11, 1–19. doi: https://doi.org/10.3389/fpls.2020.571138 Young, R. A. and Kelly, J. D. (1996). Characterization of the genetic resistance to Colletotrichum lindemuthi- anum in common bean differential cultivars. Plant https://doi.org/10.1094/PD-68-95 https://doi.org/10.1094/PD-68-95 https://doi.org/10.1007/s10681-020-2565-4 https://doi.org/10.1007/s10681-020-2565-4 https://doi.org/10.1007/BF00223378 https://doi.org/10.1046/j.1365-3059.1996.d01-148.x https://doi.org/10.1046/j.1365-3059.1996.d01-148.x http://hdl.handle.net/10150/552200 https://doi.org/10.1007/BF02862280 http://dx.doi.org/10.1094/PDIS-04-13-0391-RE https://doi.org/10.1007/BF02930631 https://doi.org/10.1017/S1479262111000682 https://doi.org/10.1017/S1479262111000682 https://doi.org/10.1093/jee/75.4.567 https://doi.org/10.1093/jee/75.4.567 https://doi.org/10.1093/jee/76.6.1255 https://doi.org/10.1017/S1479262114000082 https://doi.org/10.1186/s13059-016-0883-6 https://doi.org/10.1016/0378-4290(89)90062-2 https://doi.org/10.1016/0378-4290(89)90062-2 https://doi.org/10.1073/pnas.0606292104 https://doi.org/10.1073/pnas.0606292104 https://doi.org/10.3389/fpls.2020.571138 Genetic Resources (2021), 2 (4), 21–43 Impact of a bean collection 43 Dis 80, 650–654. doi: https://doi.org/10.1094/PD- 80-0650 Yuste-Lisbona, F. J., Santalla, M., Capel, C., Garćıa- Alcázar, M., Fuente, M. D. L., Capel, J., Ron, A. M. D., and Lozano, R. (2012). Marker-based linkage map of Andean common bean (Phaseolus vulgaris L.) and mapping of QTLs underlying popping ability traits. BMC Plant Biology 12, 1–16. doi: https://doi.org/10. 1186/1471-2229-12-136 Zambre, M., Goossens, A., Cardona, C., Montagu, M. V., Terryn, N., and Angenon, G. (2005). A reproducible genetic transformation system for cultivated Phase- olus acutifolius (tepary bean) and its use to assess the role of arcelins in resistance to the Mexican bean weevil. Theor. Appl. Genet 110, 914–924. doi: https: //doi.org/10.1007/s00122-004-1910-7 Zapata, M., Freytag, G. F., and Wilkinson, R. E. (1985). Evaluation for bacterial blight resistance in beans. Phytopathology 75, 1032–1039. doi: https://doi.org/ 10.1094/Phyto-75-1032 Zaugg, I., Magni, C., Panzeri, D., Daminati, M. G., Bollini, R., Benrey, B., Bacher, S., and Sparvoli, F. (2013). QUES, a new Phaseolus vulgaris genotype resistant to common bean weevils, contains the arcelin-8 allele coding for new lectin-related variants. Theor. Appl. Genet 126, 647–661. doi: https://doi.org/ 10.1007/s00122-012-2008-2 Zaumeyer, W. J. and Thomas, H. R. (1957). A monographic study of bean diseases and methods for their control volume 868 of Technical Bulletin. (Washington, D.C.) 255p. doi: https://doi.org/10. 22004/ag.econ.169625 Zeven, A. C. (1997). The introduction of the common bean (Phaseolus vulgaris L.) into Western Europe and the phenotypic variation of dry beans collected in the Netherlands in 1946. Euphytica 94, 319–328. doi: https://doi.org/10.1023/A:1002940220241 Zhao, C., Zhang, Y., Du, J., Duo, X., Wen, W., Gu, S., Wang, J., and Fan, J. (2019). Crop phenomics: current status and perspectives. Front. Plant Sci 10, 1–16. doi: https://doi.org/10.3389/fpls.2019.00714 Zimmerer, K. S. (1992). Biological diversity and local development. Mountain Res. Dev 12, 47–61. doi: https://doi.org/10.2307/3673747 https://doi.org/10.1094/PD-80-0650 https://doi.org/10.1094/PD-80-0650 https://doi.org/10.1186/1471-2229-12-136 https://doi.org/10.1186/1471-2229-12-136 https://doi.org/10.1007/s00122-004-1910-7 https://doi.org/10.1007/s00122-004-1910-7 https://doi.org/10.1094/Phyto-75-1032 https://doi.org/10.1094/Phyto-75-1032 https://doi.org/10.1007/s00122-012-2008-2 https://doi.org/10.1007/s00122-012-2008-2 https://doi.org/10.22004/ag.econ.169625 https://doi.org/10.22004/ag.econ.169625 https://doi.org/10.1023/A:1002940220241 https://doi.org/10.3389/fpls.2019.00714 https://doi.org/10.2307/3673747 The purpose for establishing a collection of genetic resources at CIAT How the Phaseolus collection was assembled The diversity in the bean collection and its use Distribution of the bean collection Impact of the bean genetic resources collection The other impact: the contribution to knowledge Knowledge often overlooked, although associated with crop germplasm for millennia Serving the breeders community and beyond Discussion Concluding remarks Author contributions Conflict of interest statement