Sainfoin (Onobrychis viciifolia) a legume with great ecological and agronomical potential under climate change

The Journal of Agricultural Science cambridge.org/ags Crops and Soils Review Cite this article: Sakhraoui A, Ltaeif HB, Sakhraoui A, Villalba JJ, Castillo JM, Rouz S (2024). Sainfoin (Onobrychis viciifolia) a legume with great ecological and agronomical potential under climate change. The Journal of Agricultural Science 162, 307–331. https:// doi.org/10.1017/S0021859624000327 Received: 23 November 2023 Revised: 25 June 2024 Accepted: 3 August 2024 Keywords: crop yield; global warming; nutraceutical properties; sainfoin; stress tolerance Corresponding author: Anis Sakhraoui; Email: [email protected] © The Author(s), 2024. Published by Cambridge University Press. This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial licence (http://creativecommons.org/licenses/ by-nc/4.0), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original article is properly cited. The written permission of Cambridge University Press must be obtained prior to any commercial use. Sainfoin (Onobrychis viciifolia) a legume with great ecological and agronomical potential under climate change Anis Sakhraoui1,2,3 , Hela B. Ltaeif2, Asma Sakhraoui4,5, Juan J. Villalba6, Jesús M. Castillo3and Slim Rouz2 1 Higher School of Agriculture of Kef, University of Jendouba, Le Kef, Tunisia; 2 Department of Agricultural Production –Laboratory of Agricultural Production Systems and Sustainable Development (SPADD), LR03AGR02, Higher School of Agriculture of Mograne, Carthage University, Mograne, Zaghouan, Tunisia; 3 Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Sevilla, Spain; 4 Higher Institute of Biotechnology of Beja, University of Jendouba, Beja, Tunisia; 5 Centro de Investigação de Montanha (CIMO), Instituto Politécnico de Bragança, Campus de Santa Apolónia, Bragança, Portugal and 6 Department of Wildland Resources, Utah State University, Logan, UT, USA Abstract Climate change is a global challenge to ecosystem services, altering crop yields and food security worldwide. In the context of climate change, Onobrychis viciifolia Scop. (sainfoin) can offer a multitude of ecosystem services conferred by its multifaceted beneficial properties. We reviewed the morphological, biochemical and physiological responses to environmental stressors of O. viciifolia, summarized its ecological, agronomic, nutritional and biological interests, and we discussed its use under climate change. Onobrychis viciifolia is a hemicryptophyte forage legume adapted to arid and semiarid regions by evolving a diverse array of protective mechanisms against abiotic stressors at morphological, biochemical and physiological levels. In the present scenario of climate change, O. viciifolia has desirable forage characteristics such as high nutritive value, high voluntary intake and palatability to grazing animals, leading to satisfying animal performance for milk, meat, honey and wool production. Recent studies suggest that O. viciifolia has several highly beneficial phytochemical properties including condensed tannins and polyphenol content, which have been demonstrated to have anthelmintic activities, enhance protein utilization, and prevent bloating. In addition, O. viciifolia also has the potential to reduce greenhouse gas emissions and sequestrate atmospheric carbon and nitrogen into the soil. Ethnobotanical investigations show that O. viciifolia possesses antimicrobial, antiseptic and vulnerary activities. This review could be helpful for understanding of O. viciifolia characteristics, interests and uses, thus promoting its reasonable cultivation under a changing climate. Introduction Global climate change has become a compelling environmental problem as it is hindering the yield performance of crops due to increasing environmental stresses including pest diseases and extreme climatic events (Jiang et al., 2016; Zhang et al., 2019a; Bakala et al., 2021; Skendžićet al., 2021). In addition, climate change may exacerbate soil erosion (Lal, 2012) and cause disturbances to ecosystem functions (van der Geest et al., 2019). Ecosystems functions are the respective direct and indirect benefits arising from the ecological functioning of healthy productive ecological systems (Millennium Ecosystem Assessment, 2005; Beaumont et al., 2007). Crop yields are projected to decline through the 21st century (Zinyengere et al., 2013; Petersen, 2019) and there is a need to identify and characterized perennial forage legumes that would be able to stand high environmental stress levels while offering relatively high agronomic production (Seo and Mendelsohn, 2008; Komainda et al., 2019). Moreover, ecological restoration of degraded lands is included in the array of adaptation and mitigation responses to climate change (Harris et al., 2006;O’Mara, 2012; Simonson et al., 2021). The genus Onobrychis Miller (Fam. Fabaceae) comprises a few agronomically known forage legume species such as O. transcaucasica Grossh., O. arenaria (Kit.) DC. and O. viciifolia Scop. (sainfoin), the most commonly cultivated species of the genus (Lock, 2005; Mabberley, 2008; Amirahmadi et al., 2014). Onobrychis viciifolia has a long history of traditional cultivation in Europe, Asia and North America in the 19th and 20th centuries (Miller and Hoveland, 1995; Frame et al., 1998). Indeed, its cultivation decline started in the middle of the 20th century due to the adoption of more intensive farming methods with the introduction of relatively low-cost nitrogen (N) fertilizers (Carbonero et al., 2011). Consequently, O. viciifolia cultivation was gradually displaced by alfalfa (Medicago sativa L.) and clover species (Trifolium spp.) whose https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press higher yields and easier establishment made them more desirable to farmers. Onobrychis viciifolia can be cultivated in multitude soils and climatic conditions (Tufenkci et al., 2006; Carbonero et al., 2011; Yin et al., 2020). Agronomically, O. viciifolia have positive characteristics such as a deep tap root that allows it to be very tolerant to drought (Irani et al., 2015a,2015b; Malisch et al., 2016) and N fixation up to 168 kg N 2 /ha via symbiosis with rhizobia (Malisch et al., 2017). Culture trials of O. viciifolia under harsh climatic conditions of dry areas in the Middle East and North Africa (MENA) region gave promising results (Le Houérou, 1969; Jafari et al., 2014;Sayaret al., 2022). In addition, O. viciifolia is also particularly valued for its content of condensed tannins, which have been shown to improve animal growth and health (Waghorn, 2008; Girard et al., 2016). The Mediterranean Basin has been identified as one of the most climate-vulnerable regions and a climate change ‘hotspot’(Salvia et al., 2021). In addition, the Mediterranean Basin is one of the areas with the most serious soil degradation and desertification rates in the world, reaching critical limits for its ability to provide ecosystem services and land productivity (Ferreira et al., 2022). In this sense, the large-scale grassland degradation in Mediterranean Basin aggravates the shortage of forage supply (Ferreira et al., 2022; Soares et al., 2022). Consequently, restoring degraded grasslands and increasing forage grass supply are urgent needs in this area, but the forage quality of O. viciifolia has not been deeply studied in the Mediterranean Basin. Additionally, O. viciifolia has obvious application advantages in soil and vegetation restoration that should be also analysed in detail in the Mediterranean Basin. The study of O. viciifolia has regained interest in recent decades (Fig. 1) and four studies have reviewed its cultivation and agronomic potential (Carbonero et al., 2011; Bhattarai et al., 2016; Mora-Ortiz and Smith, 2018;Sheppardet al., 2019). However, no work has focussed on the role of O. viciifolia in the present scenario of climate change. In this work, we review the geographical distribution, main functional traits, stress tolerance and beneficial proprieties for humans of O. viciifolia under the ongoing climate change scenario. Our review is meant to provide information on the importance of O. viciifolia for its possible utilization in cropping systems in a changing environment. Also, it is an attempt to recognize the lesserexplored aspects and knowledge gaps in the research on O. viciifolia. Methods Google Scholar, Web of Science, Springer and PubMed databases were used to search for published literature on O. viciifolia. The filtering was based on titles, abstracts and keywords including the words Hedysarum onobrychis L., Onobrychis sativa Lam., Onobrychis viciaefolia Scop. and O. viciifolia Scop. or sainfoin. Afterwards, the full text of all peer reviewed articles, books, book chapters and PhD thesis were reviewed. The deadline for the literature selected was up to July 2024. The Plant List (http://www.theplantlist.org/tpl1.1/search?q=Onobrychis+viciifolia), International Plant Name Index (https://www.ipni.org/n/510168-1), Kew Botanical Garden (https://powo.science.kew.org/taxon/urn:lsid: ipni.org:names:510168-1) and Global Biodiversity Information Facility (https://www.gbif.org/fr/species/2972595) were used for validating the scientific name as well as information on cultivars and the species synonyms. Origin and distribution Onobrychis viciifolia is derived from the natural hybridization between O. arenaria and O. montana (Falistocco, 1991), which are native to Central-Southern Europe, and temperate Southwest Asia and North Africa, respectively (Angevain and Prosperi, 1995; Jin et al., 2021). Onobrychis viciifolia is mostly tetraploid, through there are reports of diploid accessions (Carbonero et al., 2013). In addition, Abou-El-Enain (2002) reported the appearance of 2n= 22, 27, 28 and 29 chromosomes that demonstrated the role of aneuploid alterations in the evolution of this species. AfewOnobrychis taxa, such as O. viciifolia, have been cultivated for hundreds of years as forage and ornamental crops in warm and temperate regions of Europe, Asia and North Figure 1. Evolution of annual number of publications on Onobrychis species and O. viciifolia published from 1963 to 2024 (Sources: Google Scholar, Web of Science, Springer and PubMed). 308 Anis Sakhraoui et al. https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press America (Lock and Simpson, 1991; Yakovlev et al., 1996; Mabberley, 1997; Frame et al., 1998; Frame, 2005; Carbonero et al., 2011)(Fig. 2). Cultivated Onobrychis species were introduced to Central Europe from the Mediterranean Basin during the 16th century (Piper, 1924; Burton and Curley, 1968). Onobrychis cultivation was introduced to North America in 1786 (Bhattarai et al., 2016), but was only grown occasionally until the 1960s, when improved varieties allowed wider cultivation. Today, O. viciifolia is cultivated mainly in Eastern Europe, Iran and around the Mediterranean Basin (Eken et al., 2004; Avci et al., 2014; Bolat, 2019). The Mediterranean Basin is one of the most affected regions by climate change (Cammarano et al., 2019). One of the most relevant consequences of climate change is certainly water scarcity, as result of a reduction of surface runoff and groundwater levels (Noto et al., 2023). Onobrychis viciifolia once represented an important forage legume in semiarid environments of Italy, but its cultivation area has decreased from 160 to 9 thousand ha from 1983 to 2013 (ISTAT, 2013). It is recorded that more than 150 tonnes of seeds were sold every year in the late 1950s in the UK, enough for cropping 2500 ha (Hill, 1997). In the late 1970s, only approximately 150 ha were cropped. Today, O. viciifolia has become rare in the UK, and this is due, in part, to its poor response to the changing requirements and circumstance of British agriculture (Hutchinson, 1966). Onobrychis viciifolia could potentially be grown on 950 thousand ha in England and Wales, where the soil is sufficiently alkaline (Doyle et al., 1984). On the other hand, Wang et al. (2018) mentioned O. viciifolia as a major fodder grass species cultivated in Gansu Province, Northwest China, in 2016. Responses to environmental stressors Biotic stressors Ongoing climate change poses considerable threats to sustainable food security, including increased number of generations of pests and plant pathogens resulting from a compressed life cycle due to a warmer climate combined to elevated CO 2 concentrations, increased risk of invasion by migratory pests and reduced effectiveness of biological control (Skendžićet al., 2021). As climate change exacerbates the pest problem, there is a great need for future pest management strategies (Wei et al., 2020). Onobrychis viciifolia is relatively resistant to most common pests and diseases in Western Canada and Northern Europe compared with other legumes such as M. sativa (Goplen et al., 1991; Frame et al., 1998). This has been attributed to the presence of a range of secondary metabolites, such as tannins and polyphenols, within the foliage of O. viciifolia (Malisch et al., 2016). Even so, O. viciifolia can be damaged by fungal diseases related to certain Fusarium, Stemphyllium and Sclerotinia species (Mathre, 1968). In addition, an important number of insect and nematode species can damage O. viciifolia stands (Mathre, 1968; Wallace, 1968; Morrill et al., 1998). But O. viciifolia is resistant to the alfalfa weevil (Hypera postica Gyll.), so it can be an alternative forage legume to M. sativa in areas where this pest causes severe damage (Morrill et al., 1998; Böttger et al., 2013). Onobrychis viciifolia is relatively resistant and free from serious pest and disease problems compared with other legumes such as M. sativa (Goplen et al., 1991). Medicago sativa suffers from several economically important insect pests such as H. postica and Figure 2. Centenary evolution of worldwide geographical distribution of Onobrychis viciifolia (88.635 occurrences) from 1600 to 2024. The colours from yellow to orange represent the density of occurrence for a given area. Source: Global Biodiversity Information Facility, https://www.gbif.org/ The Journal of Agricultural Science 309 https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press Acyrthosiphon pisum, which do not affect O. viciifolia. This could encourage farmers to grow O. viciifolia as an alternative solution to M. sativa (Morrill et al., 1998). Two closely related species to H. postica (Phytonomus farinosus and Hypera trilineata) are mentioned as pests of O. viciifolia in some European countries (Wallace, 1968). Other pests such as Empoasca fabae,Lygus elisus, L. hesperus and Adelphocoris lineolatus appeared to have marginal effects on O. viciifolia and occurs only in localized areas (Morrill et al., 1998). Furthermore, only one pest (Sitona scissifrons), which feed on the roots of O. viciifolia, has been observed on accessions growing in United Kingdom, but there were no accessions that were severely affected (Carbonero et al., 2011). Adult S. scissifrons weevils become active in the field in June and eat the edges of the leaves of O. viciifolia, leaving characteristic notches along the leaves in Montana (USA). This damage could be disastrous at the seedling stage in the field (Wallace, 1968). Other members from this genus, including S. lineata,S. calloso and S. crinite, have been reported to cause minor damage in O. viciifolia in Europe (Wallace, 1968). However, Contarinia onobrychidis and Eurytoma onobrychidis represent a serious pest for O. viciifolia in some areas of Europe (Wallace, 1968). Other insects can also damage the seed production of O. viciifolia in Europe but marginally; these include Perrisia onobrychidis,Apion pisi,Odontothrips intermedius, Otiorhynchus ligustici and Melanotus erythropus. Therefore, the inclusion of O. viciifolia as a rotation component could affect the presence of host-specific pests by disturbing their life cycle. Abiotic stressors Climate change is increasing the frequency and intensity of abiotic stress combinations that pose a serious threat to crop productivity (Zandalinas et al., 2022). Onobrychis viciifolia have evolved a diverse array of protective mechanisms against abiotic stressors at biochemical and physiological levels related to hormone homoeostasis, transcriptional factors, photosynthesis, and the biosynthesis of antioxidants and osmotic adjustment-related substances (Yin et al., 2021). Consequently, O. viciifolia tolerates low nutrient conditions (Carbonero et al., 2011), high levels of active lime in the soil (De Falco et al., 2000a,2000b), drought and alkalinity, and saline-alkaline stress (Fig. 3). In addition, O. viciifolia tolerates high concentrations of lead and copper (Beladi et al., 2011) and can grow in coal mined areas (Roy et al., 2021). Moreover, O. viciifolia can grow under seasonally cold and hot climatic conditions (Sengul, 2003; Tufenkci et al., 2006), and extreme climatic conditions at high altitudes (Yin et al., 2020,2021). Rhizobia have the potential to be used in improving symbiotic N fixation on O. viciifolia under cold stress (Prévost et al., 2003). Climate change can affect the intensity and frequency of precipitation (Feng et al., 2019) and worsen ozone pollution over many populated regions, with larger impacts at higher concentrations (East et al.,2024). It has long been observed that the environmental gamma-ray dose rate increases noticeably during precipitation intervals (Mercier et al.,2009). Onobrychis viciifolia tolerates high levels of gamma radiation (Beyaz et al., 2016), but its growth is reduced after ozone exposure (Bungener et al., 1999). Salt tolerance Salt is one of the main abiotic stresses affecting crop yields around the world (Zörb et al., 2019). Seed germination is one of the most sensitive physiological phenomena to stress in the lifecycle of plants (Al-Turki et al., 2022), and seeds of O. viciifolia withstand moderate saline environments (up to 400 mM). In this sense, seeds of O. viciifolia retain germinability under high salinity, displaying tolerance mechanisms such as physiological dormancy till the occurrence of favourable conditions (Li et al., 2021a,2021b). Karamian and Ataei-Barazande (2013) reported decreasing germination rates in O. viciifolia with increasing salinity levels over 200 mM NaCl and indicated that germination was totally inhibited at 400 mM NaCl which is higher than for Trifolium repens L. (up to 180 mM) (Chu et al., 2022), Trifolium pratense L. (up to 240 mM) (Asci, 2011) and M. sativa (up to 257 mM) (Kadri et al., 2021). The germination of O. viciifolia is considered more tolerant to salinities c. 170 mM NaCl than other Onobrychis species (Uzun et al., 2017). Saline-alkaline conditions resulted in oxidative stress and the accumulation of proline in seedlings of O. viciifolia (Wu et al., 2021). Along with organic osmolytes, O. viciifolia under salinity also increased the production of reactive oxygen species (ROS) scavengers such as catalase, superoxide dismutase, glutathione reductase and ascorbate peroxidase (Beyaz, 2019). In fact, O. viciifolia can grow without much yield and quality loss in salt-affected areas (c. 109 mM NaCl), where it can provide enough highquality forage production for livestock without altering its macro-mineral content (Temel et al., 2016a,2016b)(Fig. 3a). Nonetheless, Wu et al.(2017a,2017b) reported reduced growth and chlorophyll and water contents, diminished root potassium concentration, and increased malondialdehyde (MDA) concentration and relative membrane permeability in O. viciifolia shoots under salinity (100 mM NaCl). This study also reported that, when supplied exogenously, proline and silicon improved salt stress tolerance in O. viciifolia by mitigating sodium toxicity (Fig. 3a). Under salinity, O. viciifolia maintain better cellular function and overall physiological homoeostasis evidenced by less drastic imbalance in intracellular Na + /K + ratio than M. sativa (Li et al., 2010;Beyaz2019) which is one of the key determinants of plant salt tolerance under climate change (El Sabagh et al., 2021). Drought tolerance Drought is the largest contributor to world-wide crop losses (Lesk et al., 2016; Santos-Medellín et al., 2021). In this general context that is exacerbated by climate change (Cook et al., 2018), O. viciifolia produces indehiscent fruits (pods) that break down slowly, promoting seed survivorship during drought periods (Majidi and Barati, 2011; Avci and Kaya, 2013). In this sense, organic, hydrogel and mineral seed coating improved germination speed of O. viciifolia with and without drought (Mehrabi and Chaichi, 2012). Contradictorily, Kintl et al.(2021) showed that O. viciifolia did not respond positively to the seed coating under drought. Uncoated seeds exhibited a greater drought resistance than the coated seeds which showed a sharp, significant decline of germination capacity and a great increase in the dead seed percentage due to the death of a fraction from the hard seeds. Nasirzadeh et al.(2005) reported that O. viciifolia can be considered as a semi-resistant species to drought. Adult plants of O. viciifolia tolerate exposure to the combined effects of drought and ozone (Bungener et al., 1999). The response mechanisms of O. viciifolia to drought include osmotic adjustment (Dehabadi, 1997; Irani et al., 2015a,2015b; Beyaz, 2019;Beyaz and Yildiz, 2021), ROS scavenging, reduced transpiration (Roy et al., 2021), increasing stomatal resistance and water use efficiency (Dehabadi et al., 1993a,1993b; Dehabadi, 1997; Huang 310 Anis Sakhraoui et al. https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press Figure 3. Summary of the main tolerance mechanisms of Onobrychis viciifolia to (a) salinity and (b) drought stress. The Journal of Agricultural Science 311 https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press et al., 2020), and increasing carotenoid contents with decreasing chlorophyll contents (Irani et al., 2015a,2015b). In addition, O. viciifolia tolerance to drought involves also morphological adaptations such as a deep root system (Koch et al., 1972; Dehabadi, 1997; March-Salas et al., 2021) and reduced leaf area (Dehabadi et al., 1993b). Besides all its responses to drought, O. viciifolia shows reduced plant heights which resulted in significant yield losses when exposed to severe drought (Irani et al., 2015a,2015b). In this sense, Bolger and Matches (1990) found a higher yield potential for O. viciifolia in spring than in summer, possibly indicating higher water use efficiency. To tide over periodic drought stress, Malisch et al.(2016) highlighted the importance of harvesting at optimal stages to have good forage performance for O. viciifolia. Onobrychis viciifolia have greater ability to resist drought and adapt to dry habitats compared to several forage species. Considering the field capacity as the upper limit of soil water availability, O. viciifolia had the widest range of adaptability to soil water compared to other crop species such as Astragalus adsurgens, Elymus nutans and Lolium multiflorum (Huang et al., 2020). Moreover, O. viciifolia exhibited a lower average lower limit of relative soil water content compared to A. adsurgens,E. nutans, and L. multiflorum. In addition, O. viciifolia closed stomata more rapidly with the decrease of relative soil water content, suggesting that the species had better drought resistance and allowed plants to keep water in plant tissues (Huang et al., 2020). The intrinsic water use efficiency (WUE i ) represents an important indicator of the adaptability for higher plants to climate change (Weiwei et al., 2018). WUEi increased more rapidly in O. viciifolia than the other three forage under moderate water deficit (Huang et al., 2020). High temperatures tolerance Onobrychis viciifolia is an alternative forage for semi-arid regions, where M. sativa and Trifolium sp. cannot be sown. Although there is little published data, there is considerable observational evidence that O. viciifolia is tolerant to relatively high temperatures. Maximum air temperatures of above 32°C did not affect O. viciifolia in small plots in northern Greece and southern Spain (Carbonero et al., 2011). However, O. viciifolia exhibits poor growth following periods of high ambient temperatures and few plants survived at 35°C due to severe leaf loss causing plant death because high metabolic rates cannot be supported by existing leaf area or taproot carbohydrates even under wellwatered conditions (Kallenbach et al., 1996). High temperatures at the beginning of summer interrupt regrowth under traditional and intensive cutting regimes in southern Italy (De Falco et al., 2000a,2000b). Onobrychis viciifolia had a higher rate of biomass accumulation compared to M. sativa. However, M. sativa tended to grow faster during the warmer months (July–September) in Texas (USA). Interests and uses Agronomic characteristics and value Changing climatic conditions have reduced plant productivity and generated food security issues. In this context of food security, legumes exhibit promising benefits making them an exceptional food to meet nutritional needs (Akram et al., 2018). Onobrychis viciifolia is considered as an excellent component of a rotation in cropping systems by enhancing productivity and improving soil physicochemical properties including soil texture, fertility, water retention and organic matter content (Decourtye et al., 2007; Malisch et al., 2017; Sariyildiz and Savaci, 2020). Agronomic advantages Global climate change is predicted to impact on soil fertility through the physical, chemical, and biological properties of soil due to rise in temperature, alternation in precipitation patterns, increase in greenhouse gases concentration in the atmosphere, etc. (Mondal, 2021; Bibi and Rahman, 2023). In addition, climate change could lead to the loss of soil function for fertility maintenance and greater dependence on mineral fertilizers (Pareek, 2017). For centuries, O. viciifolia was widely grown across Europe before commercial fertilizers were used. The species does not need fertile soil to thrive if its requirements for lime and humidity are satisfied. Onobrychis viciifolia can thrive in less fertile soils than M. sativa and T. repens and can also grow well in more fertile soils. Medicago sativa and T. repens will, however, produce better yields in fertile and irrigated lands, but O. viciifolia provides better outcomes growing in low fertility soils compared with M. sativa (Benaiges, 1971; Demdoum, 2012). Mature plants of O. viciifolia have over 2-m-long taproots, partly responsible for its drought tolerance. The root is quite branched, especially at the bottom and multiples thin lateral roots constitute the bulk of the root system (Carbonero et al., 2011; Mora-Ortiz and Smith, 2018). The O. viciifolia root systems rivals M. sativa for its ability to access deep subterranean waters (Mora-Ortiz and Smith, 2018). In the Mediterranean Basin, O. viciifolia prefers altitudes above 600 m, but it performs well when cultivated in a range between 100 and 2500 m (García Salmerón et al., 1966; Demdoum, 2012). Agronomic disadvantages Onobrychis viciifolia is a forage legume of renewed interest worldwide, with equally weighted advantages and disadvantages that prevent many farmers from considering this crop a viable alternative to other forage legumes. In this sense, a wide distribution of O. viciifolia in productive grassland systems is hampered by the limited availability of high-performing cultivars adapted to different environmental conditions (Subedi, 2018; Sheppard et al., 2019). In fact, O. viciifolia weaknesses are related to its lower yield when compared to other forage legumes, its poor competitive ability against weeds especially during the establishment year, a limited persistence, susceptibility to waterlogging and frost (Sheehy and Popple, 1981; Liu et al., 2010), low tolerance to frequent cutting (Malisch et al., 2017), and susceptibility to diseases such as powdery mildew or Phytophthora root rot (Sears et al., 1975; Carbonero et al., 2011). Onobrychis viciifolia prefers welldrained soils and does not grow well in heavy soils or under flood irrigation (García Salmerón et al., 1966; Demdoum, 2012; Anderson, 2016). Onobrychis viciifolia does not perform properly in acidic soils. Poor O. viciifolia establishment was obtained on soils at pH lower than 6 (Bland, 1971; Carbonero et al., 2011). In Spain, O. viciifolia is traditionally cultivated on neutral or slightly alkaline brown-earth soils. Onobrychis viciifolia died out primarily during winter due to aerial interspecific competition, resulting in reduced root reserves (Liu et al., 2010). Persistence of O. viciifolia appears to be dependent on minimal pressure from competing plants, harvest or grazing, and good growth conditions from midsummer into fall, allowing for adequate root reserves for survival. It is possible that judicious use of glyphosate in late season might lessen 312 Anis Sakhraoui et al. https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press competition in that critical period as O. viciifolia is more glyphosate-tolerant than M. sativa (Peel et al., 2013). Crop residue Due to its deep, extensive and nodulated roots system, O. viciifolia uses water reserves in deep soil layers, increases carbon sequestration, reduces moisture and nutrient loss through leaching and runoff, prevents soil erosion, and improves the physicochemical and microbiological properties of the soil, including reductions on nitrification rates (Sergeeva, 1955;Komaindaet al., 2019; Clemensen et al., 2022). The irrigated cultivation of O. viciifolia accumulate in the soil up to 16.2 t/ha/year of residues, which represents approximately four times the quantity left by M. sativa (4.2 t/ ha/year) (Sergeeva, 1955). This could be explained by its high root biomass compared to other cultivated legumes (Bolat, 2019;Rossi et al., 2020). In fact, O. viciifolia can be used for soil organic matter improvement (Porqueddu et al., 2000;Wuet al., 2018). In view of these studies, cultivating O. viciifolia would help increasing the role of agricultural soils as carbon sinks to mitigate climate change. In addition to supplies biologically fixed N 2 ,O. viciifolia displays a range of adaptations for the acquisition and retention of other important resources. O. viciifolia has excellent resource use efficiency in low input environments (Carbonero et al., 2011). By virtue of their large active root systems and mycorrhization, O. viciifolia can efficiently accelerate the absorption of water and nutrients (Kong et al., 2014). Onobrychis viciifolia has the ability to acquire phosphorous via specialized root structures, through arbuscular mycorrhizal associations under controlled environment (Kong et al., 2014). The large rooting systems of O. viciifolia function to increase soil organic C by reducing erosion, reducing microbial respiration (via lack of tillage). As a result, nutrients are retained in the cropping system for use by subsequent crops (Carbonero et al., 2011). Fossil fuel burning in the energy sector is a major contributor to greenhouse gas emissions. Biofuels, considered as a substitute for fossil fuels, have become top priority due to its eco-friendly nature (Prasad et al., 2020). In addition to the biodiesel production from the legume (Ndukwu and Onyeoziri, 2022), all the biomass of O. viciifolia can serve to produce second-generation biofuel due to its high N content (Slepetys et al., 2012). Moreover, the use of O. viciifolia showed potential for methane production in biogas plants (Hunady et al., 2021). Onobrychis viciifolia contains phenolic compounds (tannins) that can influence soil nutrient dynamics by inhibiting microbial activity, which could slow N mineralization rates and minimize N losses in field (Clemensen et al., 2020,2022; Slebodnik et al., 2019). Tannins, at low concentrations in the soil, may increase some enzyme activity (Adamczyk et al., 2017), inactivate other soil enzymes, in part due to their antibiotic properties (Benoit and Starkey, 1968; Field and Lettinga, 1992; Joanisse et al., 2007; Triebwasser et al., 2012), and to the formation of tannin–protein complexes (Adamczyk et al., 2019). Dehydrogenase enzymatic activity was reported to be higher in O. viciifolia than M. sativa sown plots (Clemensen et al., 2020,2022). Atmospheric di-nitrogen fixation Crop production is dependent on inorganic N and other fertilizers inputs to resupply nutrients lost as harvested grain and forage, via soil erosion/runoff, and by other natural or anthropogenic causes (Schlautman et al., 2018; Bibi and Rahman, 2023). Nitrogen-fertilizers are one of the most monetary and environmentally expensive inputs in agricultural settings, which are currently more expensive than ever before (Herrera et al., 2016; Adjesiwor and Islam, 2016). The mobility of applied inorganic N fertilizers results in less than 50% fertilizer N-recovery efficiency by the first crop with substantial amounts of the remaining N leaving the cropping system as N 2 O and NO 3 (Crews and Peoples, 2004; Ladha et al., 2005). Onobrychis species are soil enriching via the fixation of atmospheric N. The symbiosis between legumes and root-nodule bacteria supplies biologically fixed N to natural and agroecosystems around the globe (Crews, 1993). This form of N is directly incorporated into the growing plant, overcoming problems of low fertilizer N-recovery efficiency. Onobrychis viciifolia is able to provide relief from reliance on synthetic N while supplying high forage quality in lowinput agricultural ecosystems (Carbonero et al., 2011). While N 2 fixation in legumes is considered to have higher energy and carbon requirements than N assimilation by plants using reduction of NO 3 for growth, the energy is supplied via solar radiation rather than through fossil fuels; thus, the resulting CO 2 respired by the nodules originates though photosynthesis and is not a net contributor to atmospheric CO 2 concentrations (Crews and Peoples, 2004; Jensen et al., 2012). Onobrychis species form symbioses with bacteria belonging to the genera Mesorhizobium,Rhizobium and Bradyrhizobium (Baimiev et al., 2007). In field conditions, Nitrogen deficiency symptoms were reported in O. viciifolia despite plants being abundantly nodulated, which indicates that the strain of N-fixing bacteria present was inefficient or short lived (Burton and Curley, 1968; Schneiter et al., 1969), but these symptoms disappeared with time in plants nodulated by effective strains (Prévost et al., 1987a). Small young nodules are generally the most effective in O. viciifolia and are scarce in early stages of growth in the field (Burton and Curley, 1968). In this sense, it seems likely that O. viciifolia is dependent on some mineral N at early growth stages and later growth stages benefit significantly from an effective symbiosis (Carbonero et al., 2011). However, the N-fixing system of O. viciifolia is very sensitive to low levels of nitrate under glasshouse conditions (Hume and Withers, 1985). Onobrychis viciifolia can be cross inoculated by Rhizobium species isolated from different leguminous species (Burton and Curley, 1968; Prévost et al., 1987a). Furthermore, inoculating O. viciifolia with rhizobia isolated from three arctic legume species improved biological nitrogen fixation during cold phases of the growing season (Prévost et al., 1987a,1987b). Based on acetylene reduction rates, the general effect of adding strains of Rhizobium to other strains of Rhizobium in symbiosis with O. viciifolia was additive (Hill, 1980). Kong et al.(2014) demonstrated that the inoculation of arbuscular mycorrhizal fungi can improve mycorrhizal infection rate and plant growth, accelerating the absorption of water and nutrients by the roots compared with uninoculated plants. Kon (1980) established that O. viciifolia, when infected with the appropriate Rhizobium spp. and arbuscular fungi, produced more and larger nodules and, consequently, a greater nodule dry weight and exhibited greater N 2 fixation than plants infected with only the rhizobia in a glasshouse conditions. Over two-year experiments, O. viciifolia fixed 106 kg N ha/year in rain-fed Mediterranean conditions, which was below the usual range of 130–160 kg N ha/year and quite far from the potential value of 270 kg N ha/year from non-Mediterranean areas (Provorov and Tikhonovich, 2003;Reet al., 2014)(Table 1). Issah et al.(2020) quantified biological N 2 fixation using 15 N isotope dilution and estimated resource partitioning in O. viciifolia under controlled conditions. The percentage of N derived from atmosphere was The Journal of Agricultural Science 313 https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press 81% corresponding to estimated N contributions of 65 kg N ha/year. In view of previous works, cultivating O. viciifolia would help mitigating climate change through the reduction of N fertilizers and related greenhouse gasses emissions. As well, the cultivationofO.viciifoliawouldsupportfarmersontheireffortstocope with climate change and to face increasing costs of N fertilizers. Weed and pest control Climate change is opening new geographic windows for disease outbreaks, insect herbivory and weed infestations in crops worldwide (Bajwa et al., 2020; Gullino et al., 2022). The inclusion of O. viciifolia can reduce number and cover of weeds in cereal fields (Cirujeda et al., 2019). Mummey and Ramsey (2017) concluded that O. viciifolia may be a useful bridge species for improving soil conditions while allowing for weed control during restoration of invasive crested wheatgrass (Agropyron cristatum (L.) Gaertmn.) stands, improving conditions for native species establishment in dry rangeland in North America. In addition, O. viciifolia can offer a multitude of ecosystem services by supporting biodiversity and hosting important enemies of crop pests in agricultural landscapes. For example, González et al.(2022) found almost 147 morphospecies of hymenopteran parasitoids in O. viciifolia patches providing a low-cost strategy for biological pest control in Brassica napus L. fields. According to these studies, cultivating O. viciifolia would improve biological control of pests just when their impacts are growing due to climate change. Honey production The change in climatic conditions is bound to have an impact on the physiology, distribution and survival of bees (Le Conte and Navajas, 2008; Smoliński et al., 2021). Under this scenario, conservation of honeybees remains a challenging task (Wood et al., 2020). As O. viciifolia is self-sterile, it relies on flower visitors for crosspollination and requires multiple visits to maximize pollination (Bogoyavlenskii, 1955,1974; Kropacova and Haslbachova, 1969). Bee pollination of O. viciifolia gave an increase of seed productivity by more than 30% (Pankov, 2013). Consequently, its flowers are a rich source of pollen and nectar, attracting ten times more bees than Trifolium repens L. and M. sativa (Rosov, 1952;McGregor, 1976;Kells,2001; Deveci and Kuvanci, 2012). Onobrychis viciifolia is visited by managed and indigenous pollinator insect species, including Apis,Bombus and Osmia in southern Alberta (Canada), Eastern Washington (USA), the British Isles (UK), Europe and Japan (Richards and Edwards, 1988;Horne,1995; Clement et al., 2006; Howes, 2007;USDASARE,2007; Westphal et al., 2008;Takiet al., 2009). Rozen et al.(2010)notedthat O. viciifolia is the only pollen source for Osmia avosetta Warncke bees in Turkey. In addition, different studies have described a very diverse pollinator community, dominated by Bombus and different bee species, foraging on O. viciifolia in Italy, Canada, USA, Europe and Turkey (Ricciardelli d’Albore and Roscioni, 1990; Kells, 2001;Clementet al., 2006;Decourtyeet al., 2010;Manino et al., 2010;Özbek,2011; Pearce et al., 2012;Richards,2019). Richards and Edwards (1988) found that bumblebees visited O. viciifolia flowers at a much greater rate than western honeybees in Canada. As previously stated, O. viciifolia is a good nectar and pollen source for many pollinator species and, additionally, it shows a long-lasting flowering period to offer bee pasture for western honeybees (Apies mellifera L.). and wild bees (Szalai, 2001). In addition, weeds in O. viciifolia crops are mainly represented by melliferous species in Russia (Pankov, 2014). When grown as a forage crop, O. viciifolia is mown late so flowering has normally finished, maximizing its value as a bee forage crop (Ayers, 1993). With a reduced number of flowers per plant under drought, O. viciifolia maintained similar per-flower nectar production (Phillips et al., 2018). Onobrychis viciifolia can yield up to 400 kg/ha of honey (Howes, 2007) with a distinctive taste, smell, texture and colour (Vereshchagin et al., 2015), which constitute an additional revenue (Pankov, 2012). Recently, it has been demonstrated that the caffeine present in the nectar of O. viciifolia reduces the infection of bumblebees (Bombus terrestris) by the microsporidian parasite Nosema bombi Fantham and Porter (Folly et al., 2021). Growing O. viciifolia may promote a diversification of agronomic production with honeybee related products, which is key to stand the impacts of climate change (Zhang et al., 2022). Erosion control Global warming is expected to lead to a more vigorous hydrological cycle, including more total rainfall and more Table 1. Effective bacterial and mycorrhiza strains for Onobrychis viciifolia inoculation Origin Variety References Bacteria Arctic N 31 Astragalus alpinus Melrose Prévost et al.(1987b) Arctic N 11 ,N 28 Oxytropis maydelliana Temperate SM-2 Onobrychis viciifolia cv Melrose Temperate 116M15 Commercial inoculant (Nitragin Co., Milwaukee, WI) 116A27, 116A14, 116A8, 124Z1, 124B1 Commercial inoculant (Nitragin Co., Milwaukee, WI) Remont Hill (1980) NZP 5301 Onobrychis viciifolia cv Fakir Fakir Kon (1980) Rhizobium ciceri Onobrychis spinacrisbi –Yousef and Abdul-Karim (2012) Arbuscular mycorrhiza Gigaspora magarita ––Kon (1980) Glomus fasciculata Glomus tenuis 314 Anis Sakhraoui et al. https://doi.org/10.1017/S0021859624000327 Published online by Cambridge University Press frequent torrential rainfall events, which may lead to higher soil erosion in many locations worldwide (Eekhout and de Vente, 2022; Dash and Maity, 2023). Cover of O. viciifolia and Rosa canina L. provided year-round soil protection, improving the soil structure, increasing its water holding capacity and its nutrient retention in Northwest Turkey (Sariyildiz and Savaci, 2020). O. viciifolia enhanced soil productivity by increasing soil organic carbon, soil total N and soil organic carbon stock capacity (Sariyildiz and Savaci, 2020). Yu et al.(2015) highlighted the superiority of O. viciifolia in water retention compared to different tree and herbaceous species in China. The structural stability of the soil under O. viciifolia continued for a long period and the infiltration rate was high, preventing an increase of runoff with time. Reduced-tillage systems coupled with O. viciifolia cropping should be considered as an efficient management practice and should be improved to withstand extreme rainfall conditions. When used as ridge-furrow rainwater harvesting with mulch, O. viciifolia offers farmers means to address drought, water loss and soil erosion in arable lands in arid and semiarid regions (Zhang et al., 2019b). Yüksek and Yüksek (2015) reported that plant cover of O. viciifolia was the main factor reducing surface runoff. Hairy leaves of O. viciifolia accumulate high sediment loads per leaf area, presumably, because hairs create a buffer zone of reduced water flow velocity enhancing sedimentation (Kretz et al., 2020). O. viciifolia is used for erosion control in northwest China and Turkey (Turk and Celik, 2006;Xuet al., 2006). Yakupoglu et al.(2021) showed that O. viciifolia cultivation exhibited the lowest soil losses when compared to fallow and wheat (Triticum aestivum L.) in Southern Turkey. O. viciifolia is an efficient cover crop in the conservation of soil and water, for example, in Mediterranean vineyards (Ben-Salem et al., 2018). According to these studies, cultivating O. viciifolia would reduce carbon emissions from soils since lowering erosion also reduces soil carbon dioxide emissions (Mandal et al., 2020;Ranet al., 2021). Ecological restoration Ecological restoration is a major nature-based solution towards meeting a wide range of global development goals by improving food and water security, protecting biodiversity and promoting adaptation and mitigation of climate change (Liu et al., 2020; Simonson et al., 2021). The improvement of semi-arid and arid degraded lands is one of the most important uses of O. viciifolia, since leguminous crops naturally increase soil productivity due to their association with N fixing microbes (Singh et al., 2019). In this sense, Roy et al.(2021) suggested that O. viciifolia is suitable when designing an appropriate strategy for achieving a successful revegetation of coal mined areas. Moreover, Ibragimov et al. (2019) highlighted the importance of the cultivation of multicomponent mixtures, including O. viciifolia, to face desertification in Southeast Russia. Recently, there has been growing concern over the potential impacts of global climate change on the sensitivity of weeds to herbicides. Reduced glyphosate sensitivity is projected in response to climate change (Matzrafi et al., 2019). Crop tolerance to glyphosate can reduce competition from weeds, leading to potentially higher yields and increased efficiency in weed control (Raza et al., 2023). Onobrychis viciifolia is relatively tolerant to glyphosate application. Based on the dose estimated to cause 50% mortality (LD 50 ), O. viciifolia seedlings are over six times, and mature plants are over 20 times, more tolerant to glyphosate than M. sativa. Based on the dose required to produce a 50% reduction in biomass yield (GR 50 ), glyphosate has a 10-fold greater negative impact on M. sativa biomass yield than it does on O. viciifolia. In addition, the GR 50 in O. viciifolia seedling was over two-fold and six-fold higher than M. sativa at the first and second harvests, respectively (Peel et al., 2013). However, no study has addressed the impact of glyphosate application on seed production. Hard seed levels vary considerably in O. viciifolia (up to 90%), and it appears to vary considerably with the cultivars (Bhattarai and Biligetu, 2018). Hard seed pod character may increase weediness of glyphosate tolerant O. viciifolia as reported for M. sativa (USDA, 2005) suggesting that O. viciifolia might pose weediness in ecological sensitive areas where it is not native and/or disperse into wild populations and persist in seed banks. Glyphosate-resistant crops have become a significant part of cropping systems in North America while it remains used extensively in the mediterranean basin probably due to lawsuits and concerns about gene flow and impacts on organic agriculture (Putnam and Orloff, 2013). Medicago sativa is a relatively recent crop to have glyphosate-resistant technology introduced. While weed control in sainfoin still a complex issue, O. viciifolia has not yet benefited from this technology. Given the low vigour of sainfoin, glyphosate resistant O. viciifolia offers new weed control options for sainfoin establishment for an improved long-term crop vigour and yield (McCordick et al.,2008). Adopted this technology could encourage many growers to adopt sainfoin as an alternative forage for apparent improvements in crop safety, quality, profitability and herbicide application simplicity. Nutritional interest and animal performance Livestock production is a major and highly diverse component of agriculture that is being exposed to changes in climate impacting on forage and feed crop production (Moore and Ghahramani, 2013; Rojas-Downing et al., 2017; Godde et al., 2021). O. viciifolia has aroused renewed interest in its use in livestock diets, as it has important nutritional properties such as high palatability and great nutritional value leading to very satisfactory animal performance (Gayrard et al., 2021). Scharenberg et al.(2007a) found that the palatability of dried and ensiled O. viciifolia was 20–24% higher than that of grasses and 10–29% higher than for Trifolium pratense L. and M. sativa (Waghorn et al., 1990). O. viciifolia hay was preferred to L. corniculatus hay by sheep (Scharenberg et al., 2007b) and nonlactating cows (Scharenberg et al., 2009; Lagrange et al., 2020). Contrary to forages like alfalfa, sainfoin is a non-bloating legume due to the presence of condensed tannins that attenuate the formation of biofilms in the rumen (Wang et al., 2006). In addition, condensed tannins attenuate the excessive accumulation of ammonia in the rumen through reductions in proteolysis (Lagrange et al., 2020). 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