Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review

Md  Abdul Muktadir; Kedar  Nath Adhikari; Andrew Merchant; Kiflemariam  Y. Belachew; Albert Vandenberg; Frederick  L. Stoddard; Hamid Khazaei

doi:10.3390/agronomy10091345

Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review

Muktadir, Md Abdul;Adhikari, Kedar Nath;Merchant, Andrew;Belachew, Kiflemariam Y.;Vandenberg, Albert;Stoddard, Frederick L.;Khazaei, Hamid 2020-09-07 00:00:00 agronomy Review Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review 1 , 2 , 3 1 2 Md Abdul Muktadir , Kedar Nath Adhikari , Andrew Merchant , 4 , 5 6 4 Kiﬂemariam Y. Belachew , Albert Vandenberg , Frederick L. Stoddard 6 , and Hamid Khazaei * Plant Breeding Institute, The University of Sydney, Narrabri, NSW 2390, Australia; muktadirgpb@gmail.com (M.A.M.); kedar.adhikari@sydney.edu.au (K.N.A.) Centre for Carbon, Water and Food, The University of Sydney, Camperdown, NSW 2570, Australia; andrew.merchant@sydney.edu.au Pulses Research Centre, Bangladesh Agricultural Research Institute, Gazipur 1701, Bangladesh Department of Agricultural Sciences and Viikki Plant Science Centre, University of Helsinki, PO Box 27, 00014 Helsinki, Finland; kiﬂemariam.belachew@helsinki.ﬁ (K.Y.B.); frederick.stoddard@helsinki.ﬁ (F.L.S.) Department of Plant Sciences, Bahir Dar University, Bahir Dar 5501, Ethiopia Department of Plant Sciences, 51 Campus Drive, University of Saskatchewan, Saskatoon, SK S7N 5A8, Canada; bert.vandenberg@usask.ca * Correspondence: hamid.khazaei@usask.ca Received: 11 August 2020; Accepted: 4 September 2020; Published: 7 September 2020 Abstract: Grain legumes are commonly used for food and feed all over the world and are the main source of protein for over a billion people worldwide, but their production is at risk from climate change. Water deﬁcit and heat stress both signiﬁcantly reduce the yield of grain legumes, and the faba bean is considered particularly susceptible. The genetic improvement of faba bean for drought adaptation (water deﬁcit tolerance) by conventional methods and molecular breeding is time-consuming and laborious, since it depends mainly on selection and adaptation in multiple sites. The lack of high-throughput screening methodology and low heritability of advantageous traits under environmental stress challenge breeding progress. Alternatively, selection based on secondary characters in a controlled environment followed by ﬁeld trials is successful in some crops, including faba beans. In general, measured features related to drought adaptation are shoot and root morphology, stomatal characteristics, osmotic adjustment and the eciency of water use. Here, we focus on the current knowledge of biochemical and physiological markers for legume improvement that can be incorporated into faba bean breeding programs for drought adaptation. Keywords: Vicia faba; drought; root; shoot; metabolomics 1. Introduction Among the cultivated grain legume crops, the faba bean (Vicia faba L.) ranked sixth globally in production, with a value of 4.5 Million tonnes from 2.5 Mha in 2019 [1]. The common bean (Phaseolus vulgaris L.) ranked ﬁrst, followed by the ﬁeld pea (Pisum sativum L.), chickpea (Cicer arietinum L.), cowpea (Vigna unguiculata (L.) Walp) and lentil (Lens culinaris Medik.), and the global average yield per hectare of the faba bean exceeds all of these other species. The faba bean was one of the ﬁrst domesticated crops in the Middle East [2] and spread from there eastward to Central Asia, India and China; westward to North Africa and Europe and, in more recent times, to Australia and the Americas [3]. While the wild antecedent of the faba bean is not known [4], carbonised remains dating back to 14,000 B.P. are viewed as examples of its existence [5]. Agronomy 2020, 10, 1345; doi:10.3390/agronomy10091345 www.mdpi.com/journal/agronomy Agronomy 2020, 10, 1345 2 of 19 Grain legumes provide substantial advantages in cereal-based cropping systems by breaking the life cycles of certain diseases, host-speciﬁc nematodes and weed species [6]. Like other grain legumes, faba bean and its symbiotic rhizobacteria ﬁx atmospheric nitrogen in a wide range of conditions. Biological nitrogen ﬁxation provides about 80% of the plant’s nitrogen needs [7], reaching 160 kg ha [7–9], and about half of the crop’s ﬁxed nitrogen content is left in the ﬁeld after grain harvest. Hence, it is considered important for both its contribution to residual nitrogen in crop rotation [6] and its potential in green manuring [10]. Faba bean seeds have high contents of protein and micronutrients and are also a good source of energy and dietary ﬁbre [11,12]. The average protein content is 29% [13], ranging from 24% to 35% [14], making it one of the most protein-rich pulses (starchy grain legumes). Mature beans are cooked into a stew or paste for human consumption in many countries and are also used as animal feed in many others. In its vegetable form, immature pods are harvested when the seeds are ﬁlling, and the young seeds are used as salad or cooked as vegetables. Whole-crop silage can be made from the whole plant and is a way of rescuing value from the crop if, for example, an exceptionally wet autumn prevents a harvest of the dry grain. Among cultivated grain legumes, the faba bean is considered to be sensitive to water deﬁcit (Figure 1). The faba bean yield in irrigated agriculture is signiﬁcantly higher than in rainfed systems [15], although the majority of its cultivation lies outside irrigated areas. Yield-based meta-analyses data from 1980 to 2014 indicated that the faba bean yield was reduced by 40% following a 65% reduction in water availability, and the loss in yield depended on the cultivar and other environmental conditions [16]. Improving drought tolerance is vital to improve the performance and stability of the yield, but ecient selection protocols and the mixed breeding system of this crop pose major challenges for eective plant breeding programs [17,18]. Field phenotyping for drought responses is expensive and time-consuming and is often unrepeatable because of variations in the timing of onset, duration and severity of the drought [19]. The mean outcrossing rate is about 33%, depending on the population of pollinators, cultivars and environmental conditions [20], and if cross-pollination between susceptible and tolerant plants occurs before drought stress occurs, the eectiveness of selection for the drought response is compromised [21]. On the other hand, controlled condition screening based on secondary physiological characteristics of roots and shoots, including stomatal conductance, relative water content, water potential, osmotic potential, root morphology, root plasticity and isotopic carbon discrimination, can provide generally reliable and repeatable information for selection, but the population size is compromised. Metabolic proﬁling, which provides insight into how changes in metabolite concentrations are inﬂuenced by changes in the environment, also holds great promise. In this review, we bring together the current physiological and biochemical knowledge on traits related to drought adaptation in the faba bean and elaborate how this knowledge can be used in breeding faba beans. A schematic overview of the roadmap to achieving these aims and how these relate to one another is shown in Figure 2. Agronomy 2020, 10, 1345 3 of 19 Agronomy 2020, 10, x FOR PEER REVIEW 3 of 19 Agronomy 2020, 10, x FOR PEER REVIEW 3 of 19 Figure 1. Faba bean plants (FB 9-4) under water-deficit conditions (left) and irrigated conditions Fig Figure ure 1. 1. Faba Fababean bean plants plant(FB s (F9-4) B 9-under 4) und water er wa -deﬁcit ter-defconditions icit conditio (left ns )(and left)irrigated and irrig conditions ated condi (right tions) (right) in Limerick and Outlook, Saskatchewan (Canada), respectively. ( in righ Limerick t) in Lim and erick Outlook, and Out Saskatchewan look, Saskatch (Canada), ewan (Carn espectively ada), respec . tively. Figure 2. The key elements of the roadmap and how these relate to one another. Figure 2. The key elements of the roadmap and how these relate to one another. Figure 2. The key elements of the roadmap and how these relate to one another. 1.1. Faba Bean Yield Response to Drought 1.1. Faba Bean Yield Response to Drought 1.1. Faba Bean Yield Response to Drought Three types of strategies to cope with drought stress have been characterised—namely, drought Three types of strategies to cope with drought stress have been characterised—namely, drought Three types of strategies to cope with drought stress have been characterised—namely, drought avoidance, drought dehydration tolerance and drought escape. Drought avoidance refers to avoidance, drought dehydration tolerance and drought escape. Drought avoidance refers to avoidance, drought dehydration tolerance and drought escape. Drought avoidance refers to mechanisms related to keeping a high plant water status under water-limited conditions by minimising mechanisms related to keeping a high plant water status under water-limited conditions by mechanisms related to keeping a high plant water status under water-limited conditions by the water loss and maximising the water uptake through root characteristics. Dehydration tolerance minimising the water loss and maximising the water uptake through root characteristics. minimising the water loss and maximising the water uptake through root characteristics. refers to maintaining metabolic activities at the low-tissue water potential (surviving internal water Dehydration tolerance refers to maintaining metabolic activities at the low-tissue water potential Dehydration tolerance refers to maintaining metabolic activities at the low-tissue water potential deﬁcits). Drought escape is the ability of a crop to complete its life cycle before the onset of drought or (surviving internal water deficits). Drought escape is the ability of a crop to complete its life cycle (surviving internal water deficits). Drought escape is the ability of a crop to complete its life cycle unfavourable conditions [22]. The faba bean is prone to water deﬁcit from seedling to maturity [19,22], before the onset of drought or unfavourable conditions [22]. The faba bean is prone to water deficit before the onset of drought or unfavourable conditions [22]. The faba bean is prone to water deficit but in the Mediterranean-type climates, where it is sown in autumn and harvested in spring as from seedling to maturity [19,22], but in the Mediterranean-type climates, where it is sown in autumn from seedling to maturity [19,22], but in the Mediterranean-type climates, where it is sown in autumn the temperature increases and rainfall declines, the faba bean often experiences so-called “terminal” and harvested in spring as the temperature increases and rainfall declines, the faba bean often and harvested in spring as the temperature increases and rainfall declines, the faba bean often droughts [23]. Adapted materials escape terminal droughts by early maturity, completing their life experiences so-called “terminal” droughts [23]. Adapted materials escape terminal droughts by early experiences so-called “terminal” droughts [23]. Adapted materials escape terminal droughts by early maturity, completing their life cycles before a drought occurs, often accompanied by a yield penalty. maturity, completing their life cycles before a drought occurs, often accompanied by a yield penalty. Besides terminal drought, the faba bean often experiences transient droughts in subtropical and Besides terminal drought, the faba bean often experiences transient droughts in subtropical and Agronomy 2020, 10, 1345 4 of 19 cycles before a drought occurs, often accompanied by a yield penalty. Besides terminal drought, the faba bean often experiences transient droughts in subtropical and temperate environments. Transient droughts reduce the plant stature and number of reproductive nodes in faba beans [24]. In contrast to escaping, there is no comparable and simple strategy to deal with unpredictable and intermittent transient droughts. Maintaining higher relative water contents under water deﬁcits, which demonstrates eective stomatal regulation and stomatal function [25], root morphology, plasticity and function [26], epicuticular wax and osmotic adjustment [22], play vital roles in the management of transient droughts. Although the faba bean originates from a semi-arid region, drought adaptation is not common. Its relatively shallow root system [27,28] is unable to extract water from deep soil, causing moisture stress during the reproductive phase when the topsoil dries. Genetic resources that can adjust to variations in soil moisture levels exist [19,29–33], indicating that there is potential to breed for moisture-limited environments. Link et al. [32] selected drought-tolerant cultivars and breeding lines from the Mediterranean region where water distribution is irregular and moisture levels are moderate (~500 mm rainfall). Maalouf et al. [34] also found dierent tolerance levels to water deﬁcits. The existence of wide genotypic variations makes it possible to develop drought-tolerant faba bean genotypes through classical breeding approaches. The plant developmental stage and the magnitude of water deﬁcit determine the yield loss of the faba bean. The most susceptible stages for developmental inhibition have been variously described as ﬂowering [35], early podding [36] and pod setting [37], but all of these studies generally agree that the early reproductive phase is the most sensitive stage [19,38]. Moderate drought stress had a negative eect on the pod number per plant but had no eect on the seed size or seed number per pod [35,39]. The extent of drought stress determined whether the plant had partial damage or complete death. These observations highlight the importance of identifying the developmental stage when assessing the impact of drought conditions in faba beans. Seed quality is also aected by water deﬁcit. Genotypic background and environmental factors, i.e., drought and heat, are the major factors that regulate seed protein contents [40]. Winter faba beans have slightly higher protein concentrations than spring beans, which may be interpreted as an indication that water deﬁcits tend to increase protein contents [41]. Faba bean crops grown in water-deﬁcit conditions have improved proteins [42] and sulphur contents [43] compared to those grown with adequate water. In drought-prone environments, reduced protein biosynthesis is due to reducing the N ﬁxation and partitioning [44]. On the other hand, Smith [45] reported that droughts caused yield reductions but did not alter the mineral nutritional quality (calcium, iron, potassium, magnesium, phosphorus, sulphur and zinc) or amino acid concentrations in the common bean. Generally, seed mineral uptake is not impacted by drought. A high N ﬁxation is usually observed in the faba bean under optimal conditions, whereas droughts can considerably impair the N ﬁxation [46,47]. Under water deﬁcits, modiﬁcations of the bacteroid environment cause the decline in N ﬁxation [48] and reduced nodule numbers in faba beans [49]. Combined, these observations illustrate the importance of physiological responses to droughts in the faba bean and the inﬂuence this has on crop yields and yield quality. It is therefore important to identify tools by which the physiological status may be quantiﬁed to assist in management and breeding to help mitigate the eects of drought conditions on plant performances. 1.2. Physiological Attributes Related to Stress Adaptation It is well-established that the phenotypic selection, based on adaptive traits that are secondary to yield, can be used for improving production in water-limited environments [50–52]. Secondary traits chosen for this purpose should be genetically associated with yield in the target environment, highly heritable and easy to measure. Drought-tolerance trait selections were found to be more meaningful when conducted on a large population [53]. Several physiological traits, including water use eciency (WUE) [31], stomatal features [54–56], leaf temperature and carbon isotope discrimination [19], have Agronomy 2020, 10, 1345 5 of 19 been found to be suitable selection criterion for the improvement of drought adaptation in faba bean breeding programs. 3+ Drought stress interacts with low temperatures, soil salinity and Al toxicity. Salinity and drought 3+ aect the osmotic equilibrium in a similar way [57], while Al toxicity hampers root development [58], and cold aects both the movement of water within roots and the ability of the plant to develop symbiosis [59]. Among legumes, Al-drought interactions have been studied in the common bean [60] 3+ and soybean (Glycine max (L.) Merr.) [61], and the Al toxicity exacerbated the eects of the drought mainly due to its inhibition of root growth. On the other hand, the drought was reported to ameliorate 3+ Al injury by reducing the uptake of the toxic ion. The Al-drought interaction has a synergistic eect on crops, rendering them unable to recover after exposure to these stresses. Salinity coupled with drought reduced the symbiotic nitrogen ﬁxation, which may be due to its eect on the supply of photosynthates or oxygen to the nodule and bacteroids [62]. Crosstalk in stress signalling and gene expression has been reviewed in drought and cold stress responses [63] and in cold and salinity responses [57]. In the faba bean, little genetic connection between the drought response and freezing tolerance was observed [64]. 2. Root Traits Compared with the aboveground traits, relatively few studies have been performed on belowground traits. A root trait analysis is complex, involving clumsy measurement systems, so maintaining a high level of precision is dicult in ﬁeld level screening [65]. Among the root architectural features, morphology and plasticity are the two general types of variation that exist. Genetic variations in root morphological characteristics have a signiﬁcant inﬂuence on the capacity and ecacy of a plant to search for and absorb moisture and nutrients from the soil. Deep-rooted soybean genotypes have a higher water-absorption capacity from deep horizons of soil, leading to a higher yield potential [66]. Moreover, the alteration of the root architecture (plasticity) follows several mechanisms under stress and nutrient availability. For example, the root/shoot biomass ratio increased in white lupin (Lupinus albus L.) and Andean lupin (L. mutabilis Sweet) during water deﬁcit [67]. Changes in the root density of L. angustifolius genotypes in response to phosphorus availability have also been observed [68]. Faba bean genotypes with extensive and proliﬁc root characteristics usually exhibit drought tolerance [29]. A variability in the root characteristics and root-based phenotyping for drought tolerance was also found in cowpeas [69], chickpeas [65,70,71], lentils [72,73] and the common bean [74]. Under water-deﬁcit conditions, Husain et al. [75] showed an increased root growth per unit area during the ﬂowering stage. Manschadi et al. [27] described the root length density, along with the dry root weight, and both were considerably reduced under drought conditions. Belachew et al. [26] identiﬁed root phenotypic markers associated with drought avoidance characteristics in young faba bean plants in GROWSCREEN-Rhizo boxes, a phenotyping robotic tool for measuring root and shoot growths [76]. Accordingly, two faba bean accessions (IG 70622 and IG 11320) that exhibit deeper root systems and higher root area coverage, displayed drought-avoidance traits through the maintenance of their primary and tertiary root lengths relatively well. The same observation was noted by Muktadir et al. [77] while screening drought-adapted genotypes in a hydroponic screening system. The growth of the tap root in the faba bean is a major inﬂuence on the total rooting depth; however, the tap root appears unable to acquire water for growth, even if the root surface has access to it. At shallow depths, lateral root growth is important for access to surface moisture and nutrients and is thought to be a major inﬂuence on plant health. Selection on the basis of rapid growth of the taproot and expansion of the lateral root system to maintain the root length density and dry root weight may be an eective method for increasing drought adaptation in faba bean breeding programs. There has been limited research on the genetic variability of root growth and branching in faba beans. Appropriate measurements of root systems include root mass, root mass fraction, rooting volume, root length and Agronomy 2020, 10, 1345 6 of 19 root/shoot ratio. Among them, the root mass is probably the easiest to measure, as, in chickpeas, it was strongly correlated to the shoot mass and represented 30–34% of the total dry matter [65]. 3. Shoot Related Traits Under stress conditions, selection for a higher yield is not always eective, because yield is controlled by several traits controlled by quantitative trait loci (QTL). To select genotypes for drought tolerance, the breeding process should be focused on the contributing characteristics rather than the yield itself. Contributing characters need to be causal, and shoot-related traits play a vital role in maintaining the water status when grown in water-deﬁcit conditions. 3.1. Leaf/Canopy Temperature The temperature of the exterior of the canopy is related to the vapour pressure deﬁcit and directly inﬂuences the amount of transpiration that leads to cooling by evaporation. Direct and easy measurement of the canopy temperature (CT) without disturbing the crop can be completed by using an infrared thermometer (IRT), which can be mounted on a drone to cover a large area in a relatively short time to minimise environmental ﬂuctuations. Blum et al. [78] introduced CT as a selection trait for dehydration tolerance. During water-deﬁcit conditions, closed stomata cause a decrease in transpiration, which ultimately leads to an increase in leaf temperature [79,80]. In ﬁeld conditions, maintaining a lower CT is generally linked with improving the absorption capacity of a plant under stress conditions [81]. CT can be used as a substitute selection trait to screen faba bean genotypes grown in control environments [19,22]. In a large set of faba bean germplasm collected from regions with contrasting moisture regimes around the globe, the leaﬂet and canopy temperatures were the most informative measurements distinguishing the germplasm from wet and dry origins [82,83]. CT has been found to be a prominent trait associated with drought tolerance for soybeans [84], chickpeas [85–87], cowpeas [88] and lentils [89]. The preference for use of CT is its noninvasive nature and application to early evaluations in large numbers of genotypes. The protocol for using an IRT should be followed carefully to avoid a large variance error and nonrepeatable results. Thermal infrared imaging of crop canopies is a further technology for the study of stomatal responses and for phenotyping plants for dierences in stomatal behaviours. The use of remote imaging, when combined with an eective image analysis tool, provides a powerful approach for the comparison of large germplasm collections in typical ﬁeld conditions [90]. 3.2. Leaf Water Relations During water-deﬁcit conditions, plants may maintain the water potential by the production and accumulation of cellular metabolites/osmotica, which are sensed by stomata for the maintenance of sustaining the turgor pressure. Plant species and their developmental stages are the determinants of the types and functions of these metabolites. Relatively few candidate molecules can function as cellular osmotica, as they must be compatible with cellular functions at high concentrations. These candidate molecules may be organic acids, inorganic ions, polyols, polyamines and carbohydrates. In chickpeas, carbohydrates and polyols contribute more than 50% to the osmotic pool [23], and in ﬁeld peas, these ranged from 10–46% [91]. More broadly, the osmotic potential ( s) and turgor potential ( p), the two main components of leaf water potential ( ), were found to be an eective selection trait for drought tolerance screening. Generally, leaf is considered a major component of the leaf-level water deﬁcit [92], and it can ultimately drive interpretations of the plant water status [93,94]. Sustaining leaf under stress involves a number of mechanisms that are related to both root and shoot and are considered to be connected to drought avoidance [95]. Higher leaf turgor in response to water deﬁcit is one of the adaptation strategies for many plant species [96,97]. Osmotic adjustment-driven drought adaptation was also observed in chickpeas [98,99], ﬁeld peas [100] and lentils [101,102]. In faba beans, drought tolerance through osmotic adjustment has not yet been demonstrated in the wide germplasm but, as a selection criterion under drought, is sporadically observed, e.g., [103]. Metabolic adjustments Agronomy 2020, 10, 1345 7 of 19 in response to drought conditions may highlight pools of metabolites that play vital roles in the metabolism and physiology and may indicate which pathways have been perturbed by the stress. 3.3. Relative Water Content The relative water content (RWC) is a robust and simply assessable selection criterion that can describe the plant water status to the metabolism irrespective of plant parts and species. It can be expressed as the water content of tissues in normal conditions compared to hydrated conditions [104]. During water-deﬁcit conditions, the RWC plays an important role by preserving water (stomatal features, leaf area reduction and leaves dropping) or maximising the water absorption (root plasticity). Sinclair and Ludlow [105] found the RWC superior over water potential to assess plant water statuses. Khazaei et al. [55] stated the RWC as one of the most important traits that diered between wet- and dry-adapted faba bean accessions under nonstress conditions. The RWC is composed of a relative change in cell turgor and s, so it relates to both the solute concentrations and cell wall rigidity [106]. The RWC can eciently identify drought-tolerant genotypes based on their plant water status in faba beans [19,82,107], common beans [108] and chickpeas [109,110]. Therefore, it can be said that genotypes that can sustain a higher RWC in a water deﬁcit environment would be suitable for use in breeding faba beans for drought adaptation. 3.4. Stomatal Conductance Drought avoidance involves the maintenance of gas exchange during drought conditions, which causes either higher stomatal conductance, g (low stomatal sensitivity to drought) or stomatal closure to restrict water loss. There is a trade-o between gas exchange and stomatal closure during stress, which ultimately aects photosynthesis and, then, carbon assimilation. Stomatal conductance has been proposed as an eective selection tool and, when measured on multiple plants in a canopy, is equally eective as CT [111]. The measurement of g depends on several stomatal features. Faba bean stomatal characteristics are assessed through microscopy [25,29], but due to the rapid response to stress, the stomatal opening size is hard to measure. Leaf porometer or portable photosynthesis machines quantify g but may not reﬂect the variability over longer timeframes, as it changes rapidly. The measurement of g is highly inﬂuenced by environmental conditions (high genotype by environment interaction), time of day and plant developmental stage. Leport et al. [101] found that white lupin, chickpeas, faba beans, ﬁeld peas, grass peas (Lathyrus sativus L.) and lentils all responded similarly under water-deﬁcit conditions. During early stage drought, g was remarkably reduced, but at later stages, after the initiation of pod ﬁlling, it had little or no eect. Faba bean genotypes with higher stomatal density were lower-yielding and exhibited low drought tolerance, while genotypes with low stomatal density performed better in stress conditions [56]. In a relatively small set of faba bean germplasm, g was found to be an important vital trait [19,112]. The considerable variation for g among 402 faba bean accessions under nonstress conditions indicates the potential use of this trait [25]. The drought treatment of faba beans during the ﬁrst three weeks of growth resulted in the expected reductions in biomass and g [113]. The gas exchange measurements, along with stomatal morphology characteristics, have been genetically mapped in the faba bean. The QTL governing stomatal morphology, g and CT were all co-located in faba bean chromosome 2 [83]. A study of the gene actions showed that breeders selecting for the productivity of faba beans can maximise genetic gain by selecting early generations for CT and g [114]. The eectiveness of stomatal control over transpiration eciency increases if nonstomatal transpiration pathways are restricted. An important nonstomatal water vapour pathway is the leaf cuticle. The epicuticular wax (ECW) quantity is considered as an important drought avoidance strategy in plant species. There was a considerable variation for ECW in 197 faba bean accessions, ranging from 0.680 to 2.104 mg/dm [115]. This variation may allow the genetic improvement of ECW as a drought-adaptive character in faba bean breeding programs. Agronomy 2020, 10, 1345 8 of 19 3.5. Carbon Isotope Discrimination Carbon isotope discrimination (D) is proposed extensively as a proxy for the plant physiological status, especially WUE [116]. It is used to evaluate the transpiration eciency (TE) in cereals and, more recently, in legumes, common beans [117–119], soybeans [120], chickpeas [121], cowpeas [122] and lentils [123]. In faba beans, drought-tolerant genotypes ILB 938 and Mélodie had signiﬁcantly lower D than those of the drought-susceptible genotypes, e.g., Aurora [19]. In a larger faba bean germplasm, D varied from 24.43% to 28.82‰, equivalent to an intrinsic water use eciency (WUE ) of 98.53–179.75 mol CO mol H O (manuscript in preparation). There is some controversy regarding 2 2 the relationship between D and TE. Turner et al. [123] argued that TE was not signiﬁcantly correlated with D in three grain legumes, i.e., lentils, narrow-leafed lupin (L. angustifolius L.) and chickpeas. Carbon isotope discrimination may not always indicate the prediction of actual WUE, because generally, D is measured from leaf tissue, which has limitations for estimating short-term environmental changes [124]. Carbon isotope discrimination-based screening methods are expensive and require sophisticated and costly instrumentation, e.g., isotope ratio mass spectrometry (IRMS). A wider spectrum of faba bean germplasm needs to be surveyed for genetic variations in D under various environmental conditions to allow D to be used as a strong screening tool in faba breeding programs. 4. Metabolomics for Legume Breeding Metabolomics is a fast-emerging area of knowledge that integrates gene expression, protein interaction and other regulatory progressions. Nowadays, metabolic products are used as biomarkers in crop improvement due to their strong linkage with environmental characteristics [125]. So far, more than 200,000 metabolites have been identiﬁed in plants. These have a diverse set of functions and quantiﬁcation, and the qualiﬁcation of these composite characteristics into subsets of metabolic functions can oer a unique view of the inducible chemical and physiological response mechanisms [126]. The identiﬁcation and quantiﬁcation of low molecular weight metabolites require special analytical and separation techniques involving gas chromatography (GC) [127], liquid chromatography (LC) [127,128] and high-performance liquid chromatography (HPLC) [129]. These methods can characterise a vast range of metabolites at extraordinary scales and accuracy. Recently, nuclear magnetic resonance (NMR) has provided a greater ability for researchers to proﬁle metabolites [130]. Metabolic proﬁling studies of grain legumes are relatively unexplored and seemingly absent for faba beans. Zhang et al. [131] studied metabolic variations between symbionts in Medicago truncatula Gaertn. through an untargeted quantitative mass spectrometry-based (MS) method. Short-term water deﬁcit eects on the overall growth through metabolic changes were studied by NMR-based metabolic proﬁling [132]. Plants produce many primary and secondary metabolites during stress. Two dierent options can deﬁne this process: osmotic adjustment, where the plant regulates solute synthesis to decrease the osmotic potential under adverse situations [133], and solute accumulation, which occurs due to reductions, interruptions or ﬂuctuations in the solute transport [134]. Generally, osmotica are easily synthesised from readily accessible antecedents and are transformed to metabolically active and movable compounds. Overall, pre-existing metabolomic resources for legume research will beneﬁt faba bean improvements. However, accelerated applications of these tools may uncover new solutes/biochemical markers for stress tolerance in faba bean breeding. 4.1. Metabolite Accumulation in Legumes in Response to Drought and Their Use as Biomarkers 4.1.1. Amino Acids The accumulation of amino acids and other nitrogen-based molecules in response to stress is one of the most important biochemical signals for almost all plants. These essential metabolites are shown to accumulate during stresses in dierent legumes, including the model species M. truncatula and soybeans [135–139]. The accumulated enhanced protein breakdown is triggered by stress, and a higher amino acid concentration helps a plant to survive under stress [140]. Agronomy 2020, 10, 1345 9 of 19 Proline is found to be the most prevalent amino acid found in plant tissues under stress conditions (drought, cold and salinity). Singh et al. [141] demonstrated a correlation between drought and an increased free proline accumulation in drought-tolerant barley cultivars compared to a more drought-susceptible genotype. Similar correlations have been found in other crops [142], but there are also reports of poor correlations between drought and proline accumulations [143] in legume species. For example, Lotus spp. and soybeans showed a positive association with increased proline concentrations during the reproductive stage only [132,144]. Again, during water deﬁcit, proline accumulation was observed in the pre-ﬂowering stage of peanuts (Arachis hypogaea L.) [145]. Proline accumulation relies not only on the water status but, also, on the growth stage of the plant. Short-term stress can be identiﬁed through proline quantiﬁcation. Venekamp et al. [146] found that just one day of water deﬁcit at the seedling stage induced proline accumulation. An increased proline concentration in faba beans was observed with the increase of the stress intensity, and the variation in proline concentrations at the genotypic level was reported to be low under optimal conditions [46,107,147,148]. However, an exogenous proline application can decrease stomatal opening under drought, and this had a positive impact on drought tolerance mechanisms [149,150]. Proline accumulation provides an indication of the plant physiological status, i.e., whether it is stressed or not, but not a descriptive drought tolerance indicator in faba beans. An exogenous application of -aminobutyric acid (BABA) as a nonprotein amino acid was shown to enhance the accumulation of proline and soluble sugars, which improved drought adaptation in faba beans [151]. Besides proline accumulation, other amino acids are also observed in response to droughts in plants [152]. In lentils, methionine, isoleucine, valine, arginine and histidine increased under drought stress [138]. Drought stress-mediated GABA (gamma-aminobutyric acid) synthesis was observed in 2+ Arabidopsis thaliana, soybeans and common beans [153]. Abiotic stresses enhanced cytosolic Ca levels, which ultimately promoted GABA synthesis, but until now, no evidence was found where GABA stimulated the stomata opening or closing through its ion transporter function [154]. 4.1.2. Polyamines Another plant response to abiotic stresses is polyamines (PA) synthesis, but the association between PA accumulation and fortiﬁcation remains inconclusive. Three commonly found polyamines are putrescine, spermidine and spermine. Usually, stress-tolerant accessions contain a higher amount of PA than sensitive accessions [155,156]. Nevertheless, all three PAs do not accumulate at the same time, but one type of PA shows a stronger response. For example, under PEG-osmotic stress conditions, lentil cotyledons and roots exhibited increased putrescine and spermidine, while the cadaverine presence was nonsigniﬁcant. Drought-adapted yellow lupin (L. luteus L.) accessions produced a high amount of PAs compared to moderately adapted genotypes. Drought stress also increased the concentrations of spermidine and spermine [156]. Beside leaves, seeds commonly exhibit opposite trends, where leaves accumulate more Pas, and the seed content is reduced. Nayyar et al. [157] observed more PA accumulations in chickpeas compared to soybeans under water-deﬁcit conditions. In relay cropping with legumes, 18 rice (Oryza sativa L.) cultivars showed signiﬁcantly higher spermine levels when exposed under salt stress [158]. With this information, it can be said that PA accumulation does not depend on a single factor. Multiple factors like plant species, stress type and level, and the physiological status of the studied tissues, are involved. The PA dynamics of abiotic stress eects can unveil contradictory results of PA accumulation. The stress tolerance of a given species often correlates with the PA pool size, which can answer some underlying questions about the importance of PAs in assisting the protection against stresses. In faba beans, spermine, cadaverine and total polyamine increased in parallel with the salinity level, whereas the putrescine and spermidine levels decreased [159]. In faba beans, PA accumulations in response to drought stress have not been studied to date. Agronomy 2020, 10, 1345 10 of 19 4.1.3. Organic Acids Organic acid plays an important role in plant metabolism as an early source of photosynthesis and precursors of the synthesis of many other compounds. Organic acids support stomata regulation, ion equilibrium, ammonium manufacture and nutrient absorption [160]. Among the proﬁled metabolite classes estimated from soybean leaf tissue, organic acids occupy around 20% of the metabolites [161]. Nitrogen ﬁxation in the nodule is impacted by the malic acid concentration, which regulates the bacteroid respiration [162]. The abundance of organic acids also depends on the type of organ. Organic acid concentrations were lower in lentil root tissue than in cotyledon tissue [138]. Sassi et al. [163] observed a reduced amount of organic acids in common bean leaves under osmotic stress conditions. The amount of succinate was doubled in drought-treated soybean leaves. In lentils, isocitric, nicotinic and oxaloacetic acid concentrations increased considerably in plants exposed to osmotic stress [164]. In soybeans, reduced amounts of organic acids in drought-adapted genotypes suggested metabolic ﬂexibility, as plants shifted from growth to survival [132]. Organic acid functions in response to stress in faba beans have not yet been demonstrated, but it could become an area for future enquiry. 4.1.4. Carbohydrates Carbohydrates are often referred to as appropriate osmotica and represent one of the main components of osmoregulation in many plant species [165]. The metabolic proﬁling of the model forage legume Lotus japonicus L. when aected by drought showed the accumulation of the sugars fructose, galactose, glucose and maltose, while arabitol, ununitol and galactitol were the most abundant polyols [144]. In soybean leaves, about 30% of the metabolites identiﬁed were soluble sugars and sugar alcohols, which are important for plant adaptation against stresses, especially during water deﬁcits [161]. The close association among carbohydrates and their involvement in the primary metabolism suggested a molecular modiﬁcation may be possible to improve the stress tolerance through the synthesis and degradation of these compounds [166]. However, there is no general acceptance of the hypothesis that “osmotic adjustment arises from the accumulation of solute due to the persistence of photosynthesis after cessation of leaf growth” [133]. Among the dominant carbohydrates, trehalose, a nonreducing disaccharide, accumulates in large quantities in the unusual desiccation-tolerant plant Myrothamnus ﬂabellifolia Wolw. [167,168]. High levels of trehalose can stabilise proteins and membranes [169]. It has been recently reported that rhizobium inoculation can also increase the dehydration tolerance of several legume species through trehalose biosynthesis [170–173]. Moreover, an increased trehalose concentration was found to be a signiﬁcant contributor to drought tolerance [174]. Polyhydric alcohols or polyols are a major metabolite group reviewed by Merchant and Richter [175]. The quantity of polyols found in plant tissues was found to be sensitive to environmental conditions [176,177]. Further, Dumschott et al. [178] characterised D-pinitol as being inﬂuenced by the developmental stage. D-Pinitol is present in most legumes at some level under optimal conditions, but an increase is triggered during water and salinity stress [179]. While there is a general consensus on the function of pinitol in plant systems, gaps remain in understanding the conditions leading to pinitol accumulation, as well as the molecular control of the accumulation. 5. Faba Bean Genetic Resource to Aid Breeding for Drought Adaption A wealth of faba germplasm is available, comprising over 43,000 accessions (Dr. Kenneth Street, personal communication) that are conserved mostly within 37 global gene banks. The ICARDA (International Centre for Agricultural Research in the Dry Areas) collection exceeds 9000 accessions (21% of the global collection) [55]. Wide genetic variations have already been reported in faba bean genetic resources for various traits, including physiological traits related to drought adaptation (reviewed in [82]). This enormous variability is expected in this ancient domesticated crop with its wide adaptability to various latitudes and altitudes. The rich germplasm collection of faba beans Agronomy 2020, 10, 1345 11 of 19 should be systematically maintained and could be characterised for the physiological and metabolic parameters in order to improve drought adaptation in this species. 6. Conclusions Improvement of global faba bean production will have a positive impact on the food supply and cropping systems of many nations. Tools to improve faba bean production will incorporate both management activities and improved genotypes. The adoption of these tools must balance the necessity for broad-scale characterisations and cost with the precision required for appropriate detection at the plant scale. Many traits have been identiﬁed for drought tolerance studies. Some traits, like canopy temperature, can be used eciently for large numbers of genotypes in breeding programs, while, for example, carbon isotope discrimination is largely limited to low numbers of genotypes. Metabolite-based biomarkers and bioindicators can easily supplement the selection process in faba bean breeding programs. The identiﬁcation and quantiﬁcation of given primary and/or secondary metabolites against speciﬁc stresses could become valuable decision-making tools for plant breeders if their associations are of sucient strength and their analytical costs are low. The available metabolomic resources from other legumes should be explored to understand the molecular insights of stresses. The large genome of the faba bean is currently being sequenced, which will soon make molecular breeding possible. Finally, no single trait and approach are adequate to improve yields under drought conditions, the most complex environmental factor for faba bean productivity. A combination of screening methods suitable for speciﬁc environments and expansion of the scale of breeding will be required to allow expansion of the production area and yield of the faba bean, a crop that is an increasingly important source of plant-based protein in drought-prone production regions. Author Contributions: Writing—original draft preparation, M.A.M., and writing—review and editing, K.N.A., A.M., K.Y.B., A.V., F.L.S. and H.K. All authors have contributed, read and agreed to the published version of the manuscript. Funding: M.A.M. acknowledges the support from University of Sydney International Scholarship and also supplemented by the Grains Research and Development Corporation. K.Y.B.’s participation was funded by the European Union through its ERANET SusCrop projects “ProFaba” and “LegumeGap”. H.K. acknowledges funding from Agriculture Development Fund (Government of Saskatchewan, Canada); Western Grains Research Foundation, Canada; Saskatchewan Pulse Growers, Canada; and the NORFAB (Protein for the Northern Hemisphere) project funded by Innovation Fund, Denmark. 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Abstract

agronomy Review Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review 1 , 2 , 3 1 2 Md Abdul Muktadir , Kedar Nath Adhikari , Andrew Merchant , 4 , 5 6 4 Kiﬂemariam Y. Belachew , Albert Vandenberg , Frederick L. Stoddard 6 , and Hamid Khazaei * Plant Breeding Institute, The University of Sydney, Narrabri, NSW 2390, Australia; muktadirgpb@gmail.com (M.A.M.); kedar.adhikari@sydney.edu.au (K.N.A.) Centre for Carbon, Water and Food, The University of Sydney, Camperdown, NSW 2570, Australia; andrew.merchant@sydney.edu.au Pulses Research Centre, Bangladesh Agricultural Research Institute, Gazipur 1701, Bangladesh Department of Agricultural Sciences and Viikki Plant Science Centre, University of Helsinki, PO Box 27, 00014 Helsinki, Finland; kiﬂemariam.belachew@helsinki.ﬁ (K.Y.B.); frederick.stoddard@helsinki.ﬁ (F.L.S.) Department of Plant Sciences, Bahir Dar University, Bahir Dar 5501, Ethiopia Department of Plant Sciences, 51 Campus Drive, University of Saskatchewan, Saskatoon, SK S7N 5A8, Canada; bert.vandenberg@usask.ca * Correspondence: hamid.khazaei@usask.ca Received: 11 August 2020; Accepted: 4 September 2020; Published: 7 September 2020 Abstract: Grain legumes are commonly used for food and feed all over the world and are the main source of protein for over a billion people worldwide, but their production is at risk from climate change. Water deﬁcit and heat stress both signiﬁcantly reduce the yield of grain legumes, and the faba bean is considered particularly susceptible. The genetic improvement of faba bean for drought adaptation (water deﬁcit tolerance) by conventional methods and molecular breeding is time-consuming and laborious, since it depends mainly on selection and adaptation in multiple sites. The lack of high-throughput screening methodology and low heritability of advantageous traits under environmental stress challenge breeding progress. Alternatively, selection based on secondary characters in a controlled environment followed by ﬁeld trials is successful in some crops, including faba beans. In general, measured features related to drought adaptation are shoot and root morphology, stomatal characteristics, osmotic adjustment and the eciency of water use. Here, we focus on the current knowledge of biochemical and physiological markers for legume improvement that can be incorporated into faba bean breeding programs for drought adaptation. Keywords: Vicia faba; drought; root; shoot; metabolomics 1. Introduction Among the cultivated grain legume crops, the faba bean (Vicia faba L.) ranked sixth globally in production, with a value of 4.5 Million tonnes from 2.5 Mha in 2019 [1]. The common bean (Phaseolus vulgaris L.) ranked ﬁrst, followed by the ﬁeld pea (Pisum sativum L.), chickpea (Cicer arietinum L.), cowpea (Vigna unguiculata (L.) Walp) and lentil (Lens culinaris Medik.), and the global average yield per hectare of the faba bean exceeds all of these other species. The faba bean was one of the ﬁrst domesticated crops in the Middle East [2] and spread from there eastward to Central Asia, India and China; westward to North Africa and Europe and, in more recent times, to Australia and the Americas [3]. While the wild antecedent of the faba bean is not known [4], carbonised remains dating back to 14,000 B.P. are viewed as examples of its existence [5]. Agronomy 2020, 10, 1345; doi:10.3390/agronomy10091345 www.mdpi.com/journal/agronomy Agronomy 2020, 10, 1345 2 of 19 Grain legumes provide substantial advantages in cereal-based cropping systems by breaking the life cycles of certain diseases, host-speciﬁc nematodes and weed species [6]. Like other grain legumes, faba bean and its symbiotic rhizobacteria ﬁx atmospheric nitrogen in a wide range of conditions. Biological nitrogen ﬁxation provides about 80% of the plant’s nitrogen needs [7], reaching 160 kg ha [7–9], and about half of the crop’s ﬁxed nitrogen content is left in the ﬁeld after grain harvest. Hence, it is considered important for both its contribution to residual nitrogen in crop rotation [6] and its potential in green manuring [10]. Faba bean seeds have high contents of protein and micronutrients and are also a good source of energy and dietary ﬁbre [11,12]. The average protein content is 29% [13], ranging from 24% to 35% [14], making it one of the most protein-rich pulses (starchy grain legumes). Mature beans are cooked into a stew or paste for human consumption in many countries and are also used as animal feed in many others. In its vegetable form, immature pods are harvested when the seeds are ﬁlling, and the young seeds are used as salad or cooked as vegetables. Whole-crop silage can be made from the whole plant and is a way of rescuing value from the crop if, for example, an exceptionally wet autumn prevents a harvest of the dry grain. Among cultivated grain legumes, the faba bean is considered to be sensitive to water deﬁcit (Figure 1). The faba bean yield in irrigated agriculture is signiﬁcantly higher than in rainfed systems [15], although the majority of its cultivation lies outside irrigated areas. Yield-based meta-analyses data from 1980 to 2014 indicated that the faba bean yield was reduced by 40% following a 65% reduction in water availability, and the loss in yield depended on the cultivar and other environmental conditions [16]. Improving drought tolerance is vital to improve the performance and stability of the yield, but ecient selection protocols and the mixed breeding system of this crop pose major challenges for eective plant breeding programs [17,18]. Field phenotyping for drought responses is expensive and time-consuming and is often unrepeatable because of variations in the timing of onset, duration and severity of the drought [19]. The mean outcrossing rate is about 33%, depending on the population of pollinators, cultivars and environmental conditions [20], and if cross-pollination between susceptible and tolerant plants occurs before drought stress occurs, the eectiveness of selection for the drought response is compromised [21]. On the other hand, controlled condition screening based on secondary physiological characteristics of roots and shoots, including stomatal conductance, relative water content, water potential, osmotic potential, root morphology, root plasticity and isotopic carbon discrimination, can provide generally reliable and repeatable information for selection, but the population size is compromised. Metabolic proﬁling, which provides insight into how changes in metabolite concentrations are inﬂuenced by changes in the environment, also holds great promise. In this review, we bring together the current physiological and biochemical knowledge on traits related to drought adaptation in the faba bean and elaborate how this knowledge can be used in breeding faba beans. A schematic overview of the roadmap to achieving these aims and how these relate to one another is shown in Figure 2. Agronomy 2020, 10, 1345 3 of 19 Agronomy 2020, 10, x FOR PEER REVIEW 3 of 19 Agronomy 2020, 10, x FOR PEER REVIEW 3 of 19 Figure 1. Faba bean plants (FB 9-4) under water-deficit conditions (left) and irrigated conditions Fig Figure ure 1. 1. Faba Fababean bean plants plant(FB s (F9-4) B 9-under 4) und water er wa -deﬁcit ter-defconditions icit conditio (left ns )(and left)irrigated and irrig conditions ated condi (right tions) (right) in Limerick and Outlook, Saskatchewan (Canada), respectively. ( in righ Limerick t) in Lim and erick Outlook, and Out Saskatchewan look, Saskatch (Canada), ewan (Carn espectively ada), respec . tively. Figure 2. The key elements of the roadmap and how these relate to one another. Figure 2. The key elements of the roadmap and how these relate to one another. Figure 2. The key elements of the roadmap and how these relate to one another. 1.1. Faba Bean Yield Response to Drought 1.1. Faba Bean Yield Response to Drought 1.1. Faba Bean Yield Response to Drought Three types of strategies to cope with drought stress have been characterised—namely, drought Three types of strategies to cope with drought stress have been characterised—namely, drought Three types of strategies to cope with drought stress have been characterised—namely, drought avoidance, drought dehydration tolerance and drought escape. Drought avoidance refers to avoidance, drought dehydration tolerance and drought escape. Drought avoidance refers to avoidance, drought dehydration tolerance and drought escape. Drought avoidance refers to mechanisms related to keeping a high plant water status under water-limited conditions by minimising mechanisms related to keeping a high plant water status under water-limited conditions by mechanisms related to keeping a high plant water status under water-limited conditions by the water loss and maximising the water uptake through root characteristics. Dehydration tolerance minimising the water loss and maximising the water uptake through root characteristics. minimising the water loss and maximising the water uptake through root characteristics. refers to maintaining metabolic activities at the low-tissue water potential (surviving internal water Dehydration tolerance refers to maintaining metabolic activities at the low-tissue water potential Dehydration tolerance refers to maintaining metabolic activities at the low-tissue water potential deﬁcits). Drought escape is the ability of a crop to complete its life cycle before the onset of drought or (surviving internal water deficits). Drought escape is the ability of a crop to complete its life cycle (surviving internal water deficits). Drought escape is the ability of a crop to complete its life cycle unfavourable conditions [22]. The faba bean is prone to water deﬁcit from seedling to maturity [19,22], before the onset of drought or unfavourable conditions [22]. The faba bean is prone to water deficit before the onset of drought or unfavourable conditions [22]. The faba bean is prone to water deficit but in the Mediterranean-type climates, where it is sown in autumn and harvested in spring as from seedling to maturity [19,22], but in the Mediterranean-type climates, where it is sown in autumn from seedling to maturity [19,22], but in the Mediterranean-type climates, where it is sown in autumn the temperature increases and rainfall declines, the faba bean often experiences so-called “terminal” and harvested in spring as the temperature increases and rainfall declines, the faba bean often and harvested in spring as the temperature increases and rainfall declines, the faba bean often droughts [23]. Adapted materials escape terminal droughts by early maturity, completing their life experiences so-called “terminal” droughts [23]. Adapted materials escape terminal droughts by early experiences so-called “terminal” droughts [23]. Adapted materials escape terminal droughts by early maturity, completing their life cycles before a drought occurs, often accompanied by a yield penalty. maturity, completing their life cycles before a drought occurs, often accompanied by a yield penalty. Besides terminal drought, the faba bean often experiences transient droughts in subtropical and Besides terminal drought, the faba bean often experiences transient droughts in subtropical and Agronomy 2020, 10, 1345 4 of 19 cycles before a drought occurs, often accompanied by a yield penalty. Besides terminal drought, the faba bean often experiences transient droughts in subtropical and temperate environments. Transient droughts reduce the plant stature and number of reproductive nodes in faba beans [24]. In contrast to escaping, there is no comparable and simple strategy to deal with unpredictable and intermittent transient droughts. Maintaining higher relative water contents under water deﬁcits, which demonstrates eective stomatal regulation and stomatal function [25], root morphology, plasticity and function [26], epicuticular wax and osmotic adjustment [22], play vital roles in the management of transient droughts. Although the faba bean originates from a semi-arid region, drought adaptation is not common. Its relatively shallow root system [27,28] is unable to extract water from deep soil, causing moisture stress during the reproductive phase when the topsoil dries. Genetic resources that can adjust to variations in soil moisture levels exist [19,29–33], indicating that there is potential to breed for moisture-limited environments. Link et al. [32] selected drought-tolerant cultivars and breeding lines from the Mediterranean region where water distribution is irregular and moisture levels are moderate (~500 mm rainfall). Maalouf et al. [34] also found dierent tolerance levels to water deﬁcits. The existence of wide genotypic variations makes it possible to develop drought-tolerant faba bean genotypes through classical breeding approaches. The plant developmental stage and the magnitude of water deﬁcit determine the yield loss of the faba bean. The most susceptible stages for developmental inhibition have been variously described as ﬂowering [35], early podding [36] and pod setting [37], but all of these studies generally agree that the early reproductive phase is the most sensitive stage [19,38]. Moderate drought stress had a negative eect on the pod number per plant but had no eect on the seed size or seed number per pod [35,39]. The extent of drought stress determined whether the plant had partial damage or complete death. These observations highlight the importance of identifying the developmental stage when assessing the impact of drought conditions in faba beans. Seed quality is also aected by water deﬁcit. Genotypic background and environmental factors, i.e., drought and heat, are the major factors that regulate seed protein contents [40]. Winter faba beans have slightly higher protein concentrations than spring beans, which may be interpreted as an indication that water deﬁcits tend to increase protein contents [41]. Faba bean crops grown in water-deﬁcit conditions have improved proteins [42] and sulphur contents [43] compared to those grown with adequate water. In drought-prone environments, reduced protein biosynthesis is due to reducing the N ﬁxation and partitioning [44]. On the other hand, Smith [45] reported that droughts caused yield reductions but did not alter the mineral nutritional quality (calcium, iron, potassium, magnesium, phosphorus, sulphur and zinc) or amino acid concentrations in the common bean. Generally, seed mineral uptake is not impacted by drought. A high N ﬁxation is usually observed in the faba bean under optimal conditions, whereas droughts can considerably impair the N ﬁxation [46,47]. Under water deﬁcits, modiﬁcations of the bacteroid environment cause the decline in N ﬁxation [48] and reduced nodule numbers in faba beans [49]. Combined, these observations illustrate the importance of physiological responses to droughts in the faba bean and the inﬂuence this has on crop yields and yield quality. It is therefore important to identify tools by which the physiological status may be quantiﬁed to assist in management and breeding to help mitigate the eects of drought conditions on plant performances. 1.2. Physiological Attributes Related to Stress Adaptation It is well-established that the phenotypic selection, based on adaptive traits that are secondary to yield, can be used for improving production in water-limited environments [50–52]. Secondary traits chosen for this purpose should be genetically associated with yield in the target environment, highly heritable and easy to measure. Drought-tolerance trait selections were found to be more meaningful when conducted on a large population [53]. Several physiological traits, including water use eciency (WUE) [31], stomatal features [54–56], leaf temperature and carbon isotope discrimination [19], have Agronomy 2020, 10, 1345 5 of 19 been found to be suitable selection criterion for the improvement of drought adaptation in faba bean breeding programs. 3+ Drought stress interacts with low temperatures, soil salinity and Al toxicity. Salinity and drought 3+ aect the osmotic equilibrium in a similar way [57], while Al toxicity hampers root development [58], and cold aects both the movement of water within roots and the ability of the plant to develop symbiosis [59]. Among legumes, Al-drought interactions have been studied in the common bean [60] 3+ and soybean (Glycine max (L.) Merr.) [61], and the Al toxicity exacerbated the eects of the drought mainly due to its inhibition of root growth. On the other hand, the drought was reported to ameliorate 3+ Al injury by reducing the uptake of the toxic ion. The Al-drought interaction has a synergistic eect on crops, rendering them unable to recover after exposure to these stresses. Salinity coupled with drought reduced the symbiotic nitrogen ﬁxation, which may be due to its eect on the supply of photosynthates or oxygen to the nodule and bacteroids [62]. Crosstalk in stress signalling and gene expression has been reviewed in drought and cold stress responses [63] and in cold and salinity responses [57]. In the faba bean, little genetic connection between the drought response and freezing tolerance was observed [64]. 2. Root Traits Compared with the aboveground traits, relatively few studies have been performed on belowground traits. A root trait analysis is complex, involving clumsy measurement systems, so maintaining a high level of precision is dicult in ﬁeld level screening [65]. Among the root architectural features, morphology and plasticity are the two general types of variation that exist. Genetic variations in root morphological characteristics have a signiﬁcant inﬂuence on the capacity and ecacy of a plant to search for and absorb moisture and nutrients from the soil. Deep-rooted soybean genotypes have a higher water-absorption capacity from deep horizons of soil, leading to a higher yield potential [66]. Moreover, the alteration of the root architecture (plasticity) follows several mechanisms under stress and nutrient availability. For example, the root/shoot biomass ratio increased in white lupin (Lupinus albus L.) and Andean lupin (L. mutabilis Sweet) during water deﬁcit [67]. Changes in the root density of L. angustifolius genotypes in response to phosphorus availability have also been observed [68]. Faba bean genotypes with extensive and proliﬁc root characteristics usually exhibit drought tolerance [29]. A variability in the root characteristics and root-based phenotyping for drought tolerance was also found in cowpeas [69], chickpeas [65,70,71], lentils [72,73] and the common bean [74]. Under water-deﬁcit conditions, Husain et al. [75] showed an increased root growth per unit area during the ﬂowering stage. Manschadi et al. [27] described the root length density, along with the dry root weight, and both were considerably reduced under drought conditions. Belachew et al. [26] identiﬁed root phenotypic markers associated with drought avoidance characteristics in young faba bean plants in GROWSCREEN-Rhizo boxes, a phenotyping robotic tool for measuring root and shoot growths [76]. Accordingly, two faba bean accessions (IG 70622 and IG 11320) that exhibit deeper root systems and higher root area coverage, displayed drought-avoidance traits through the maintenance of their primary and tertiary root lengths relatively well. The same observation was noted by Muktadir et al. [77] while screening drought-adapted genotypes in a hydroponic screening system. The growth of the tap root in the faba bean is a major inﬂuence on the total rooting depth; however, the tap root appears unable to acquire water for growth, even if the root surface has access to it. At shallow depths, lateral root growth is important for access to surface moisture and nutrients and is thought to be a major inﬂuence on plant health. Selection on the basis of rapid growth of the taproot and expansion of the lateral root system to maintain the root length density and dry root weight may be an eective method for increasing drought adaptation in faba bean breeding programs. There has been limited research on the genetic variability of root growth and branching in faba beans. Appropriate measurements of root systems include root mass, root mass fraction, rooting volume, root length and Agronomy 2020, 10, 1345 6 of 19 root/shoot ratio. Among them, the root mass is probably the easiest to measure, as, in chickpeas, it was strongly correlated to the shoot mass and represented 30–34% of the total dry matter [65]. 3. Shoot Related Traits Under stress conditions, selection for a higher yield is not always eective, because yield is controlled by several traits controlled by quantitative trait loci (QTL). To select genotypes for drought tolerance, the breeding process should be focused on the contributing characteristics rather than the yield itself. Contributing characters need to be causal, and shoot-related traits play a vital role in maintaining the water status when grown in water-deﬁcit conditions. 3.1. Leaf/Canopy Temperature The temperature of the exterior of the canopy is related to the vapour pressure deﬁcit and directly inﬂuences the amount of transpiration that leads to cooling by evaporation. Direct and easy measurement of the canopy temperature (CT) without disturbing the crop can be completed by using an infrared thermometer (IRT), which can be mounted on a drone to cover a large area in a relatively short time to minimise environmental ﬂuctuations. Blum et al. [78] introduced CT as a selection trait for dehydration tolerance. During water-deﬁcit conditions, closed stomata cause a decrease in transpiration, which ultimately leads to an increase in leaf temperature [79,80]. In ﬁeld conditions, maintaining a lower CT is generally linked with improving the absorption capacity of a plant under stress conditions [81]. CT can be used as a substitute selection trait to screen faba bean genotypes grown in control environments [19,22]. In a large set of faba bean germplasm collected from regions with contrasting moisture regimes around the globe, the leaﬂet and canopy temperatures were the most informative measurements distinguishing the germplasm from wet and dry origins [82,83]. CT has been found to be a prominent trait associated with drought tolerance for soybeans [84], chickpeas [85–87], cowpeas [88] and lentils [89]. The preference for use of CT is its noninvasive nature and application to early evaluations in large numbers of genotypes. The protocol for using an IRT should be followed carefully to avoid a large variance error and nonrepeatable results. Thermal infrared imaging of crop canopies is a further technology for the study of stomatal responses and for phenotyping plants for dierences in stomatal behaviours. The use of remote imaging, when combined with an eective image analysis tool, provides a powerful approach for the comparison of large germplasm collections in typical ﬁeld conditions [90]. 3.2. Leaf Water Relations During water-deﬁcit conditions, plants may maintain the water potential by the production and accumulation of cellular metabolites/osmotica, which are sensed by stomata for the maintenance of sustaining the turgor pressure. Plant species and their developmental stages are the determinants of the types and functions of these metabolites. Relatively few candidate molecules can function as cellular osmotica, as they must be compatible with cellular functions at high concentrations. These candidate molecules may be organic acids, inorganic ions, polyols, polyamines and carbohydrates. In chickpeas, carbohydrates and polyols contribute more than 50% to the osmotic pool [23], and in ﬁeld peas, these ranged from 10–46% [91]. More broadly, the osmotic potential ( s) and turgor potential ( p), the two main components of leaf water potential ( ), were found to be an eective selection trait for drought tolerance screening. Generally, leaf is considered a major component of the leaf-level water deﬁcit [92], and it can ultimately drive interpretations of the plant water status [93,94]. Sustaining leaf under stress involves a number of mechanisms that are related to both root and shoot and are considered to be connected to drought avoidance [95]. Higher leaf turgor in response to water deﬁcit is one of the adaptation strategies for many plant species [96,97]. Osmotic adjustment-driven drought adaptation was also observed in chickpeas [98,99], ﬁeld peas [100] and lentils [101,102]. In faba beans, drought tolerance through osmotic adjustment has not yet been demonstrated in the wide germplasm but, as a selection criterion under drought, is sporadically observed, e.g., [103]. Metabolic adjustments Agronomy 2020, 10, 1345 7 of 19 in response to drought conditions may highlight pools of metabolites that play vital roles in the metabolism and physiology and may indicate which pathways have been perturbed by the stress. 3.3. Relative Water Content The relative water content (RWC) is a robust and simply assessable selection criterion that can describe the plant water status to the metabolism irrespective of plant parts and species. It can be expressed as the water content of tissues in normal conditions compared to hydrated conditions [104]. During water-deﬁcit conditions, the RWC plays an important role by preserving water (stomatal features, leaf area reduction and leaves dropping) or maximising the water absorption (root plasticity). Sinclair and Ludlow [105] found the RWC superior over water potential to assess plant water statuses. Khazaei et al. [55] stated the RWC as one of the most important traits that diered between wet- and dry-adapted faba bean accessions under nonstress conditions. The RWC is composed of a relative change in cell turgor and s, so it relates to both the solute concentrations and cell wall rigidity [106]. The RWC can eciently identify drought-tolerant genotypes based on their plant water status in faba beans [19,82,107], common beans [108] and chickpeas [109,110]. Therefore, it can be said that genotypes that can sustain a higher RWC in a water deﬁcit environment would be suitable for use in breeding faba beans for drought adaptation. 3.4. Stomatal Conductance Drought avoidance involves the maintenance of gas exchange during drought conditions, which causes either higher stomatal conductance, g (low stomatal sensitivity to drought) or stomatal closure to restrict water loss. There is a trade-o between gas exchange and stomatal closure during stress, which ultimately aects photosynthesis and, then, carbon assimilation. Stomatal conductance has been proposed as an eective selection tool and, when measured on multiple plants in a canopy, is equally eective as CT [111]. The measurement of g depends on several stomatal features. Faba bean stomatal characteristics are assessed through microscopy [25,29], but due to the rapid response to stress, the stomatal opening size is hard to measure. Leaf porometer or portable photosynthesis machines quantify g but may not reﬂect the variability over longer timeframes, as it changes rapidly. The measurement of g is highly inﬂuenced by environmental conditions (high genotype by environment interaction), time of day and plant developmental stage. Leport et al. [101] found that white lupin, chickpeas, faba beans, ﬁeld peas, grass peas (Lathyrus sativus L.) and lentils all responded similarly under water-deﬁcit conditions. During early stage drought, g was remarkably reduced, but at later stages, after the initiation of pod ﬁlling, it had little or no eect. Faba bean genotypes with higher stomatal density were lower-yielding and exhibited low drought tolerance, while genotypes with low stomatal density performed better in stress conditions [56]. In a relatively small set of faba bean germplasm, g was found to be an important vital trait [19,112]. The considerable variation for g among 402 faba bean accessions under nonstress conditions indicates the potential use of this trait [25]. The drought treatment of faba beans during the ﬁrst three weeks of growth resulted in the expected reductions in biomass and g [113]. The gas exchange measurements, along with stomatal morphology characteristics, have been genetically mapped in the faba bean. The QTL governing stomatal morphology, g and CT were all co-located in faba bean chromosome 2 [83]. A study of the gene actions showed that breeders selecting for the productivity of faba beans can maximise genetic gain by selecting early generations for CT and g [114]. The eectiveness of stomatal control over transpiration eciency increases if nonstomatal transpiration pathways are restricted. An important nonstomatal water vapour pathway is the leaf cuticle. The epicuticular wax (ECW) quantity is considered as an important drought avoidance strategy in plant species. There was a considerable variation for ECW in 197 faba bean accessions, ranging from 0.680 to 2.104 mg/dm [115]. This variation may allow the genetic improvement of ECW as a drought-adaptive character in faba bean breeding programs. Agronomy 2020, 10, 1345 8 of 19 3.5. Carbon Isotope Discrimination Carbon isotope discrimination (D) is proposed extensively as a proxy for the plant physiological status, especially WUE [116]. It is used to evaluate the transpiration eciency (TE) in cereals and, more recently, in legumes, common beans [117–119], soybeans [120], chickpeas [121], cowpeas [122] and lentils [123]. In faba beans, drought-tolerant genotypes ILB 938 and Mélodie had signiﬁcantly lower D than those of the drought-susceptible genotypes, e.g., Aurora [19]. In a larger faba bean germplasm, D varied from 24.43% to 28.82‰, equivalent to an intrinsic water use eciency (WUE ) of 98.53–179.75 mol CO mol H O (manuscript in preparation). There is some controversy regarding 2 2 the relationship between D and TE. Turner et al. [123] argued that TE was not signiﬁcantly correlated with D in three grain legumes, i.e., lentils, narrow-leafed lupin (L. angustifolius L.) and chickpeas. Carbon isotope discrimination may not always indicate the prediction of actual WUE, because generally, D is measured from leaf tissue, which has limitations for estimating short-term environmental changes [124]. Carbon isotope discrimination-based screening methods are expensive and require sophisticated and costly instrumentation, e.g., isotope ratio mass spectrometry (IRMS). A wider spectrum of faba bean germplasm needs to be surveyed for genetic variations in D under various environmental conditions to allow D to be used as a strong screening tool in faba breeding programs. 4. Metabolomics for Legume Breeding Metabolomics is a fast-emerging area of knowledge that integrates gene expression, protein interaction and other regulatory progressions. Nowadays, metabolic products are used as biomarkers in crop improvement due to their strong linkage with environmental characteristics [125]. So far, more than 200,000 metabolites have been identiﬁed in plants. These have a diverse set of functions and quantiﬁcation, and the qualiﬁcation of these composite characteristics into subsets of metabolic functions can oer a unique view of the inducible chemical and physiological response mechanisms [126]. The identiﬁcation and quantiﬁcation of low molecular weight metabolites require special analytical and separation techniques involving gas chromatography (GC) [127], liquid chromatography (LC) [127,128] and high-performance liquid chromatography (HPLC) [129]. These methods can characterise a vast range of metabolites at extraordinary scales and accuracy. Recently, nuclear magnetic resonance (NMR) has provided a greater ability for researchers to proﬁle metabolites [130]. Metabolic proﬁling studies of grain legumes are relatively unexplored and seemingly absent for faba beans. Zhang et al. [131] studied metabolic variations between symbionts in Medicago truncatula Gaertn. through an untargeted quantitative mass spectrometry-based (MS) method. Short-term water deﬁcit eects on the overall growth through metabolic changes were studied by NMR-based metabolic proﬁling [132]. Plants produce many primary and secondary metabolites during stress. Two dierent options can deﬁne this process: osmotic adjustment, where the plant regulates solute synthesis to decrease the osmotic potential under adverse situations [133], and solute accumulation, which occurs due to reductions, interruptions or ﬂuctuations in the solute transport [134]. Generally, osmotica are easily synthesised from readily accessible antecedents and are transformed to metabolically active and movable compounds. Overall, pre-existing metabolomic resources for legume research will beneﬁt faba bean improvements. However, accelerated applications of these tools may uncover new solutes/biochemical markers for stress tolerance in faba bean breeding. 4.1. Metabolite Accumulation in Legumes in Response to Drought and Their Use as Biomarkers 4.1.1. Amino Acids The accumulation of amino acids and other nitrogen-based molecules in response to stress is one of the most important biochemical signals for almost all plants. These essential metabolites are shown to accumulate during stresses in dierent legumes, including the model species M. truncatula and soybeans [135–139]. The accumulated enhanced protein breakdown is triggered by stress, and a higher amino acid concentration helps a plant to survive under stress [140]. Agronomy 2020, 10, 1345 9 of 19 Proline is found to be the most prevalent amino acid found in plant tissues under stress conditions (drought, cold and salinity). Singh et al. [141] demonstrated a correlation between drought and an increased free proline accumulation in drought-tolerant barley cultivars compared to a more drought-susceptible genotype. Similar correlations have been found in other crops [142], but there are also reports of poor correlations between drought and proline accumulations [143] in legume species. For example, Lotus spp. and soybeans showed a positive association with increased proline concentrations during the reproductive stage only [132,144]. Again, during water deﬁcit, proline accumulation was observed in the pre-ﬂowering stage of peanuts (Arachis hypogaea L.) [145]. Proline accumulation relies not only on the water status but, also, on the growth stage of the plant. Short-term stress can be identiﬁed through proline quantiﬁcation. Venekamp et al. [146] found that just one day of water deﬁcit at the seedling stage induced proline accumulation. An increased proline concentration in faba beans was observed with the increase of the stress intensity, and the variation in proline concentrations at the genotypic level was reported to be low under optimal conditions [46,107,147,148]. However, an exogenous proline application can decrease stomatal opening under drought, and this had a positive impact on drought tolerance mechanisms [149,150]. Proline accumulation provides an indication of the plant physiological status, i.e., whether it is stressed or not, but not a descriptive drought tolerance indicator in faba beans. An exogenous application of -aminobutyric acid (BABA) as a nonprotein amino acid was shown to enhance the accumulation of proline and soluble sugars, which improved drought adaptation in faba beans [151]. Besides proline accumulation, other amino acids are also observed in response to droughts in plants [152]. In lentils, methionine, isoleucine, valine, arginine and histidine increased under drought stress [138]. Drought stress-mediated GABA (gamma-aminobutyric acid) synthesis was observed in 2+ Arabidopsis thaliana, soybeans and common beans [153]. Abiotic stresses enhanced cytosolic Ca levels, which ultimately promoted GABA synthesis, but until now, no evidence was found where GABA stimulated the stomata opening or closing through its ion transporter function [154]. 4.1.2. Polyamines Another plant response to abiotic stresses is polyamines (PA) synthesis, but the association between PA accumulation and fortiﬁcation remains inconclusive. Three commonly found polyamines are putrescine, spermidine and spermine. Usually, stress-tolerant accessions contain a higher amount of PA than sensitive accessions [155,156]. Nevertheless, all three PAs do not accumulate at the same time, but one type of PA shows a stronger response. For example, under PEG-osmotic stress conditions, lentil cotyledons and roots exhibited increased putrescine and spermidine, while the cadaverine presence was nonsigniﬁcant. Drought-adapted yellow lupin (L. luteus L.) accessions produced a high amount of PAs compared to moderately adapted genotypes. Drought stress also increased the concentrations of spermidine and spermine [156]. Beside leaves, seeds commonly exhibit opposite trends, where leaves accumulate more Pas, and the seed content is reduced. Nayyar et al. [157] observed more PA accumulations in chickpeas compared to soybeans under water-deﬁcit conditions. In relay cropping with legumes, 18 rice (Oryza sativa L.) cultivars showed signiﬁcantly higher spermine levels when exposed under salt stress [158]. With this information, it can be said that PA accumulation does not depend on a single factor. Multiple factors like plant species, stress type and level, and the physiological status of the studied tissues, are involved. The PA dynamics of abiotic stress eects can unveil contradictory results of PA accumulation. The stress tolerance of a given species often correlates with the PA pool size, which can answer some underlying questions about the importance of PAs in assisting the protection against stresses. In faba beans, spermine, cadaverine and total polyamine increased in parallel with the salinity level, whereas the putrescine and spermidine levels decreased [159]. In faba beans, PA accumulations in response to drought stress have not been studied to date. Agronomy 2020, 10, 1345 10 of 19 4.1.3. Organic Acids Organic acid plays an important role in plant metabolism as an early source of photosynthesis and precursors of the synthesis of many other compounds. Organic acids support stomata regulation, ion equilibrium, ammonium manufacture and nutrient absorption [160]. Among the proﬁled metabolite classes estimated from soybean leaf tissue, organic acids occupy around 20% of the metabolites [161]. Nitrogen ﬁxation in the nodule is impacted by the malic acid concentration, which regulates the bacteroid respiration [162]. The abundance of organic acids also depends on the type of organ. Organic acid concentrations were lower in lentil root tissue than in cotyledon tissue [138]. Sassi et al. [163] observed a reduced amount of organic acids in common bean leaves under osmotic stress conditions. The amount of succinate was doubled in drought-treated soybean leaves. In lentils, isocitric, nicotinic and oxaloacetic acid concentrations increased considerably in plants exposed to osmotic stress [164]. In soybeans, reduced amounts of organic acids in drought-adapted genotypes suggested metabolic ﬂexibility, as plants shifted from growth to survival [132]. Organic acid functions in response to stress in faba beans have not yet been demonstrated, but it could become an area for future enquiry. 4.1.4. Carbohydrates Carbohydrates are often referred to as appropriate osmotica and represent one of the main components of osmoregulation in many plant species [165]. The metabolic proﬁling of the model forage legume Lotus japonicus L. when aected by drought showed the accumulation of the sugars fructose, galactose, glucose and maltose, while arabitol, ununitol and galactitol were the most abundant polyols [144]. In soybean leaves, about 30% of the metabolites identiﬁed were soluble sugars and sugar alcohols, which are important for plant adaptation against stresses, especially during water deﬁcits [161]. The close association among carbohydrates and their involvement in the primary metabolism suggested a molecular modiﬁcation may be possible to improve the stress tolerance through the synthesis and degradation of these compounds [166]. However, there is no general acceptance of the hypothesis that “osmotic adjustment arises from the accumulation of solute due to the persistence of photosynthesis after cessation of leaf growth” [133]. Among the dominant carbohydrates, trehalose, a nonreducing disaccharide, accumulates in large quantities in the unusual desiccation-tolerant plant Myrothamnus ﬂabellifolia Wolw. [167,168]. High levels of trehalose can stabilise proteins and membranes [169]. It has been recently reported that rhizobium inoculation can also increase the dehydration tolerance of several legume species through trehalose biosynthesis [170–173]. Moreover, an increased trehalose concentration was found to be a signiﬁcant contributor to drought tolerance [174]. Polyhydric alcohols or polyols are a major metabolite group reviewed by Merchant and Richter [175]. The quantity of polyols found in plant tissues was found to be sensitive to environmental conditions [176,177]. Further, Dumschott et al. [178] characterised D-pinitol as being inﬂuenced by the developmental stage. D-Pinitol is present in most legumes at some level under optimal conditions, but an increase is triggered during water and salinity stress [179]. While there is a general consensus on the function of pinitol in plant systems, gaps remain in understanding the conditions leading to pinitol accumulation, as well as the molecular control of the accumulation. 5. Faba Bean Genetic Resource to Aid Breeding for Drought Adaption A wealth of faba germplasm is available, comprising over 43,000 accessions (Dr. Kenneth Street, personal communication) that are conserved mostly within 37 global gene banks. The ICARDA (International Centre for Agricultural Research in the Dry Areas) collection exceeds 9000 accessions (21% of the global collection) [55]. Wide genetic variations have already been reported in faba bean genetic resources for various traits, including physiological traits related to drought adaptation (reviewed in [82]). This enormous variability is expected in this ancient domesticated crop with its wide adaptability to various latitudes and altitudes. The rich germplasm collection of faba beans Agronomy 2020, 10, 1345 11 of 19 should be systematically maintained and could be characterised for the physiological and metabolic parameters in order to improve drought adaptation in this species. 6. Conclusions Improvement of global faba bean production will have a positive impact on the food supply and cropping systems of many nations. Tools to improve faba bean production will incorporate both management activities and improved genotypes. The adoption of these tools must balance the necessity for broad-scale characterisations and cost with the precision required for appropriate detection at the plant scale. Many traits have been identiﬁed for drought tolerance studies. Some traits, like canopy temperature, can be used eciently for large numbers of genotypes in breeding programs, while, for example, carbon isotope discrimination is largely limited to low numbers of genotypes. Metabolite-based biomarkers and bioindicators can easily supplement the selection process in faba bean breeding programs. The identiﬁcation and quantiﬁcation of given primary and/or secondary metabolites against speciﬁc stresses could become valuable decision-making tools for plant breeders if their associations are of sucient strength and their analytical costs are low. The available metabolomic resources from other legumes should be explored to understand the molecular insights of stresses. The large genome of the faba bean is currently being sequenced, which will soon make molecular breeding possible. Finally, no single trait and approach are adequate to improve yields under drought conditions, the most complex environmental factor for faba bean productivity. A combination of screening methods suitable for speciﬁc environments and expansion of the scale of breeding will be required to allow expansion of the production area and yield of the faba bean, a crop that is an increasingly important source of plant-based protein in drought-prone production regions. Author Contributions: Writing—original draft preparation, M.A.M., and writing—review and editing, K.N.A., A.M., K.Y.B., A.V., F.L.S. and H.K. All authors have contributed, read and agreed to the published version of the manuscript. Funding: M.A.M. acknowledges the support from University of Sydney International Scholarship and also supplemented by the Grains Research and Development Corporation. K.Y.B.’s participation was funded by the European Union through its ERANET SusCrop projects “ProFaba” and “LegumeGap”. H.K. acknowledges funding from Agriculture Development Fund (Government of Saskatchewan, Canada); Western Grains Research Foundation, Canada; Saskatchewan Pulse Growers, Canada; and the NORFAB (Protein for the Northern Hemisphere) project funded by Innovation Fund, Denmark. 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Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review

Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review

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Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review

Physiological and Biochemical Basis of Faba Bean Breeding for Drought Adaptation—A Review

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