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Review

Ex Situ Conservation of Plant Genetic Resources: An Overview of Chickpea (Cicer arietinum L.) and Lentil (Lens culinaris Medik.) Worldwide Collections

by
Angela Rosa Piergiovanni
Istituto Bioscienze Biorisorse, Consiglio Nazionale delle Ricerche (CNR-IBBR), via Amendola 165/a, 70126 Bari, Italy
Diversity 2022, 14(11), 941; https://doi.org/10.3390/d14110941
Submission received: 5 October 2022 / Revised: 28 October 2022 / Accepted: 30 October 2022 / Published: 2 November 2022
(This article belongs to the Section Biodiversity Conservation)
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Abstract

:
The collection and conservation of chickpea and lentil germplasm has great importance due to their role as a staple food for millions of people. Nowadays, the largest chickpea collection, 41.2% of the total accessions, is held by ICRISAT, while the main lentil collection is stored by ICARDA. The main fraction of both collections is constituted by Indian landraces. In recent decades, several efforts have been made to integrate all genebanks into a global conservation system of plant genetic resources. The release of informatics platforms allowed the creation of virtual genebanks, which are powerful tools routinely consulted by germplasm users. The information available for the chickpea and lentil accessions included in the Genesys and EURISCO platforms has been taken into consideration in this mini review. This review also presents and discusses the strengths and drawbacks of the worldwide collections of both species emerging from the analysis of data obtained by enquiring these two platforms. The availability of core collections is of great utility for germplasm users, while the lack of origin and biological status for a significant fraction of accessions are the main drawbacks. Moreover, this review highlights the necessity of sharing as much as possible of the non-omic and omic characterization data.

Graphical Abstract

1. Introduction

Chickpea and lentil are, together with cereals, among the founder crops of agriculture [1,2]. Domesticated in the Near East about ten millennia ago, these species spread towards the west side of the Mediterranean basin and central Asia in a relatively short time. Successively, their cultivation started in Ethiopia and neighbouring regions, and only some centuries ago were they introduced in America and Australia. From the beginning of their cultivation to the present, chickpea and lentil have significantly contributed to human nutrition, being valuable sources of proteins, minerals and vitamins. Over time, small-scale farmers selected a myriad of landraces, choosing from the annual harvest the best seeds for the subsequent sowing. Farmer-to-farmer seed flow was mainly based on local social networks or family relationships. These empiric processes progressively enhanced the adaptation of each crop to different environments of cultivation, increasing genetic diversity, yield, stress resistance and seed nutritional quality [3]. Nowadays, chickpea and lentil are among the most cultivated legumes, with a worldwide production of 15,083,871 and 6,537,581 tons in 2020, respectively (FAOSTAT http://faostat.fao.org/default.aspx, accessed on 1 August 2022). Starting from the 1950s, the cultivation has progressively declined in European Mediterranean countries, increasing elsewhere such as in Canada [4]. The relocation of cultivation regions prompted the new producers towards the extensive cultivation of improved cultivars, which were realised in recent decades and better adapted to the new pedo-climatic conditions. This has caused the abandonment and consequent disappearance of an unknown number of landraces. As for other species [5], the assessment of genetic erosion experienced by chickpea and lentil cannot be quantified exactly due to the lack of inventories of materials grown more than a century ago. In fact, the systematic collection of crop germplasm started in the first decades of the 20th century, and only after the beginning of this activity were the first genebanks created. Nowadays, a very low number of chickpea and lentil landraces are still cultivated by some local communities, mainly in the marginal areas (on farm conservation) of some countries, such as Algeria, Italy, Spain and Greece [6,7,8]. Based on these considerations, it can be inferred that germplasm collections retain the main fraction of the early genetic variation of chickpea and lentil.

Scope and Focus of This Review

Researchers and breeders currently use cooperative platforms for the management of seeds and information pertaining to germplasm accessions held by the worldwide genebanks network. However, the sharing and utilisation of ex situ collections is directly related to the quality and quantity of available information [9]. Only in recent times has the creation of global infrastructures for information exchange allowed the creation and sharing of big databases. The sharing of canonical passport data together with additional information for each accession is great progress toward a more sustainable use of chickpea and lentil germplasm [10].
This paper provides a review of the present status of chickpea and lentil worldwide collections, as obtained by querying the most important online platforms, Genesys (Virtual Genebank of Plant Genetic Resources for Food Agriculture, https://www.genesys-pgr.org/, accessed on 1 August 2022) and EURISCO (European Search Catalogue for Plant Genetic Resources, https://eurisco.ipk-gatersleben.de/apex/eurisco_ws/r/eurisco/home, accessed on 1 August 2022). These two legume species are the object of the project “Legumes in biodiversity based farming systems in Mediterranean basin”, which aims to identify promising genetic resources for Mediterranean climate within the stored germplasm. The size and characteristics of chickpea and lentil collections held in the worldwide genebank network and the related information available online are analysed. The contribution that omic studies have made to improve the knowledge of stored collections is concisely presented.

2. Assembly and Management of Chickpea and Lentil Collections

In the second half of the 20th century, the genebanks, progressively founded around the world, started to create their own collections through collection missions or seed sample exchange with other institutions [11]. In 2008, the size of chickpea and lentil collections held by the genebanks jointed to the CGIAR (Consultative Group for International Agricultural Research) network was considerable, being constituted by 41.096 and 18.114 accessions for chickpea and lentil, respectively. At that time, the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT) held 41.2% of chickpea accessions (Table 1). The assemblage of this collection started in 1972 with the institute foundation, and chickpea was one of the five assigned mandate crops to ICRISAT [12]. As concerns lentil, in 2008, the International Centre for Agricultural Research in the Dry Areas (ICARDA) maintained 55.8% of the accessions in their own facilities (Table 1).
Based on international directives, ICRISAT and ICARDA continue to provide global leadership for the conservation of chickpea and lentil germplasm. Over time, the size of both collections has increased, and presently, the two institutes conserve in their facilities 33.9% of chickpea and 43.5% of lentil accessions (Figure 1). The relevance of ICRISAT and ICARDA, with respect to the other genebanks, is related to the extensive cultivation of both these legumes in the semi-arid climatic conditions that are typical of several Asian and sub-Saharan regions. Chickpea and lentil are staple foods for people living in countries located in these geographic areas.
The overview of collections held by European genebanks, as returned by the European Search Catalogue for Plant Genetic Resources (EURISCO), shows that, globally, this network keeps an accession number that is significantly lower with respect to that conserved by ICRISAT and ICARDA (Figure 2).
However, it should be underlined that European collections constitute a further source of germplasm because they are not merely duplicates of subsets of the collections held by ICRISAT and/or ICARDA.
The Russian genebank, Vavilov Institute of Plant Industry (VIR), keeps the largest European collections of both species (Figure 2) and has increased their size in the last fifteen years (Table 1). The importance of VIR among the European genebanks is due to its very long activity in the field of plant genetic resources safeguarding. It should be underlined that the first lentil collection was created and characterized by Russian scientists at beginning of the 20th century [13]. This collection still maintains high scientific relevance because it includes samples of landraces collected in the 1920–1930s which are no longer cultivated [14]. The query of the EURISCO database shows that in addition to large collections, small or very small chickpea and lentil collections are stored in European genebanks. Some examples are shown in Table 2.
Despite their smaller collection size, the role of these genebanks (Table 2) in the safeguarding of chickpea and lentil germplasm is important, being complementary to the role played by the most important ones. Generally, the scientists of the small genebanks devote particular attention toward the collection, characterization and conservation of landraces and populations of their own country. The local collection teams’ deep knowledge of their own country is the key to assuring a systematic screening of the marginal areas frequently undersampled in the larger collections but rich in biodiversity. This allows the collection and ex situ conservation of autochthonous genetic resources that still survive but are under the threat of disappearance within a very short time [15,16].
The ex situ conservation of chickpea and lentil germplasm offers to breeders the opportunity to broaden the genetic bases of commercial varieties belonging to both species. Scientists working at ICRISAT and ICARDA took undoubted advantages during the planning and development of breeding programmes aimed at selecting improved varieties, from the in loco availability of large collections. This is testified by the release of several improved varieties in recent decades by scientists working in both genebanks [17,18,19,20,21]. The diffusion of these new varieties has had positive effects on the production in several underdeveloped countries, contributing to alleviating the chronic scarcity of food.
However, only some decades after the genebank foundation, the drawbacks derived from the management of very large collections by single institutes became manifest. The main drawbacks were due to the costs of keeping, distributing and multiplying their own accessions, in addition to the obligation of cyclical acquisitions of new samples [22]. In consequence of the main genebank role to make stored accessions available to researchers, breeders, farmers and so on, from 1990, great efforts were devoted to setting up chickpea and lentil core collections or mini core collections [23]. These collections encompass a reduced number of accessions that are as representative as possible of the genetic diversity present in the whole collection. In this way, the amount of material that needs to be distributed and multiplied can be substantially reduced. In recent years, several chickpea and lentil core collections—including the diversity of important traits such as pest resistance [24], morphological characters [25,26,27] and so on—have been created by ICRISAT and ICARDA. This process is far from completion as a consequence of the cyclic acquisition of new materials, as well as of the great advancement of knowledge derived from omic techniques [28,29].
It is well known that the narrow genetic variation of modern varieties of chickpea and lentil is the major issue in the further improvement of these species, as required by present and future challenges. For example, the most popular chickpea varieties are particularly vulnerable to water stress and climate changes [30]. A more efficient use of available germplasm requests broadening the genetic diversity of commercial varieties and the enhancement of genetic gain during the breeding steps [31]. The core collections could be a very useful starting point for germplasm users. They can remove time- and resource-consuming steps, such as the screening of large germplasm segments to identify the parents carrying the desirable traits.

3. The Passport Data of the Collections

The main critical bottleneck for the best use of germplasm collections is the insufficient sharing of data relative to stored accessions. Nowadays, Genesys (https://www.genesys-pgr.org/, accessed on 1 August 2022) is the most complete platform for germplasm search in the worldwide genebank network. It was launched in 2008 with the aim of improving the sharing of Plant Genetic Resources for Food and Agriculture (PGRFA) that are held in the thousands of genebanks operating around the world. The query is free and allows access to the passport and characterization data of 4,207,031 accessions conserved in 450 genebanks. The setup of this platform, which can enable access to large and small collections, is the logical evolution of the previous fragmentation of the information relative to the germplasm collections. Until a few years ago, the passport data of stored accessions were dispersed in several databases that were independently managed by each genebank. Concerning the species object of this paper, Genesys returns 65,475 and 33,357 accessions of chickpea and lentil, respectively (accessed 31 August 2022). The comparison of these numbers with those of the CGIAR database (Table 1) evidences the great increase in accessible records from 2008 to the present (+59.3 % and +84.2 % for chickpea and lentil, respectively). As shown in Figure 1, all genebanks increased the size of both the collections, but the increase was more significant for the institutes labelled “Others” in Genesys. Despite the advancements in database structure, the quantification of how many new entries really are newly collected samples or merely duplicates created by exchange among genebanks, and how many were not previously included in the CGIAR database, is not easy. The change of the identifier accession code usually occurs when the material passes from one genebank to another, for example, to complement a collection. This custom makes the direct identification of duplicates difficult [32,33]. A promising strategy to address this critical issue can be the attribution to each accession of the Digital Object Identifier (DOI), a standardized alphanumeric string provided by the secretariat of the International Treaty on Plant Genetic Resources for Food and Agriculture (ITPGRFA). The assigned DOI remains unchanged during the transfers of seed samples among genebanks, allowing the instantaneous identification of duplicates. Although this proposal dates back to 1998 [34] and would offer undoubted advantages in germplasm management (i.e., the link of information from different sources to each accession), the use of DOI is far from being widely adopted. This exposes germplasm users to the risk of accidental inclusions of duplicates during the selection and request of the accessions best fitting the aim of their research.
The availability of as much data as possible is fundamental for the optimal use of the collections, and specifically, to observe the contributions that each accession could give. The Genesys database shows that a very large fraction of chickpea and lentil germplasm comes from Asiatic countries (Figure 3). The main fraction of both the collections is material collected in India (21.6 % and 12.0 % for chickpea and lentil, respectively).
The important role played by chickpea and lentil as sources of proteins in the daily diet of people living in Near East Asian countries could explain the predominance of Indian accessions in the worldwide collections. The geographic origin of the accessions included in Genesys can be visualized as dots on the planisphere, using the tool “Map” (https://www.genesys-pgr.org/a/map/, accessed on 1 August 2022).
The picture generated by the map shows that, on a worldwide level, the Mediterranean basin and some Near East countries are, for both species, the most sampled areas after the Indian subcontinent. This underlines the great attention devoted toward the autochthonous material cultivated in these macro-areas, as the domestication of chickpea and lentil took place in these areas [1,2], and their cultivation has been an uninterrupted practice until the present. Although the samples from the Americas or Australia could also have useful traits, the main part of genetic variation is certainly held by the Mediterranean and Asian germplasm.
A weakness of chickpea and lentil worldwide collections is the high percentage of accessions, of which the geographic origin is declared “Not defined” in Genesys (8147 and 3406 accessions for chickpea and lentil, respectively). Generally, the choice of accessions to be requested is addressed by users toward those collected in the areas that will benefit from the established goal to be achieved (i.e., an increase in yield, tolerance or resistance to biotic and abiotic stress; resilience to climatic changes, etc.). Accessions whose collection site is known at the level of region, province or village are preferred compared to those for which only the country of origin is declared. This modus operandi is due to the impossibility of successfully transferring germplasm among areas with different microclimatic conditions, which is a very common situation in each country. Based on the available information, it cannot be inferred if the origin of these accessions can be recovered by consulting the old databases managed by each genebank, whether completely (collection site) or partially (region or country of provenance). On the other hand, it is possible that, for some of these accessions, the origin cannot be declared, being breeding lines obtained from parents with different countries. Nowadays, the chance that these accessions could be utilized is lowered by the lack of important passport data such as the origin. For example, the origin cannot be disregarded when the research aims to study the spread of a species from its centre of origin towards other regions or continents [35]. Similarly, accessions that lack the origin cannot be taken into consideration when it might be required for the reintroduction of autochthonous germplasm in the areas in which it is disappeared. This is the case for actions that aim to restore the agricultural production in regions that have experienced natural disasters or wars.
The biological status of the accessions is another very useful piece of information for germplasm users. As shown in Figure 4, a high percentage of chickpea and lentil accessions included in Genesys is classified as landrace (49.5 % and 29.7%, for chickpea and lentil, respectively).
Although the definition of landrace is still debated by the scientific community [36,37], there is sufficient agreement on its most important features. Landraces have a recognizable identity, a good adaptation to well-defined areas and pedo-climatic conditions, and the beginning of cultivation is historically substantiated. Moreover, they are able to satisfy the agronomic, nutritional and aesthetical preferences of the community that traditionally grow each one of them. Those belonging to the same species but which are cultivated in different eco-geographical areas display an appreciable genetic variation, and, for this reason, they are an important source of useful genes for breeders [38]. The high percentages of chickpea and lentil landraces stored in genebank facilities (Figure 4) are a promising starting point for the selection of new varieties that can overcome the challenges due to the increase in world population, climatic changes, and the development of more sustainable protocols of cultivation.
Finally, attention should be afforded to the high percentage of accessions grouped under the label “Other” (Figure 4). It can be supposed that this broad group includes seed samples whose biological status was classified according to different criteria by each genebank. Once again, the importance of internationally standardised guidelines being used by all genebanks for material classification is clear, as well as planning the periodic upgrade of databases to delete obsolete definitions.
A very important drawback for germplasm utilization is the lack of material available for the distribution. In reality, less than 50% of Genesys accessions are declared available (44.2 and 35.1, chickpea and lentil, respectively), about 10% are not available, while for the remaining part no information is given. Germplasm distribution contributes to food security, but the running costs of ex situ conservation, those for acquisition and the processing of new samples, as well as the need for the cyclical regeneration of accessions requires the availability of constant financial resources [39,40]. Unfortunately, the perception by policy makers of germplasm importance is low. This hampers the transfer of appropriate financial resources to genebanks, reducing the access to the fully available genetic variation by germplasm users.

4. Non-Omic and Omic Relative to the Two Collections

Genebank activity is not merely the conservation and distribution of seed samples, but also the characterization and promotion of collection use. This goal can be obtained by highlighting the accessions with desirable and heritable traits. The sharing of further information, in addition to the FAO/biodiversity passport data, is a significant step toward a more sustainable use of the collections, especially in view of the future challenges related to the increase in food requests and climatic changes. The increase in the quantity and quality of shared data offers great opportunities to breeders, speeding up the laborious transfer from genebank to farm of desirable traits [41,42]. Characterization and evaluation data have higher utility when they are included in genebank online databases and not in the form of hardcopy archives, as in the past. The morpho-agronomic traits and grain composition of chickpea accessions held by ICRISAT [12] are available in a thematic section (http://genebank.icrisat.org/IND/Char_Chickpea?Crop=Chickpea, accessed on 1 August 2022). Similarly, the GBIS/I tool (https://gbis.ipk-gatersleben.de/gbis2i/faces/index.jsf, accessed on 1 August 2022), implemented by the Institute of Plant Genetics and Crop Plant Research (IPK, Gatersleben, Germany), allows us to retrieve characterization data, plant and seed pictures for the chickpea and lentil accessions stored in the institute facilities. The morphological data and photos of plants for segments of the chickpea and lentil collections can be viewed by consulting the database of the USDA (USA) genebank (https://npgsweb.ars-grin.gov/gringlobal/search, accessed on 1 August 2022).
The great development of omic techniques that has occurred in recent years is producing new opportunities for the better exploitation of germplasm collections, as well as to address future breeding activities. The constant increase in published papers investigating chickpea and lentil collections with omic techniques testifies the great interest of scientists toward the improvement of these species. Several studies provide insight into QTL and alleles that can be targeted in breeding programs. For example, QTL have been identified for traits involved in the drought- and heat-adaptation of chickpea [43,44,45], associated with the seed and plant traits of chickpea [44], or with some seed traits of lentil [46]. The genome-wide association analysis (GWAS) applied to the “lentil reference plus collection” of ICARDA allowed the identification of putative markers for several agronomic traits [47]. Similarly, the GWAS analysis applied to the chickpea collection maintained by VIR identified clusters of SNPs that could be associated with domestication and the spread of this species [48].
Moreover, genotyping techniques can help to identify duplicates and gaps within the germplasm collections. For example, the geographic stratification of the lentil collection held by ICARDA has been the object of some studies [49,50,51]. The authors described the different levels of genetic variation within and among pools of samples collected in different agro-ecological areas. Li et al. [52] evidenced the lower genetic diversity among the chickpea cultivars recently released in Australia in comparison with the variation present in the Australian germplasm collection. This result will open the chance to develop new cultivars that perform best in the climate of this country.
Usually, omic data describing genome, transcriptome, proteome or metabolome, are obtained by germplasm users (breeders or researchers) in the frame of specific projects. Generally, these data can be shared within the project partnership and made public after an embargo period. Conversely, data generated by genebank staff, a low percentage of the total, being not subject to restrictions, are made available to users in a short time through a thematic section of the genebank website or other internet resources related to it. This is the case for the Pulse Crop Database (PCD, https://www.pulsedb.org/, accessed on 1 August 2022) developed by the USDA-ARS Grain Legume Genetics and Physiology Research Unit (USA), in cooperation with the Main Bioinformatics Laboratory at Washington State University (USA). The PCD database, a resource for Genomics-Assisted Breeding (GAB), was created with the aim of organizing and making available to breeders the genetic and genomic data on lentil and pea.

5. Conclusions

Presently, the worldwide chickpea and lentil germplasm collections are constituted by tens of thousands of accessions stored in dozens of genebanks. These very large collections are a precious opportunity for breeders to develop new varieties that can ensure global food security in times of climate changes and increasing demand for good quality proteins. The main aim of research community will be to unlock, as quickly as possible, the genetic diversity present within the stored collections. Over the past few decades, the cooperation among genebanks has constantly intensified, and new platforms for data sharing have been successfully created. The sharing of guidelines, protocols and data is fundamental to obtaining an efficient, global and effective management of the germplasm of these species, which provide an important contribution to the nutrition of the worldwide human population. However, a more sustainable use of chickpea and lentil genetic resources requires further efforts to improve genebank cooperation and remove the weaknesses still present in all steps of collection management.

Funding

This research was funded by PRIMA Foundation, grant entitled “Legumes in biodiversity based farming systems in Mediterranean basin” (LEGU-MED).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. Size increase in the most important collections occurred from 2008 to 2022 (black and grey bars, respectively). Left: chickpea; right: lentil (source Genesys).
Figure 1. Size increase in the most important collections occurred from 2008 to 2022 (black and grey bars, respectively). Left: chickpea; right: lentil (source Genesys).
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Figure 2. Size of the collections held by the most important European genebanks. Bar colour: black—chickpea; grey—lentil (source EURISCO).
Figure 2. Size of the collections held by the most important European genebanks. Bar colour: black—chickpea; grey—lentil (source EURISCO).
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Figure 3. Distribution of stored accessions with respect to the geographic origin. Left: chickpea; right: lentil (source Genesys).
Figure 3. Distribution of stored accessions with respect to the geographic origin. Left: chickpea; right: lentil (source Genesys).
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Figure 4. Percentage distribution of stored accessions among different biological statuses. Bar colour: black—chickpea; grey—lentil (source Genesys).
Figure 4. Percentage distribution of stored accessions among different biological statuses. Bar colour: black—chickpea; grey—lentil (source Genesys).
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Table
Table 1. The most important chickpea and lentil collections conserved by the worldwide genebank network (source CGIAR 2008).
Table 1. The most important chickpea and lentil collections conserved by the worldwide genebank network (source CGIAR 2008).
Genebank NameNo. of Accessions
ChickpeaLentil
International Crops Research Institute for the Semi-Arid Tropics (ICRISAT, India)16,928-----
International Center for Agricultural Research in the Dry Areas, (ICARDA, Lebanon)12,33110,113
United States Department of Agriculture (USDA, USA)46522672
N.I. Vavilov Institute of Plant Industry (VIR, Russia)21132376
Aegean Agricultural Research Institute (AARI, Turkey)1790615
Institute for AgroBotany (ABI, Hungary)815857
Others 24671481
TOTAL41,09618,114
Table
Table 2. Size of chickpea and lentil collections conserved by some minor genebanks (source EURISCO).
Table 2. Size of chickpea and lentil collections conserved by some minor genebanks (source EURISCO).
Institute CodeGRC005CYP004ROM007ARM059ALB026
Lentil accessions
Total 971938342
Domestic 971924222
Chickpea accessions
Total 17728127429
Domestic 1772822369
GRC005: Greek Genebank, Agricultural Research Center of Macedonia and Thrace, National Agricultural Research Foundation, Greece; CYP004: National Genebank, Agricultural Research Institute, Ministry of Agriculture, Rural Development and Environment, Cyprus; ROM007: Suceava Genebank, Romania; ARM059: Scientific Center of Agrobiotechnology, Armenia; ALB026: Plant Genetic Resources Center, Albania.
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Piergiovanni, A.R. Ex Situ Conservation of Plant Genetic Resources: An Overview of Chickpea (Cicer arietinum L.) and Lentil (Lens culinaris Medik.) Worldwide Collections. Diversity 2022, 14, 941. https://doi.org/10.3390/d14110941

AMA Style

Piergiovanni AR. Ex Situ Conservation of Plant Genetic Resources: An Overview of Chickpea (Cicer arietinum L.) and Lentil (Lens culinaris Medik.) Worldwide Collections. Diversity. 2022; 14(11):941. https://doi.org/10.3390/d14110941

Chicago/Turabian Style

Piergiovanni, Angela Rosa. 2022. "Ex Situ Conservation of Plant Genetic Resources: An Overview of Chickpea (Cicer arietinum L.) and Lentil (Lens culinaris Medik.) Worldwide Collections" Diversity 14, no. 11: 941. https://doi.org/10.3390/d14110941

APA Style

Piergiovanni, A. R. (2022). Ex Situ Conservation of Plant Genetic Resources: An Overview of Chickpea (Cicer arietinum L.) and Lentil (Lens culinaris Medik.) Worldwide Collections. Diversity, 14(11), 941. https://doi.org/10.3390/d14110941

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