# Seed quality as a proxy of climate-ready orphan legumes: the need for a multidisciplinary and multi-actor vision

Alma Balestrazzi, Cinzia Calvio, Anca Macovei, Andrea Pagano, Patrick Laux, Hassane Moutahir, Loïc Rajjou, Eleni Tani, Dimosthenis Chachalis, Christos Katsis, et al.

<figure><img src="image_1.png" /></figure>

## To cite this version:

Alma Balestrazzi, Cinzia Calvio, Anca Macovei, Andrea Pagano, Patrick Laux, et al. Seed quality as a proxy of climate-ready orphan legumes: the need for a multidisciplinary and multi-actor vision. Frontiers in Plant Science, 2024, 15, pp.1388866. 10.3389/fpls.2024.1388866. hal-05166315

HAL Id: hal-05166315

https://hal.science/hal-05166315v1

Submitted on 10 Sep 2025

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

<figure><img src="image_2.png" /></figure>
<figure><img src="image_3.png" /></figure>

Check for updates

OPEN ACCESS

EDITED BY
Leo Sabatino,
University of Palermo, Italy

REVIEWED BY
Dr. Debasis Mitra,
Graphic Era University, India
Mohd. Kamran Khan,
Selçuk University, Türkiye

*CORRESPONDENCE
Alma Balestrazzi

✉ alma.balestrazzi@unipv.it

†PRESENT ADDRESS
Susana Araújo,
Mountain Environment and Ecosystem
Management, MORE - Collaborative
Laboratory Mountains of Research (MORE),
Bragança, Portugal

RECEIVED 20 February 2024

ACCEPTED 12 July 2024

PUBLISHED 01 August 2024

CITATION

Balestrazzi A, Calvio C, Macovei A, Pagano A, Laux P, Moutahir H, Rajjou L, Tani E, Chachalis D, Katsis C, Ghaouti L, Gmouh S, Majid S, Elleuch A, Hanin M, Khemakhem B, El Abed H, Nunes J, Araújo S, Benhamrouche A and Bersi M (2024) Seed quality as a proxy of climate-ready orphan legumes: the need for a multidisciplinary and multi-actor vision.

Front. Plant Sci. 15:1388866.
doi: 10.3389/fpls.2024.1388866

COPYRIGHT

© 2024 Balestrazzi, Calvio, Macovei, Pagano, Laux, Moutahir, Rajjou, Tani, Chachalis, Katsis, Ghaouti, Gmouh, Majid, Elleuch, Hanin, Khemakhem, El Abed, Nunes, Araújo, Benhamrouche and Bersi. This is an open-access article distributed under the terms of the [Creative Commons Attribution License (CC BY)](https://creativecommons.org/licenses/by/4.0/). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Seed quality as a proxy of climate-ready orphan legumes: the need for a multidisciplinary and multi-actor vision

Alma Balestrazzi<fnref n="1" />*, Cinzia Calvio<fnref n="1" />, Anca Macovei<fnref n="1" />,
Andrea Pagano<fnref n="1" />, Patrick Laux<fnref n="2" />, Hassane Moutahir<fnref n="2" />,
Loïc Rajjou³, Eleni Tani⁴, Dimosthenis Chachalis⁵,
Christos Katsis⁶, Lamiae Ghaouti⁷, Said Gmouh⁸, Sanaa Majid⁹,
Amine Elleuch<fnref n="10" />, Moez Hanin<fnref n="10" />, Bassem Khemakhem<fnref n="10" />,
Hanen El Abed<fnref n="10" />, Joao Nunes¹¹, Susana Araújo¹¹†,
Aziz Benhamrouche¹² and Mohand Bersi¹²

In developing countries, orphan legumes stand at the forefront in the struggle against climate change. Their high nutrient value is crucial in malnutrition and chronic diseases prevention. However, as the 'orphan' definition suggests, their seed systems are still underestimated and seed production is scanty. Seed priming is an effective, sustainable strategy to boost seed quality in orphan legumes for which up-to-date guidelines are required to guarantee reliable and reproducible results. How far are we along this path? What do we expect from seed priming? This brings to other relevant questions. What is the socio-economic relevance of orphan legumes in the Mediterranean Basin? How to potentiate a broader cultivation in specific regions? The case study of the BENEFIT-Med (Boosting technologies of orphan legumes towards resilient farming systems) project, developed by multidisciplinary research networks, envisions a roadmap for producing new knowledge and innovative

<footnote n="1">¹Department of Biology and Biotechnology "L. Spallanzani", University of Pavia, Pavia, Italy,</footnote>

<footnote n="2">²Institute of Meteorology and Climate Research (IMK-IFU), Karlsruhe Institute of Technology, Garmisch-Partenkirchen, Germany, ³Université Paris-Saclay, National Research Institute for Agriculture, Food and the Environment (INRAE), AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), Versailles, France, ⁴Laboratory of Plant Breeding and Biometry, Department of Crop Science, Agricultural University of Athens, Athens, Greece, ⁵Department of Pesticides' Control and Phytopharmacy, Benaki Phytopathological Institute, Athens, Greece, ⁶Agroland S.A., Sofades, Greece, ⁷Department of Plant Production, Protection and Biotechnology, Hassan II Institute of Agronomy and Veterinary Medicine, Rabat, Morocco, ⁸Laboratory Laboratory of Engineering and Materials (LIMAT), Faculty of Sciences Ben M'sick, University Hassan II of Casablanca, Casablanca, Morocco, ⁹Laboratory GeMEV, Faculty of Sciences Ain Chock, University Hassan II of Casablanca, Casablanca, Morocco,</footnote>

<footnote n="10">¹⁰Higher Institute of Biotechnology, University of Sfax, Sfax, Tunisia, ¹¹Center Bio R&D Unit, Association BLC3-Technology and Innovation Campus, Oliveira do Hospital, Portugal, ¹²Institute of Architecture and Earth Science, University Ferhat Abbas-Setif 1, Setif, Algeria</footnote>
technologies to improve seed productivity through priming, with the long-term objective of promoting sustainability and food security for/in the climate-sensitive regions. This review highlights the existing drawbacks that must be overcome before orphan legumes could reach the state of 'climate-ready crops'. Only by the integration of knowledge in seed biology, technology and agronomy, the barrier existing between research bench and local agricultural fields may be overcome, generating high-impact technical innovations for orphan legumes. We intend to provide a powerful message to encourage future research in line with the United Nations Agenda 2030 for Sustainable Development.

KEYWORDS

climate change, Greater Mediterranean Region, resilience, food security, multi-actor approach, underutilized legumes, seed priming and seed system, vulnerability mapping

# 1 Introduction

In the climate-vulnerable regions, local populations are exposed to high mortality rate due to malnutrition exacerbated by climate change. The complex interactions between climate-change and food systems, and their domino effect on human health, represent a major challenge that requires urgent and enduring actions (Hertel et al., 2021; Zurek et al., 2022). Mitigation strategies have been designed to speed up the transition towards sustainable, climate-resilient food systems, e.g. those reported by the Intergovernmental Panel on Climate Change: demand-side changes, protection of ecosystems, improved farm management, and decarbonizing supply chain (IPCC, 2022). Mitigation strategies involve multi-level players, such as political, financial, industrial, and scientific actors, together with the civil society (IPCC, 2022; Global Panel on Agriculture and Food Systems for Nutrition, 2023).

Major crops show poor genetic diversity and high vulnerability to extreme climate events, implying their replacement by a new generation of 'climate-ready' crops (Bourke et al., 2021; Xiong et al., 2022). This goal can be achieved by valorizing local minor crops (orphan crops or neglected, underutilized species-NUS) that currently have very limited impact on the market but are yet essential for small farmers' survival in developing countries (Tadele, 2019; Popoola et al., 2022). According to FAO (2019), these species "have lost relevance over the last 500 years due to societal, agronomic, or biological factors". Orphan crops include legumes, appreciated for their drought tolerance and capacity to improve soil fertility (Popoola et al., 2022), on top of their nutritional and medicinal features (Ogbole et al., 2023). These species and their seed systems are still undervalued, despite the crucial role they play in supporting human and animal nutrition, and favoring the growth of other crops (Cullis and Kunert, 2017; Popoola et al., 2022). This work provides a multidisciplinary and collaborative vision for the creation of new solutions allowing to

cope with the challenges related to orphan legumes, with a particular focus on seed quality issues.

# 2 Orphan legumes as 'climate-ready' crops

Major crops are not able to adapt to climate change. Conversely, orphan legumes are 'climate-smart' plants with outstanding agronomic features, able to support sustainable livelihood, even under harsh environments (Popoola et al., 2022). Orphan legumes did not undergo the intensive breeding selection experienced by major crops, thus retaining a huge genetic variability and unique assortments of stress resilience traits. These enormous genetic resources are exposed to erosion, linked to their underutilization, reducing the chances of their future exploitation (Popoola et al., 2022; Kumar et al., 2023). Orphan legumes are poorly represented in germplasm collections and lack formal seed supply systems. They are usually identified based on their local relevance, adaptation to marginal areas, agroecological niches. Their cultivation and use are still relying on local knowledge. The limited market potential and lack of functional value chains hamper full valorization. To revert this status, several actions are needed at different levels: policies should encourage basic/applied research on these species, breeding programs should be established to obtain improved hybrids, agrifood industries should diversify their investments including orphan legumes, and an increased consumers' awareness should stimulate the process from the basis, laying at the intersection between supply and demand (Cullis et al., 2019; Borelli et al., 2020; Elolu et al., 2023).

Orphan legumes are native to Africa, Asia, South America, North America, South Pacific, and Australia, although some species are classified as orphan in one location and as conventional crops in other areas (Talabi et al., 2022). Institutions involved in the identification and the proper management of orphan legumes are shown in Table 1.
<table><caption>TABLE 1 List of International Institutions that currently host germplasm collections of orphan legumes.</caption><thead><tr><th>Host Institution</th><th>Underutilized Species</th><th>Reference</th></tr></thead><tbody><tr><td>CIGIAR<br>https://www.cgiar.org/<br>AOOC<br>https://africanorphancrops.org/<br>FAO/RAP<br>https://www.fao.org/asiapacific/en/<br>CROP TRUST<br>https://www.croptrust.org/<br>CFF<br>https://cropsforthefutureuk.org/<br>IITA<br>https://www.iita.org/<br>WVC<br>https://avrdc.org/<br>PGRCU-USDA-ARS<br>https://www.ars.usda.gov/southeast-area/griffin-ga/<br>pgrcu/docs/about-pgrcu/</td><td>African yam bean<br>(Sphenostylis stenocarpa L.)<br>African winged bean<br>(Psophocarpus tetragonolobus L.)<br>Moth bean<br>(Vigna aconitifolia L.) Bambara groundnut<br>(Vigna subterranean L.) cowpea<br>(Vigna unguiculata L.)<br>Kersting's groundnut<br>(Macrotyloma geocarpum L.)<br>Lima bean<br>(Phaseolus lunatus L.)<br>Sword bean<br>(Canavalia gladiata L.)<br>Jack bean<br>(Canavalia ensiformis L.)<br>hyacinth bean<br>(Lablab purpureus L.)<br>pigeon pea<br>(Cajanus cajan L.)<br>ghaf<br>(Prosopis cineraria L.)<br>gum acacia<br>(Acacia senegal L.)<br>cluster bean<br>(Cyamopsis tetragonoloba L.)<br>Trigonella<br>(Trigonella foenum-graecum L.)<br>grass pea<br>(Lathyrus sativus L.)<br>forage pea<br>(Pisum sativum var. arvense)</td><td>Li and Siddique, 2018<br>Hendre et al., 2019<br>Talabi et al., 2022<br>Popoola et al., 2022<br>Abberton et al., 2022<br>Joshi et al., 2023<br>Vaz Patto and Rubiales, 2014<br>Powers and Thavarajah, 2019<br>Visuvanathan et al., 2022<br>Ramya et al., 2022<br>Gonçalves et al., 2022<br>Greveniotis et al., 2022</td></tr></tbody></table>

CGIAR, Consultative Group for International Agricultural Research; AOCC, African Orphan Crops Consortium; FAO/RAP, Agriculture Organization of the United Nations Regional Office for Asia and the Pacific; CFF, Crops for the Future; IITA, International Institute of Tropical Agriculture, Nigeria; WVC, World Vegetable Center, Taiwan; PGRCU-USDA-ARS, Plant Genetic Resources Conservation Unit - U. S. Department of Agriculture - Agricultural Research Service.

A list of underutilized crops (Future Smart Food) was compiled by the African Orphan Crops Consortium (AOCC) and the Agriculture Organization of the United Nations Regional Office for Asia and the Pacific (FAO/RAP), according to high nutritional profile, climate, resilience, local availability, and economic viability.

## 3 How would seed quality impact the productivity of orphan legumes under the challenges of climate change?

### 3.1 Seed systems: a variegated landscape moving towards climate-resilience

Enhanced seed vigor is the first step towards the valorization of any crop and, in particular, of those missing an official seed supply system. Seed systems include all the activities for variety development (Louwaars and Manicad, 2022). They are classified into categories that often co-exist in the same territory, resulting in a variegated landscape (Figure 1). Community-based seed systems rely on experienced farmers who take care of seeds provided by other farmers and share the improved products (Gonsalves, 2013). Besides a special care in ensuring a wide agrobiodiversity, the

current challenges for community-based seed systems refer to a more inclusive approach aimed at engaging increased numbers of local farmers, the organization of wide and frequent participatory activities, as well as the development of strategic partnerships with public/private sectors. Community-based seed systems are the core of local enterprises (Vernooy et al., 2022). In formal seed system, activities are strictly regulated. Seed producers are registered and possess a certification under the control of public institutions. Certified seeds are also produced in collaboration with private seed companies (Kansiime et al., 2021). Small farmers still rely on informal seed system in which seeds are acquired through personal exchanges, gifts, local markets. However, informally traded seeds are at risk in terms of genetic purity, viability and productivity. Informal systems, the main source of seeds in climate-vulnerable regions, do not provide deal with 'breeder seed' (genetically and physically pure seeds propagated under strict control) and 'basic seed' (produced by registered growers, under the control of certification agencies) (Vernooy et al., 2022). Finally, semi-formal seed systems integrate the formal and informal systems. They are represented by farmers who manage all the value chain steps, reaching enhanced seed quality with the support of technical and financial partners (ICRISAT, 2008). In response to adverse environments, the different seed
<figure><img src="image_4.png" /><figcaption>FIGURE 1</figcaption></figure>

Seed systems are crucial vehicles that allow farmers to acquire good quality seeds of new varieties, playing an essential role in the process of orphan legumes adoption in the climate-vulnerable regions of Mediterranean area. They are part of a variegated puzzle, since different types of seed systems currently exist: formal, semi-formal, informal, and community-based seed systems. Actions should be taken in order to promote remodelling and integration of the different seed systems, based on local agronomic, technical, socio-economic, and cultural needs. Stakeholders, including policy makers, are committed to provide such flexibility, as a key factor towards better climate resilience of local agroecosystems.

systems provide complementary characteristics (Figure 1), and seeds can be moved from the informal to the formal context (or vice versa) to buffer such changes (Louwaars and Manicad, 2022). However, this is not sufficient to mitigate the impact of severe climate change and ensure food security. The resilience of this variegated landscape should be reinforced not only in terms of scientific/technical skills, required for proper management of germplasm collections, but also by supporting socio-economic and political strategies. The goal is the design of political roadmaps to protect and provide local farmers with the most adapted varieties, in a rapid and efficient manner (Louwaars and Manicad, 2022).

## 3.2 Seed traits for climate-resilience

For the correct management/selection of the seeds to be used in challenging conditions, a fundamental asset is the identification of the most relevant seed traits in terms of climate resilience. Detailed agronomic and genetic information is not generally available for orphan legumes. Thus, it is imperative to link phenotype- and genotype-based information to be able to exploit these traits for future breeding strategies (Chapman et al., 2022). The identification of valuable genetic characteristics relies on the identification of quantitative trait loci (QTLs), development of codominant molecular markers and linkage maps (Oluwole et al., 2021). In Kersting's groundnut, genome wide association studies (GWAS) identified SNP (single nucleotide polymorphism)-based marker-

trait associations related to seed size/weight (Akohoue et al., 2020). GWAS performed on cowpea and castor bean accessions retrieved candidate genes associated with seed size, involved in endosperm/embryo development, and cell elongation (Lo et al., 2019; Xu et al., 2021). Increase in seed size was reported to be associated with enhanced drought tolerance, making this trait very promising in future breeding strategies (Kaydan and Yagmur, 2008; Gholami et al., 2009; Mut and Akay, 2010; Čanak et al., 2020; Martínez-López et al., 2020; Christie et al., 2022). There is also increasing evidence for a cross-talk between drought stress-mediated signaling and endogenous molecular pathways can control the final seeds size (Lv et al., 2019). It has been reported that seed size contributes to drought stress tolerance in camelina (Camelina sativa L.), however the response varies depending on biotype and intensity of the imposed stress (Čanak et al., 2020). These findings highlight the need to assess the plant performance under field conditions. Conversely, a larger seed size entails higher management costs by smallholder farmers and increased risk for seed damaging during storage and transport (Ojiewo et al., 2018).

Genes controlling seed dispersal and facilitating harvesting, as well as genes related to seed size may contribute to reduce farmers' time and efforts. Seed dispersal dynamics allow plant adaptation to climate change by facilitating the migration of species at risk (Fricke et al., 2022). The mutualistic interactions with animals acting as vehicles of dispersal is increasingly affected by the disruptive impact of climate change, and this contributes to further threaten the viability of ecosystems (Fricke et al., 2022). Seed dispersal is facing rapid changes in response to climate change. This trait, resulting
from a complex, polygenic genetic background, is still poorly investigated in both crop and model plants (Saastamoinen et al., 2018). In the specific case of crop wild relatives, source of unexplored gene pools for resilience, improved knowledge on this and other seed-related traits is required to better manage long-term conservation (Brónnvik and von Wettberg, 2019). Seed yield losses caused by pod dehiscence in forage legumes has been targeted during domestication (Liu et al., 2019; Parker et al., 2021). A better understanding of the mechanisms controlling such a process can help improving the production of forage legumes, particularly those highly resilient species, so far neglected by breeders (Parker et al., 2021; Guo et al., 2022).

Traits that influence the seed nutritional content, the cooking time, and processability have been also identified (Dawson et al., 2019). Climate-resilient crops must be able to provide healthy foods enriched with essential vitamins and minerals (iron, zinc), folate, and fiber. This is typical of neglected species producing highly nutritious seed grains, proxy of food security. In-depth research is necessary, to disclose the properties of such orphan crops and speed up the diversification of healthy diets for the global population (Zenda et al., 2021). Such efforts include the identification of major QTLs, genes and metabolic pathways that shapes the nutritional profile of seeds. This is the case of QTLs controlling iron and zinc concentration in chickpea seeds (Upadhyaya et al., 2016), oil and protein content in soybean (Huang et al., 2020), oil content, protein content, and fatty acids (linoleic and oleic acids) in groundnut (Roorkiwal et al., 2021). Cooking times are influenced by storage, environment, and genotype (Cichy et al., 2019). There is poor knowledge concerning the genetic variation of this trait. Studies carried out using fast and slow cooking bean (Phaseolus vulgaris L.) genotypes with different seed types highlighted significant correlations with seed coat thickness and cotyledon cell wall (Bassett et al., 2021). Pasting and cooking properties were assessed in a germplasm collection of orphan legumes that included grass pea (Santos et al., 2018). Multiple seed traits, e.g. size, shape, color, surface influenced physico-chemical parameters as viscosity, hydration capacity and cooking time. A deeper understanding the genetic bases ruling variability across species/ accessions could provide useful indicators for the screening of germplasm cooking properties (Santos et al., 2018).

Seed processability is related to the presence of components affecting seed protein digestibility. Such inhibitors, known as antinutrients or antinutritional factors can be removed using dedicated processing technologies, either traditional (cooking, milling, extrusion, germination, fermentation) or innovative technologies (e.g., high-pressure processing, ultrasound, irradiation, microwave). The seed response to these treatments is influenced by genetic factors, such as the qualitative and quantitative profiles of trypsin inhibitors, phytates, tannins, and lectins (Ohanenye et al., 2022). For orphan legumes, the genetic characterization of the most valuable traits and the subsequent breeders' work are part of a long-term innovation program that must be supported by seed technologists. Once the breeding program has started, several generations are necessary to reach

the status of certified seeds. Seed quality changes depending on the seed system, crop species/variety, and location of production.

## 3.3 Seed priming as a tool to mitigate the impact of climate change

Pre-sowing techniques (seed priming) are easily implementable tools, immediately available and applicable to crops, used to increase seed vigor (Pagano et al., 2023a). Seed imbibition is performed under controlled conditions (time, temperature, light/dark) with water, or in solutions containing priming agents, followed by dehydration. Controlled imbibition must be stopped before radicle protrusion occurs, otherwise, seeds will lose desiccation tolerance (Pagano et al., 2023a). Seed priming acts on specific components of the pre-germinative metabolism, a complex array of molecular pathways underlying the seed ability to scavenge the cytotoxic reactive oxygen species and repair DNA damage (Rajjou et al., 2012; Pagano et al., 2023a). The benefits provided by seed priming include improved germination performance and enhanced plant stress tolerance. Seed priming can be performed using water (hydropriming, matrix priming) or a wide range of priming agents that include salts (halopriming), PEG (polyethylene glycol; osmopriming), phytohormones (hormopriming), antioxidant and bioactive molecules (chemical priming), beneficial microorganisms (biopriming) and nanoparticles (nanopriming) (for a more comprehensive description, see review by Pagano et al., 2023a).

Seed priming improves drought tolerance in a wide range of cereal and legume crops (Saha et al., 2022) and several priming agents can effectively promote the seed antioxidant response and osmotic regulation, as mannose (Hameed and Iqbal, 2014), SiO₂, KNO₃, salicylic acid (Zheng et al., 2016; Tabassum et al., 2018; Ali et al., 2021), polyethylene glycol (Tounekti et al., 2020). Biopriming mediated by plant growth promoting bacteria can also mitigate drought stress (Pravisya and Jayaram, 2015; Shaffique et al., 2023; Srivastava et al., 2024). Soil salinity was reported to currently affect more than 30% of global irrigated land, being NaCl the most abundant salt in the soil. Seed germination is impaired under salt stress due to unfavorable osmotic potential and ion-mediated toxicity (Khan et al., 2022). Seed priming can alleviate the deleterious effects of salinity, as reported for rice seeds treated with CaCl₂-based priming (Al-Tamimi et al., 2016). Seed priming applied to wheat using glycine betaine, vitamin B₁₂, sodium nitroprusside, jasmonate, CaCl₂, and KCl enhances chlorophyll content, stabilizes membranes and triggers antioxidant enzymes activity, mitigating salt stress (Sadeghi and Robati, 2015; Keshavarz and Moghadam, 2017).

Heat stress affects the plant physiological and metabolic processes due to protein denaturation, altered membrane integrity, and enzyme inactivation. Hydropriming, osmopriming with CaCl₂, and hormopriming with salicylic acid were able to support germination of garden pea cultivars under heat stress, improving seed quality and plant development (Tamindžić et al., 2020).
2023). Priming with nitrate salts improves nitrate reductase and amylase activity, nitrogen, amino acid and chlorophyll content in leaves, increases proline and sugar content, antioxidant metabolism, under heat stress (Kumar et al., 2021; Tamindžić et al., 2023). Brassinosteroids used as seed priming agents significantly improved the growth and physiological parameters of Brassica juncea L. triggering enhanced antioxidant defense under heat stress (Neha et al., 2022). Cytokinins were used as priming agent to assess mitigation protocols against heat stress in wheat (Jaiswal et al., 2022). Field studies showed that plant survival under stress requires proteomic plasticity mediated by the ubiquitin-proteasome system. The effects of flooding stress on seed germination in rice (Oryza sativa L.) can be alleviated using seed priming with selenium (Se) (Hu et al., 2022). Selenium could limit malondialdehyde content, increase starch hydrolysis efficiency, enhance antioxidant activities, leading to improved biomass production. However, Se concentrations should be carefully selected in order to avoid the risk of seedling death during long-term flooding (Hu et al., 2022). These treatments also induce molecular mechanisms related to stress memory, accounting for trans-generational effects (Louis et al., 2023). Seed priming has an enormous potential to improve seed quality in fragile agroecosystems and fasten the route to food security, promoting drought tolerance and multiple stress resilience. Primed seeds are crucial for successful stand establishment and uniformity when farmers are forced to change the timing of sowing, due to environmental constraints (Singh et al., 2020; Devika et al., 2021; Liu et al., 2022). Improving seed quality support breeders' work during the selection of 'climate-smart' varieties (Pagano et al.,

2023a). However, the complexity of seed physiology, genetic background, and the influence of environment result in variability when the technique is applied. Current seed priming technologies would benefit from increased flexibility and efficacy, generated by integrating knowledge in seed biology/technology and agronomy of orphan legumes, moving from bench to field.

## 3.4 From bench to field: 'on-farm' seed priming

Seed priming is part of the Seed Treatment Market (estimated size in 2022: > 12.4 billion USD) (Global Market Insights, 2023). Seed companies own patented priming protocols, tailored for major crops but village farmers do not benefit from these resources. 'On-farm' seed priming, managed directly by farmers, differs from industrial strategies (Harris et al., 2005; Carrillo-Reche et al., 2018; Devika et al., 2021). In most cases, farmers know that soaking seeds in water before sowing improves plant establishment but they are often unaware of safe limits and drawbacks that might derive from inappropriate treatments. When dealing with fragile ecosystems, the choice of the most suitable priming approach should be carefully handled to maximize benefits. To fully exploit seed priming advantages, specific training with procedures tailored on seed lot/variety should be provided by means of participatory trials with local farmers, seed technologists and researchers (Harris et al., 2005) (Figure 2).

<figure><img src="image_5.png" /><figcaption>FIGURE 2</figcaption></figure>

How can orphan legumes reach the status of 'climate-ready crops'? To what extent can seed quality promote this transition? The 'seed quality' perspective, in terms of scientific, technological, and agronomic contributions is depicted. This avenue moves from bench to field as follows. The potential 'climate-ready' germplasm available deserves in-depth characterization to assess its real value. This requires the contribution of i) basic research on the molecular mechanisms (e.g. antioxidant players and DNA damage response) underlying seed quality, ii) applied research leading to advanced seed technology (e.g. more effective seed priming protocols), iii) knowledge/technology transfer to farmers and other stakeholders through training, participatory work, with focus on women empowerment.
## 4 Strategies to enhance seed quality in orphan legumes

Valorization of orphan legumes implies the intensification of their value chains, taking a series of actions ranging from geographic/climatic studies to socio-economic support measures. Multi-actor and cross-disciplinary research networks can bring innovation in orphan legumes production, building novel models in terms of profitability, resilience and environmental sustainability. A recent search carried out in PubMed using the keyword “orphan

legume” (https://pubmed.ncbi.nlm.nih.gov/?term=orphan%20legume& timeline=expanded& showed) highlighted a stationary phase in the scientific production in the 1990-2004 period, followed by a progressive increase in the number of articles dealing with this topic, mostly focused on breeding whereas issues of related value chains and socioeconomic impact are still poor investigated. EU-funded, multidisciplinary projects such as CROPDIVA (https://www.cropdiva.eu/), ForEVA (https://www.ecpgr.org/working-groups/grain-legumes/foreva), LEGUMINOSE (https://www.leguminose.eu/), and LEGU-MED

<figure><img src="image_6.png" /><figcaption>FIGURE 3</figcaption></figure>

(A) The multidisciplinary BENEFIT-Med Consortium across the Mediterranean Basin includes eleven Partners distributed in eight countries: Germany, France, Portugal, Italy, and Greece from the EU side; Morocco, Algeria, and Tunisia from North Africa. (B) The 'seed priming interactome' represents the multidisciplinary effort and multitarget action of the BENEFIT-Med Consortium, envisaged as a mitigation strategy to boost orphan legumes adoption. Such strategy, relying on dedicated seed technology, requires cross-talk at different levels: i) climate change is targeted through a multidisciplinary approach (e.g. climate science, agronomy), ii) geography is included as mapping the climate vulnerable sites of the Mediterranean area is an essential step for future actions, iii) databases (BENEFIT-Med Hub-Med database) are crucial, as knowledge source and repository, iv) farming systems as the target of seed quality-based innovation, recipients of the benefits brought by orphan legumes, v) socio-economic development of vulnerable regions supported by dedicated actions (dissemination and training, involvement of policy-makers).
(https://www.era-learn.eu/network-information/networks/prima/
section-2-call-2019-multi-topic/legumes-in-biodiversity-based-
farming-systems-in-mediterranean-basin) are currently promoting
the use of underutilized legume species, and the cross-talk between
such established research networks will be a powerful driver of more
extensive and effective knowledge transfer as well as deeper dialogue
with end users.

The case study hereby described is the BENEFIT-Med
(Boosting technologies of orphan legumes towards resilient
farming systems; https://www.benefit-med.eu/) project, funded by
the PRIMA Foundation (https://prima-med.org/), whose main goal
is to develop an innovative, and manageable seed priming-based
technology for the sustainable production of highly resilient orphan
legumes in the Mediterranean Basin.

## 4.1 The BENEFIT-Med project: filling the gap of knowledge

Sustainable and resilient agroecosystems are made of
agronomic, economic, social and ecological components. The
synergic combination of technical and scientific expertise, multi-
actors' networks, and participatory work are required to design such
complex structures (Westengen et al., 2023). Trigonella, grass pea,
and forage pea are target species selected for valorization by the
multidisciplinary BENEFIT-Med consortium, featuring the
synergic interaction of eleven partners from eight countries along
the Mediterranean Basin (Figure 3A). 'On-farm' seed priming
protocols have been developed at lab scale, and tested under
controlled conditions whereas the impact on agronomic
performance is currently under evaluation in open-field trials, at
different locations in Southern Europe and North Africa (Pagano
et al., 2023b). The extreme climate conditions occurred in 2023
allowed to carry out 'stress-tests' to assess the benefits of seed
priming but at the same time forced the asynchronous
experimentation among partner countries. When the output data
will be collected, the performance of accession-tailored protocols
will be evaluated. The participatory work with local farmers,
planned in the near future (2024) will play a crucial role to
further optimize treatments and to train farmers about their
rationale and effective use of the strategies developed within the
BENEFIT-Med consortium. Such tailored seed technologies will be
integrated into plant breeding studies to speed up the
characterization of pre-breeding materials (Weissmann et al., 2023).

Exploring the tip of the 'iceberg' represented by the biodiversity of
orphan legumes and transferring such biodiversity into their value
chains are crucial. The knowledge of local communities should be
preserved and valorized, as a carrier of resilient seed systems
(Louwaars and Manicad, 2022; Westengen et al., 2023). It should be
also underlined that mining for molecular mechanisms underlying
seed quality is an urgent task, being an example of translational
research that can accelerate the environmental adaptation of orphan
legumes and related agroecosystems (Pagano et al., 2023a). Although
seed priming is a main driver in the BENEFIT-Med model, this
technology will lose its potential if not integrated into a much wider
picture accounting for essential interactors, namely geography,

climate, existing farming systems (Figure 3B). In BENEFIT-Med,
climatologists are also investigating adaptation scenarios to unveil
the impact of climate change, estimate site vulnerability and develop
adaptation strategies able to support stakeholders and decision-
makers (Cradock-Henry et al., 2021).

## 4.2 Vulnerability mapping: an interdisciplinary approach

The rural areas of the Mediterranean region are included in the
list of most worldwide vulnerable targets (Ali et al., 2022). In order
to support orphan legumes integration into Mediterranean food
systems, a deeper understanding of consumption barriers and
production constraints is required. Without these efforts, orphan
legumes will face extinction because of 'anthropogenic negligence'
(Talabi et al., 2022). A detailed mapping of vulnerable sites,
reflecting the severity of barriers, should be developed.
Vulnerability mapping requires an interdisciplinary approach
embracing geography, environmental sciences, economics and
political sciences, agronomy and climatology. Social aspects
integrated with climate exposure metrics will allow to assess
vulnerability drivers and adaptation indicators (de Sherbinin
et al., 2023; Ngcamu, 2023; Goufa et al., 2024).

Climate-vulnerable sites are mapped based on socio-cultural
barriers resulting from the different sensitivity and adaptation
response of individuals and specific social/cultural groups.
Economic barriers impair seed production and seed systems
development, compromising market competitiveness. The challenge
lies in promoting financial investments in order to strengthen the role
of orphan legumes in the sustainable agrosystems of the
Mediterranean region. Economic failure is the result of weak/
missing supportive policies (political barriers), agriculture-related
policies and policy frameworks (institutional barriers) should be
revised to expand the use of orphan legumes e.g., by improving
services to rural populations, adding these species in the national
export strategy, or investing in the maintenance of traditional
knowledge (Aktürk and Dastgerdi, 2021). Regular cross-talks with
stakeholders are absolutely required to stimulate continuous
participatory work and mitigate conflicting interests (Aktürk and
Dastgerdi, 2021). Furthermore, awareness on climate-change impact
and the potential of orphan legumes as climate-smart crops, as well as
the nutritional value of traditional dishes, can be raised through
education. Initiatives such as the CGIAR Generation Challenge
Program (https://www.generationcp.org/) have contributed to
build a new generation of breeders who vehicle cultural changes.
Multiple socioeconomic factors (gender, class, ethnicity, age,
disability) contribute to women vulnerability in rural areas (Abu-
Rabia-Queder and Morris, 2018; FAO, 2023). Prolonged and high
workload limits the access of young girls, in charge of water
collection, to school. This compromises the possibility to bridge
the gender gap in education, among the Sustainable Developmental
Goals (SDGs) targets (UNICEF, 2020; Hamlet et al., 2021).
Furthermore, climate-driven migration disrupts communities,
charging women with heavier responsibilities and economic
insecurity (Nwoke and Ibe, 2014; FAO, 2023).
Vulnerability mapping across the Mediterranean basin will face
these problems, attempting to provide an in-depth description of
the socioeconomic and climate scenarios essential for
understanding the dynamics involving human/climatic factors
and for the prediction of future expected impacts. The
multidisciplinary character of the BENEFIT-Med team will lead
to a dedicated vulnerability mapping of the Greater Mediterranean
Region (GMR), as a starting point to develop more effective
roadmaps focused on the mitigation effects resulting from the
productive introduction of target species.

## 4.3 The Mediterranean region: a climate-change hot-spot

The Mediterranean region is considered a climate-change hot-spot of the 21st century (Giorgi, 2006). In this area, global warming rates are occurring at a greater pace and temperature extremes are expected to be reached (Lionello and Scarascia, 2018). Global air temperature increases by 1.5 and 2.0°C might lead to an increase of maximum air temperatures in the order of 2.2 and 3.0°C, respectively. Projected warming rates are connected to increased heat wave intensities and more frequent heat waves (Perkins-Kirkpatrick and Gibson, 2017), leading to reduced soil moisture and increased water stress for crops during all seasons, but with larger reduction rates during winter and spring, the main planting season for orphan legumes in the GMR (Samaniego et al., 2018). The evolution of new farming systems across the GMR, based on reliable climate information, is inevitable. One of the major challenges to overcome is the identification of the impact of climate change and variability on existing and new farming systems.

A suite of regional climate projections already exists from the Coordinated Regional Climate Downscaling Experiment (CORDEX) initiative (https://cordex.org/). Through global partnerships in regional climate modelling, various regional climate models (RCMs) are driven by large-scale general circulation models (GCMs) to derive regional-scale climate information under different emission scenarios. However, these climate projections are associated with large uncertainties as well as systematic biases, which should be reduced before applying them to climate change impact assessments (Laux et al., 2021). For the quantification of devastating extreme events in the GMR, such as the joint occurrence of severe drought and heat events, more sophisticated (multivariate) methods for bias correction (BC) are necessary (Adeyeri et al., 2023). Based on BC approaches, the co-variability of the most critical climate variables can be retained (Dieng et al., 2022; Olschewski et al., 2023), allowing the mapping of crop suitability and vulnerability to climate risk under different climate change scenarios. Crop suitability mapping is based on the growing thresholds for crops in relation to climate conditions. Within the BENEFIT-Med project, the concept of climatic crop suitability will be extended by edaphic, hydrological, and topographic conditions. Suitable threshold parameters for specific orphan legumes will be derived from field experimentations and finally upscaled to the GMR. Crop vulnerability, in this context, will

be analyzed through the characterization of current and future
patterns in soil temperature and soil moisture. In fact, soil
temperature and soil moisture, besides other factors, affect seed
germination and govern stand establishment (Elias et al., 2019).

## 4.4 Organization of the available knowledge

The current knowledge on orphan legumes is still fragmented, dispersed across repositories, from which data on few species can be retrieved. This is the case of *Moringa oleifera* L. and *Vigna subterranea* L., whose genomes are accessible at ORCAE-AOCC (Online Resource for Community Annotation of Eukaryotes - African Orphan Crops Consortium) (https://bioinformatics.psb.ugent.be/orcae/aocc/), a public genome annotation resource dedicated to underutilized crops, designed to facilitate stakeholders' efforts (Yssel et al., 2019). Ideally, a globally accessible database that collects all the information on orphan legumes should be assembled and elaborated for working at multiple levels: as interface for interactions with public authorities, for dissemination/scientific/ technical activities. A data model spanning the main components of the crop value chain in the food system has been suggested by Nizar et al. (2021). Such initiatives should be expanded to orphan legumes, merging the knowledge collected within past and current research projects.

## 5 Conclusions

This review highlights the drawbacks that must be overcome before orphan legumes could reach the state of 'climate-ready crops'. The technical/social interfaces at which multiple actors play - still inadequate - roles are discussed. From the technical side, engagement of orphan legumes in climate-resilience breeding has become a priority and breeders can benefit from the current multidisciplinary approaches and high-throughput technologies to address the need of high-quality seeds. As for seed priming, an ideal roadmap should move from basic research to the translational and agricultural research domains, fishing new hallmarks of the seed response from the complex molecular pathways that showcase the pre-germinative metabolism before their validation in applied purposes. Seed systems should be reinforced by balancing the increased potential for seed quality and profitability offered by formal systems and an easier access to seeds should be ensured by community-based seed systems.

## Author contributions

ALB: Writing – review & editing, Writing – original draft, Conceptualization. CC: Writing – review & editing. AM: Writing – review & editing. AP: Writing – review & editing. PL: Writing – review & editing. HM: Writing – review & editing. LR: Writing – review & editing. ET: Writing – review & editing. DC: Writing – review & editing. CK: Writing – review & editing. LG: Writing – review
& editing. SG: Writing – review & editing. SM: Writing – review & editing. AE: Writing – review & editing. MH: Writing – review & editing. BK: Writing – review & editing. HE: Writing – review & editing. JN: Writing – review & editing. SA: Writing – review & editing. AzB: Writing – review & editing. MB: Writing – review & editing.

## Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by PRIMA (Partnership for Research and Innovation in the Mediterranean Area) Programme-H2020, Call Multi-Topic 2021, Research & Innovation Activities-RIA, Project “Boosting technologies of orphan legumes towards resilient farming systems in the Greater Mediterranean Region: from bench to open field (BENEFIT-Med) ID: 1726 (2022-2025). AP has been awarded a Post-Doctoral Fellowship in the frame of the BENEFIT-Med project.

## References

Cullis, C., Lawlor, D. W., Chimwamurombe, P., Bbebe, N., Kunert, K., and Vorster, J. (2019). Development of marama bean, an orphan legume, as a crop. *Food Energy Sec.* 8, e00164. doi: 10.1002/fes3.164

Chapman, M. A., He, Y., and Zhou, M. (2022). Beyond a reference genome: pangenomes and population genomics of underutilized and orphan crops for future food and nutrition security. *New Phytol.* 234, 1583–1597. doi: 10.1111/nph.18021

Abberton, M., Paliwal, R., Faloye, B., Marimagne, T., Moriam, A., and Oyatomi, O. (2022). Indigenous african orphan legumes: potential for food and nutrition security in SSA. *Front. Sust. Food Syst.* 6. doi: 10.3389/fsufs.2022.708124

Abu-Rabia-Queder, S., and Morris, A. (2018). Women in drylands: barriers and benefits for sustainable livelihoods. *J. Arid Environ.* 149, 1–3. doi: 10.1016/j.jaridenv.2017.11.009

Adeyeri, O. E., Zhou, W., Laux, P., Ndehedehe, C. E., Wang, X., Usman, M., et al. (2023). Multivariate drought monitoring, propagation, and projection using bias-corrected general circulation models. *Earth's Future* 11, e022EF003303. doi: 10.1029/2022EF003303

Akohoue, F., Achigan-Dako, E. G., Sneller, C., Van Deynze, A., and Sibiya, J. (2020). Genetic diversity, SNP-trait associations, and genomic selection accuracy in a west African collection of Kersting's groundnut [*Macrotyloma geocarpum* (harms) Maréchal & Baudet]. *PloS One* 15, e0234769. doi: 10.1371/journal.pone.0234769

Aktürk, G., and Dastgerdi, A. S. (2021). Cultural landscapes under the threat of climate change: a systematic study of barriers to resilience. *Sustainability* 13, 9974. doi: 10.3390/su13179974

Ali, L. G., Nulit, R., Ibrahim, M. H., and Yien, C. Y. S. (2021). Efficacy of KNO₃, SiO₂ and SA priming for improving emergence, seedling growth and antioxidant enzymes of rice (*Oryza sativa*), under drought. *Sci. Rep.* 11, 1–11. doi: 10.1038/s41598-021-83434-3

Al-Tamimi, N., Brien, C., Oakey, H., Berger, B., Saade, S., Ho, Y. S., et al. (2016). Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping. *Nat. Commun.* 7, 1–11. doi: 10.1038/ncomms13342

Bassett, A., Hooper, S., and Cichy, K. (2021). Genetic variability of cooking time in dry beans (*Phaseolus vulgaris* L.) related to seed coat thickness and the cotyledon cell wall. *Food Res. Int.* 141, 109886. doi: 10.1016/j.foodres.2020.109886

Borelli, T., Hunter, D., Padulosi, S., Amaya, N., Meldrum, G., Moura de Oliveira Beltrame, D., et al. (2020). Local solutions for sustainable food systems: the contribution of orphan crops and wild edible species. *Agronomy* 10, 231. doi: 10.3390/agronomy10020231

Bourke, P. M., Evers, J. B., Bijma, P., van Apeldoorn, D. F., Smulders, M. J. M., Kuyper, T. W., et al. (2021). Breeding beyond monoculture: putting the “intercrop” into crops. *Front. Plant Sci.* 12. doi: 10.3389/fpls.2021.734167

Brónnvik, H., and von Wettberg, E. J. (2019). Bird dispersal as a pre-adaptation for domestication in legumes: insights for neo-domestication. *Front. Plant Sci.* 10, 1293. doi: 10.3389/fpls.2019.01293

Čanak, P., Jeromela, A. M., Vujčović, B., Kiprovski, B., Mitrović, B., Alberghini, B., et al. (2020). Is drought stress tolerance affected by biotypes and seed size in the emerging oilseed crop Camelina? *Agronomy* 10, 1856. doi: 10.3390/agronomy10121856

## Conflict of interest

Author CK was employed by the company Agroland S.A.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

## Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Carrillo-Reche, J., Vallejo-Marin, M., and Quilliam, R. S. (2018). Quantifying the potential of 'on-farm' seed priming to increase crop performance in developing countries. A meta-analysis. *Agr. Sust. Dev.* 38, 64. doi: 10.1007/s13593-018-0536-0

Christie, K., Natalie, R., Pierson, N. R., Lowry, D. B., and Holeski, L. M. (2022). Local adaptation of seed and seedling traits along a natural aridity gradient may both predict and constrain adaptive responses to climate change. *Am. J. Bot.* 109, 1529–1544. doi: 10.1002/ajb2.16070

Cichy, K. A., Wiesinger, J. A., Berry, M., Nchimbi-Msolla, S., Fourie, D., Porch, T. G., et al. (2019). The role of genotype and production environment in determining the cooking time of dry beans (*Phaseolus vulgaris* L.). *Legume Sci.* 1, e13. doi: 10.1002/ leg3.13

Cradock-Henry, N. A., Diprose, G., and Frame, B. (2021). Towards local-parallel scenarios for climate change impacts, adaptation and vulnerability. *Climate Risk Manage.* 34, 100372. doi: 10.1016/j.crm.2021.100372

Cullis, C., and Kunert, K. J. (2017). Unlocking the potential of orphan legumes. *J. Exp. Bot.* 68, 1895–1903. doi: 10.1093/jxb/erw437

Dawson, I. K., Powell, W., Hendre, P., Bančič, J., Hickey, J. M., Kindt, R., et al. (2019). The role of genetics in mainstreaming the production of new and orphan crops to diversify food systems and support human nutrition. *New Phytol.* 224, 37–54. doi: 10.1111/nph.15895

de Sherbinin, A., Bukvic, A., Rohat, G., Gall, M., McCusker, B., Preston, B., et al. (2023). Climate vulnerability mapping: a systematic review and future prospects. *WIREs Climate Change* 10, e600. doi: 10.1002/wcc.600

Devika, O. S., Singh, S., Sarkar, D., Barnwal, P., Suman, J., and Rakshit, A. (2021). Seed priming: a potential supplement in integrated resource management under fragile intensive ecosystems. *Front. Sust. Food Syst.* 5. doi: 10.3389/ fsufs.2021.654001

Dieng, D., Cannon, A. J., Laux, P., Hald, C., Adeyeri, O., Rahimi, J., et al. (2022). Multivariate bias-correction of high-resolution regional climate change simulations for West Africa: Performance and climate change implications. *J Geophysical Res: Atmospheres* 127, e0201JD034836. doi: 10.1029/2021JD034836

Elias, E. H., Flynn, R., Idowu, O. J., Reyes, J., Sanogo, S., Schutte, B. J., et al. (2019). Crop vulnerability to weather and climate risk: analysis of interacting systems and adaptation efficacy for sustainable crop production. *Sustainability* 11, 6619. doi: 10.3390/su11236619

Elolu, S., Byarugaba, R., Opiyo, A. M., Nakimbugwe, D., Mithöfer, D., and Huyskens-Keil, S. (2023). Improving nutrition-sensitive value chains of African indigenous vegetables: current trends in postharvest management and processing. *Front. Sust. Food Syst.* 7. doi: 10.3389/fsufs.2023.1118021

Guo, M. W., Zhu, L., Li, H. Y., Liu, W. P., Wu, Z. N., Wang, C. H., et al. (2022) Mechanism of pod shattering in the forage legume *Medicago ruthenica*. *Plant Physiol. Biochem.* 185, 260–267. doi: 10.1016/j.plaphy.2022.06.013

FAO. (2019). *The State of the World's Biodiversity for Food and Agriculture*. Eds. J. Bélanger and D. Pilling (Rome: FAO Commission on Genetic Resources for Food and Agriculture Assessments), 572. Available at: http://www.fao.org/3/CA3129EN/ CA3129EN.pdf. pp.
FAO. (2023). (Rome). doi: 10.4060/cc5343en

Fricke, E. C., Ordonez, A., Rogers, H. S., and Svenning, J.-C. (2022). The effects of defaunation on plants' capacity to track climate change. *Science* 375, 210–214. doi: 10.1126/science.abk3510

Gholami, A., Sharafi, S., Sharafi, A., and Ghasemi, S. (2009). Germination of different seed size of pinto bean cultivars as affected by salinity and drought stress. *J. Food Agric. Environ.* 7, 555–558.

Giorgi, F. (2006). Climate change hot-spots. *Climate* 33, L08707. doi: 10.1029/2006GL025734

Global Market Insights (GMI). (2023). *Seed treatment market - By method (chemical seed treatment, biological seed treatment, physical seed treatment) by crop (corn, wheat, barley, oats, soybean, canola, sunflower), by formulation, by equipment, by function and forecast* 2023-2032. Report ID: GM15673. Available online at: https://www.gminsights.com/industry-analysis/seed-treatment-market.

Global Panel on Agriculture and Food Systems for Nutrition. (2023). *Food Systems and Diets: a Handbook of essential policies*. Available online at: https://www.glopan.org/handbook/.

Gonçalves, L., Rubiales, D., Bronze, M. R., and Vaz Patto, M. C. (2022). Grass Pea (*Lathyrus sativus* L.) - a sustainable and resilient answer to climate challenges. *Agronomy* 12, 1324. doi: 10.3390/agronomy12061324

Gonsalves, J. (2013). *A new relevance and better prospects for wider uptake of social learning within CGIAR. CCAFS Working Paper no. 37* (Copenhagen, Denmark: CGIAR Research Program on Climate Change, Agriculture and Food Security (CCAFS). Available at: https://hdl.handle.net/10568/36033.

Goufa, M., Makeroufas, E., Gerakari, M., Sarri, E., Ragkos, A., Bebeli, P. J., et al. (2024). Understanding the potential to increase adoption of orphan crops: the case of *Lathyrus* spp. cultivation in Greece. *Agronomy* 14, 108. doi: 10.3390/agronomy14010108

Greveniotis, V., Bouloumpasi, E., Zotis, S., Korkovelos, A., and Ipsilandis, C. G. (2022). Stability, the last frontier: forage yield dynamics of peas under two cultivation systems. *Plants* 11, 892. doi: 10.3390/plants11070892

Hameed, A., and Iqbal, N. (2014). Chemo-priming with mannose, mannitol and $H_2O_2$ mitigate drought stress in wheat. *Cereal Res. Commun.* 42, 450–462. doi: 10.1556/CRC.2013.0066

Hamlet, L. C., Chakrabarti, S., and Kaminsky, J. (2021). Reduced water collection time improves learning achievement among primary school children in India. *Water Res.* 203, 117527. doi: 10.1016/j.watres.2021.117527

Harris, D., Breese, W. A., and Rao, J.V.D.K.K. (2005). The improvement of crop yield in marginal environments using "on-farm" seed priming: nodulation, nitrogen fixation and disease resistance. *Aust. J. Agr. Res.* 56, 1211–1218. doi: 10.1071/AR05079

Hendre, P. S., Muthemba, S., Kariba, R., Muchugi, A., Fu, Y., Chang, Y., et al. (2019). African Orphan Crops Consortium (AOCC): status of developing genomic resources for African orphan crops. *Planta* 250, 989–1003. doi: 10.1007/s00425-019-03156-9

Hertel, T., Elouafi, I., Tanticharoen, M., and Ewert, F. (2021). Diversification for enhanced food systems. *Nat. Food* 2, 832–834. doi: 10.1038/s43016-021-00403-9

Hu, F. Q., Jiang, S. C., Wang, Z., Hu, K., Xie, Y. M., Zhou, L., et al. (2022). Seed priming with selenium: effects on germination, seedling growth, biochemical attributes, and grain yield in rice growing under flooding conditions. *Plant Direct.* 6, e378. doi: 10.1002/pld3.378

Huang, J., Ma, Q., Cai, Z., Xia, Q., Li, S., Jia, J., et al. (2020). Identification and mapping of stable QTLs for seed oil and protein content in soybean [*Glycine max* (L.) Merr.). *J. Agr. Food Chem.* 68, 6448–6460. doi: 10.1021/acs.jafc.0c01271

ICRISAT - International Crops Research Institute for the Semi-Arid Tropics. (2008). *Community-based seed production system (CBSP) in Nigeria: an opening for complementing national supply of quality seeds*. Available online at: https://www.fao.org/plant-treaty/tools/toolbox-for-sustainable-use/details/en/c/1369802/.

IPCC (Intergovernmental Panel on Climate Change). (2022). *Climate Change 2022: Mitigation of Climate Change* (Geneva: Contribution of Working Group III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change). Available at: https://www.ipcc.ch/report/sixth-assessment-report-working-group-3/.

Jaiswal, P., Sahi, A. N., and Barthakur, S. (2022). Cytokinin seed priming mediated induction of terminal heat stress tolerance and expression profiling of *SKP1* transcripts, a component of ubiquitin proteasome system in bread wheat (*Triticum aestivum* L.): a transgenerational analysis. *Plant Growth Regul.* 98, 259–280. doi: 10.1007/s10725-022-00861-6

Joshi, T., Sehgal, H., Mandal, S. K., Joshi, M., Deepa, P. R., and Sharma, P. K. (2023). Nutraceutical and flavor profiles in underutilized desert legumes of India: gene editing strategies towards sustainable food development. *J. Plant Biochem. Biotech.* 29, 1–8. doi: 10.1007/s13562-023-00836-2

Kansiime, M. K., Bundi, M., Nicodemus, J., Ochieng, J., Marandu, D., Njau, S. S., et al. (2021). Assessing sustainability factors of farmer seed production: a case of the good seed initiative project in Tanzania. *Agr. Food Sec.* 10, 1–10. doi: 10.1186/s40066-021-00289-7

Kaydan, D., and Yagmur, M. (2008). Germination, seedling growth and relative water content of shoot in different seed sizes of triticale under osmotic stress of water and NaCl. *Agr. J. Biotechnol.* 7, 2862–2868. ISSN 1684-5315. doi: 10.5897/AJB08.512

Keshavarz, H., and Moghadam, R. S. G. (2017). Seed priming with cobalamin (vitamin B12) provides significant protection against salinity stress in the common bean. *Rhizosphere* 3, 143–149. doi: 10.1016/j.rhisph.2017.04.010

Khan, M. O., Irfan, M., Muhammad, A., Ullah, I., Nawaz, S., Khalil, M. K., et al. (2022). A practical and economical strategy to mitigate salinity stress through seed priming. *Front. Environ. Sci.* 10, 991977. doi: 10.3389/fenvs.2022.991977

Kumar, V., Dwivedi, P., Kumar, P., Singh, B. N., Kumar Pandey, D., Kumar, V., et al. (2021). Mitigation of heat stress responses in crops using nitrate primed seeds. *South Afr. J. Bot.* 140, 25–36. doi: 10.1016/j.sajb.2021.03.024

Kumar, B., Singh, A. K., Bahuguna, R. N., Pareek, A., and Singla-Pareek, S. L. (2023). Orphan crops: a genetic treasure trove for hunting stress tolerance genes. *Food Energy Sec.* 12, e436. doi: 10.1002/fes3.436

Laux, P., Rotter, R. P., Webber, H., Dieng, D., Rahimi, J., Wei, J., et al. (2021). To bias correct or not to bias correct? An agricultural impact modelers' perspective on regional climate model data. *Agr. For. Met.* 304-305, 108406. doi: 10.1016/j.agrformet. 2021.108406

Li, X., and Siddique, K. H. M. (2018). *Future Smart Food: rediscovering hidden treasures of neglected and underutilized species for Zero Hunger in Asia* Vol. 242 (Bangkok: FAO). doi: 10.18356/23b5f7ab-en

Lionello, P., and Scarascia, L. (2018). The relation between climate change in the Mediterranean region and global warming. *Reg. Environ. Change* 18, 1481–1493. doi: 10.1007/s10113-018-1290-1

Liu, X., Quan, W., and Bartels, D. (2022). Stress memory responses and seed priming correlate with drought tolerance in plants: an overview. *Planta* 255, 45. doi: 10.1007/s00425-022-03828-z

Liu, X., Zhang, H., Qin, S., Wang, Q., Yang, X., and Wang, K. (2019). Optical fiber amplifier for quantitative and sensitive point-of-care testing of myoglobin and miRNA-141. *Bios. Bioelectr.* 129, 87–92. doi: 10.1016/j.bios.2018.12.056

Lo, S., Muñoz-Amatriain, M., Hokin, S. A., Cisse, N., Roberts, P. A., Farmer, A. D., et al. (2019). A genome-wide association and meta-analysis reveal regions associated with seed size in cowpea [*Vigna unguiculata* (L.) Walp]. *Theor. Appl. Gen.* 132, 3079–3087. doi: 10.1007/s00122-019-03407-5

Louis, N., Dankher, O. P., and Manicad, G. (2022). Seed systems resilience - An overview. *Seeds* 1, 340–356. doi: 10.3390/seeds1040028

Louwaars, N. P., and Manicad, G. (2022). Seed systems resilience - An overview. *Seeds* 1, 340–356. doi: 10.3390/seeds1040028

Lv, M.-J., Wan, W., Yu, F., and Meng, L.-S. (2019). New insight into the molecular mechanisms underlying seed size control under drought stress. *J. Agr. Food Chem.* 67, 9697–9704. doi: 10.1021/acs.jafc.9b02497

Martínez-López, M., Tinoco-Ojanguren, C., and Martorell, C. (2020). Drought tolerance increases with seed size in a semiarid grassland from southern Mexico. *Plant Ecol.* 221, 989–1003. doi: 10.1007/s11258-020-01056-7

Mut, Z., and Akay, H. (2010). Effect of seed size and drought stress on germination and seedling growth of naked oat [*Avena sativa* L.]. *Bulg. J. Agric. Sci.* 16, 459–467.

Neha, T., Mohapatra, S., Sirhindi, G., and Dogra, V. (2022). Seed priming with brassinolides improves growth and reinforces antioxidative defenses under normal and heat stress conditions in seedlings of *Brassica juncea*. *Physiol. Plant* 174, e13814. doi: 10.1111/ppl.13814

Ngcamu, B. S. (2023). Climate change effects on vulnerable populations in the Global South: a systematic review. *Natural Hazards* 118, 977–991. doi: 10.1007/s11069-023-06070-2

Nizar, N. M. M., Jahanshiri, E., Tharmandram, A. S., Salama, A., Sinin, S. S. M., Abdullah, N. J., et al. (2021). Underutilised crops database for supporting agricultural diversification. *Comp. Electr. Agr.* 180, 105920. doi: 10.1016/j.compag.2020.105920

Nwoke, E. A., and Ibe, S. N. O. (2014). Climate change impact on the health of African women and adaptation strategies. *Int. J. Global Warm Climate Change* 1, 15–23.

Ogbole, O. O., Akin-Ajani, O. D., Ajala, T. O., Ogunniyi, Q. A., Fettke, J., and Odeku, O. A. (2023). Nutritional and pharmacological potentials of orphan legumes: Subfamily faboideae. *Heliyon* 9, e15493. doi: 10.1016/j.heliyon.2023.e15493

Ohanenye, I. C., Ekezie, F.-G. C., Sarteshnizi, R. A., Boachie, R. T., Emenike, C. U., Sun, X., et al. (2022). Legume seed protein digestibility as influenced by traditional and emerging physical processing technologies. *Foods* 11, 2299. doi: 10.3390/foods11152299

Ojiewo, C. O., Rubyogo, J. C., Wesonga, J. M., Bishaw, Z., Gelalcha, S. W., and Abang, M. M. (2018). *Mainstreaming efficient legume seed systems in Eastern Africa: challenges, opportunities and contributions towards improved livelihoods* (Rome: FAO), 72. ppLicense: CC BY-NC-SA 3.0 IGO.

Olschewski, P., Dieng, M. D. B., Moutahir, H., Böker, B., Haas, E., Kunstmann, H., et al. (2023). Amplified potential for vegetation stress under climate change-induced intensifying compound extreme events in the Greater Mediterranean Region. *Nat. Hazards Earth Syst. Sci. Discuss.* 24, 1099–1134. doi: 10.5194/nhess-2023-129

Oluwole, O. O., Olomitutu, O. E., Paliwal, R., Oyatomi, O. A., Abberton, M. T., and Obembe, O. O. (2021). Preliminary assessment of the association between DArT-SEQ SNP and some nutritional traits in African yam bean. *Trop. J. Nat. Prod. Res.* 4, 877–879. doi: 10.26538/tjnpr/vlii4.5
Pagano, A., Bontà, V., Calvio, C., Macovei, A., Pinna, F. Bedotto, N., et al. (2023b). "From bench to field: scaling up seed priming technology on orphan legumes of the Mediterranean Area," in *14th Biennial ISSS Conference - Challenges of Seed Science in a Changing Word, Book of Abstract*. 168. Available at: https://iss2023.sciencesconf.org/.

Pagano, A., Macovei, A., and Balestrazzi, A. (2023a). Molecular dynamics of seed priming at the crossroads between basic and applied research. *Plant Cell Rep.* 42, 657–688. doi: 10.1007/s00299-023-02988-w

Parker, T. A., Berny Mier y Teran, J. C., Palkovic, A., Jernestedt, J., and Gepts, P. (2021). Pod indehiscence is a domestication and aridity resilience trait in common bean. *New Phytol.* 225, 558–570. doi: 10.1111/nph.16164

Perkins-Kirkpatrick, S. E., and Gibson, P. B. (2017). Changes in regional heatwave characteristics as a function of increasing global temperature. *Sci. Rep.* 7, 12256. doi: 10.1038/s41598-017-12520-2

Popoola, J. O., Aworunse, O. S., Ojuederie, O. B., Adewale, B. D., Ajani, O. C., Oyatomi, O. A., et al. (2022). The exploitation of orphan legumes for food, income, and nutrition security in Sub-Saharan Africa. *Front. Plant Sci.* 13. doi: 10.3389/fpls.2022.782140

Powers, S. E., and Thavarajah, D. (2019). Checking agriculture's pulse: field pea (*Pisum Sativum* L.), sustainability, and phosphorus use efficiency. *Front. Plant Sci.* 10. doi: 10.3389/fpls.2019.01489

Pravisya, P., and Jayaram, K. M. (2015). Priming of *Abelmoschus esculentus* (L.) Moench (okra) seeds with liquid phosphobacterium: an approach to mitigate drought stress. *Soc Trop. Plant Res.* 2, 276–281. ISSN (E): 2349-1183.

Rajjou, L., Duval, M., Gallardo, K., Catusse, J., Bally, J., Job, C., et al. (2012). Seed germination and vigor. *Annu. Rev. Plant Biol.* 63, 507–533. doi: 10.1146/annurev-arplant-042811-05550

Ramya, K. R., Tripathi, K., Pandey, A., Barpete, S., Gore, P. G., Raina, A. P., et al. (2022). Rediscovering the potential of multifaceted orphan legume grasspea - a sustainable resource with high nutritional values. *Front. Nutr.* 8. doi: 10.3389/fnut.2021.826208

Roorkiwal, M., Pandey, S., Thavarajah, D., Hemalatha, R., and Varshney, R. K. (2021). Molecular mechanisms and biochemical pathways for micronutrient acquisition and storage in legumes to support biofortification for nutritional security. *Front. Plant Sci.* 12, 682842. doi: 10.3389/fpls.2021.682842

Saastamoinen, M., Bocedi, G., Cote, J., Legrand, D., Guillaume, F., Wheat, et al. (2018). Genetics of dispersal. *Biol. Rev. Cambridge Phil. Soc* 93, 574–599. doi: 10.1111/brv.12356

Sadeghi, H., and Robati, Z. (2015). Response of *Cichorium* intybus L. to eight seed priming methods under osmotic stress conditions. *Biocatal. Agric. Biotechnol.* 4, 443–448. doi: 10.1016/j.bcab.2015.08.003

Saha, D., Choyal, P., Mishra, U. N., Dey, P., Bose, B., Prathibha, M. D., et al. (2022). Drought stress responses and inducing tolerance by seed priming approach in plants. *Plant Stress* 4, 100066. doi: 10.1016/j.stress.2022.100066

Samaniego, L., Thober, S., Kumar, R., Wanders, N., Rakovec, O., Pan, M., et al. (2018). Anthropogenic warming exacerbates European soil moisture droughts. *Nat. Climate Change* 8, 421–426. doi: 10.1038/s41558-018-0138-5

Santos, C. S., Carbas, B., Castanho, A., Bronze, M. R., Serrano, C., Vasconcelos, M. W., et al. (2018). Relationship between seed traits and pasting and cooking behaviour in a pulse germplasm collection. *Crop Past. Sci.* 69, 892–903. doi: 10.1071/CP18205

Shaffique, S., Imran, M., Kang, S. M., Khan, M. A., Asaf, S., Kim, W. C., et al. (2023). Seed bio-priming of wheat with a novel bacterial strain to modulate drought stress in Daegu, South Korea. *Front. Plant Sci.* 14. doi: 10.3389/fpls.2023.1118941

Singh, V. K., Singh, R., Tripathi, S., Devi, R. S., Srivastava, P., Singh, P., et al. (2020). “Seed priming: state of the art and new perspectives in the era of climate change,” in *Climate change and soil interactions*. Eds. M. N. P. Prasad and M. Pietrzykowski (Elsevier), 143–170.

Srivastava, S., Tyagi, R., and Sharma, S. (2024). Seed biopriming as a promising approach for stress tolerance and enhancement of crop productivity: a review. *J. Sci. Food Agr.* 104, 1244–1257. doi: 10.1002/jsfa.13048

Tabassum, T., Farooq, M., Ahmad, R., Zohaib, A., Wahid, A., and Shahid, M. (2018). Terminal drought and seed priming improves drought tolerance in wheat. *Physiol. Mol. Biol. Plants* 24, 845–856. doi: 10.1007/s12298-018-0547-y

Tadele, Z. (2019). Orphan crops: their importance and the urgency of improvement. *Planta* 250, 677–694. doi: 10.1007/s00425-019-03210-6

Talabi, A. O., Vikram, P., Thushar, S., Rahman, H., Ahmadzai, H., Nhamo, N., et al. (2022). Orphan crops: a best fit for dietary enrichment and diversification in highly deteriorated marginal environments. *Front. Plant Sci.* 13. doi: 10.3389/fpls.2022.839704

Tamindžić, G., Azizbekian, S., Miljaković, D., Turan, J., Nikolić, Z., Ignjatov, M., et al. (2023). Comprehensive metal-based nanopriming for improving seed germination and initial growth of field pea (*Pisum sativum* L.). *Agronomy*. 13, 2932. doi: 10.3390/agronomy13122932

Tounekti, T., Mahdhi, M., Zarraq, A. F., and Khemira, H. (2020). Priming improves germination and seed reserve utilization, growth, antioxidant responses and membrane stability at early seedling stage of Saudi sorghum varieties under drought stress. *Notulae Bot. Horti Agrobot.* *Cluj-Napoca* 48, 938–953. doi: 10.15835/nbha48211841

UNICEF. (2020). *Gender and education* (New York: United Nations). Available at: https://data.unicef.org/topic/gender/gender-disparities-in-education.

Upadhyaya, H. D., Bajaj, D., Das, S., Kumar, V., Gowda, C. L. L., Sharma, S., et al. (2016). Genetic dissection of seed-iron and zinc concentrations in chickpea. *Sci. Rep.* 6, 24050. doi: 10.1038/srep24050

Vaz Patto, M. C., and Rubiales, D. (2014). *Lathyrus* diversity: available resources with relevance to crop improvement - *L. sativus* and *L. cicera* as case studies. *Ann. Bot.* 113, 895–908. doi: 10.1093/aob/mcu024

Vernooy, R., Rana, J., Otieno, G., Mbozi, H., and Shrestha, P. (2022). Farmer-led seed production: community seed banks enter the national seed market. *Seeds* 1, 164–180. doi: 10.3390/seeds1030015

Visuvanathan, T., Than, L. T. L., Stanslas, J., Chew, S. Y., and Vellasamy, S. (2022). Revisiting *Trigonella foenum-graecum* L.: pharmacology and therapeutic potentialities. *Plants* 11, 1450. doi: 10.3390/plants11111450

Weissmann, E. A., Yadav, R. N., Seth, R., and Udaya Bhaskar, K. (2023). “Principles of variety maintenance for quality seed production,” in *Seed Science and Technology*. Eds. M. Dadlani and D. K. Yadava (Springer, Singapore). doi: 10.1007/978-981-19-5888-5_8

Westengen, O. T., Dalle, S. P., and Mulesa, T. H. (2023). Navigating toward resilient and inclusive seeds systems. *Proc. Nat. Acad. Sci. U.S.A.* 120, e2218777120. doi: 10.1073/pnas.2218777120

Xiong, W., Reynolds, M., and Xu, Y. (2022). Climate change challenges plant breeding. *Curr. Opin. Plant Biol.* 70, 102308. doi: 10.1016/j.pbi.2022.102308

Xu, W., Wu, D. I., Yang, T., Sun, C., Wang, Z., Han, B., et al. (2021). Genomic insights into the origin, domestication and genetic basis of agronomic traits of castor bean. *Genome Biol.* 22, 113. doi: 10.1186/s13059-021-02333-y

Yssel, A. E., Kao, S.-M., Van de Peer, Y., and Sterck, L. (2019). ORCAE-AOCC: a centralized portal for the annotation of African orphan crop Genomes. *Genes* 10, 950. doi: 10.3390/genes10120950

Zenda, T., Liu, S., Dong, A., Li, J., Wang, Y., Liu, X., et al. (2021). Omics-facilitated crop improvement for climate resilience and superior nutritive value. *Front. Plant Sci.* 12. doi: 10.3389/fpls.2021.774994

Zheng, M., Tao, Y., Hussain, S., Jiang, Q., and Peng, S. (2016). Seed priming in dry direct-seeded rice: consequences for emergence, seedling growth and associated metabolic events under drought stress. *Plant Growth Regul.* 78, 167–178. doi: 10.1007/s10725-015-0083-5

Zurek, M., Hebinck, A., and Selomane, O. (2022). Climate change and the urgency to transform food systems. *Science* 376, 1416–1421. doi: 10.1126/science.abo2364