Received: 30 May 2021 | Revised: 26 November 2021 | Accepted: 3 December 2021 DOI: 10.1002/fes3.351 R E V I E W Drought and heat affect common bean minerals and human diet— What we know and where to go Alessia Losa1 | Juan Vorster2 | Eleonora Cominelli3 | Francesca Sparvoli3 | Dario Paolo3 | Tea Sala1 | Marika Ferrari4 | Marina Carbonaro4 | Stefania Marconi4 | Emanuela Camilli4 | Emmanuelle Reboul5 | Boaz Waswa6 | Beatrice Ekesa6 | Francisco Aragão7 | Karl Kunert2 1Council for Research in Agriculture and Economics, Research Centre for Abstract Genomics and Bioinformatics (CREA- Global climate change, causing large parts of the world to become drier with GB), Montanaso, Italy longer drought periods, severely affects production of common beans (Phaseolus 2Department Plant and Soil Sciences, Forestry and Agricultural vulgaris L.). The bean is worldwide the most produced and consumed food grain Biotechnology Institute, University of legume in the human diet. In common beans, adapted to moderate climates, ex- Pretoria, Pretoria, South Africa posure to drought/heat stress not only results in significant reduction of bean 3National Research Council, Institute of yield but also the nutritional value. This review explores the contribution of com- Agricultural Biology and Biotechnology (CNR- IBBA), Milan, Italy mon beans to food and nutrient security as well as health. Also discussed is the 4Council for Agricultural Research and existing knowledge of the impact of drought/heat stress, associated with a chang- Economics, Research Centre for Food ing climate, specifically on iron (Fe) and phytic acid (PA) that are both among and Nutrition (CREA- AN), Rome, Italy the most important mineral and anti- nutritional compounds found in common 5Aix- Marseille University, INRAE, INSERM, C2VN, Marseille, France beans. Further discussed is how the application of modern “omics” tools con- 6International Center for Tropical tributes in common beans to higher drought/heat tolerance as well as to higher Agriculture (CIAT), CIAT Regional Fe and reduced PA content. Finally, possible future actions are discussed to de- Office for Africa, Nairobi, Kenya velop new common bean varieties with both improved drought/heat tolerance 7Embrapa Recursos Genéticos e Biotecnologia, Norte, Brazil and higher mineral (Fe) content. Correspondence K E Y W O R D S Karl Kunert, Department Plant and antinutrients, biofortification, climate change, common bean, drought/heat, legumes, Soil Sciences, Forestry and Agricultural minerals, Phaseolus vulgaris, phytic acid, pulses Biotechnology Institute, University of Pretoria, Hillcrest, Pretoria 0002, South Africa. Email: karl.kunert@up.ac.za Funding information ERA- NET co- funding on Food Systems and Climate (FOSC) BIO- BELIEF project (Reference Number: FOSC- 288) This is an open access article under the terms of the Creat ive Common s Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Food and Energy Security published by John Wiley & Sons Ltd. Food Energy Secur. 2021;00:e351. wileyonlinelibrary.com/journal/fes3 | 1 of 28 https://doi.org/10.1002/fes3.351 2 of 28 | LOSA et al. 1 | INTRODUCTION system is dependent on rainfall, such as on the Southern Plains of the USA and in eastern Africa (Adhikari et al., 1.1 | Climate change and crop 2015; Ahmed & Stepp, 2016; Steiner et al., 2018). Impacts production of drought/heat range from negatively affecting all plant development stages with key physiological, biochemical Global climate change will severely affect the UN goal and metabolic pathways seriously disrupted (Dankher to sustainably produce enough food by 2050 to feed a & Foyer, 2018). Temperature extremes are further more projected global population of 9.1 billion people. This is strongly associated with a reduction in crop yield, com- despite previous progress in addressing global undernu- pared to precipitation extremes, and irrigation partly lim- trition with increased food production by agricultural its the negative effects of high temperatures (Vogel et al., expansion and intensification (Myers et al., 2017). Global 2019). While plants are always exposed to a combination climate change, which has a long- term impact in the form of stresses under field conditions (Hussain et al., 2018), of different abiotic stresses (Redden, 2013), will particu- most studies have focused on the impact of individual larly cause large parts of the world to become drier with stresses on crop yield (Fahad et al., 2017). Combined longer drought periods, more intense heat and irregular drought and high temperature stress is known to reduce rainfall. These changes will severely affect agriculture as yields of maize, soybean and wheat (Matiu et al., 2017). well as the stability and distribution of food production Physiological characterization of plants exposed to either (Kellogg & Schware, 2019). These changes in the climatic drought or heat stress, or a combination of both stresses, conditions might even become progressively worse (Hao has indicated that combined stresses have several dis- et al., 2018). A major factor in driving such temperature tinctive characteristics. These characteristics include low increase and altering precipitation patterns is a higher at- photosynthesis combined with increased respiration and mospheric carbon dioxide (CO2) concentration (Kellogg & closed stomata combined with increased leaf temperature Schware, 2019; Lindsey, 2020). (Mittler, 2006). However, how plants respond to a com- Warmer and drier climatic conditions, resulting in bination of different abiotic stresses cannot be simply in- increased evaporative losses, will also drive the demand ferred by the response of the plant to an individual stress for more water. A substantial part of the world's agricul- (Mittler, 2006). To develop strategies maintaining crop ture is, however, already suffering from chronic soil water productivity under such individual or combined stresses shortages due to severe drought conditions (Nadeem et al., is, therefore, a major future research challenge (Ferguson, 2019). Predicted shifts in crop production, due to regional 2019). changes in temperature and rainfall patterns, might fur- ther worsen local food shortages. The future demand for affordable nutritious food will, therefore, require integra- 1.3 | Potential of legumes tion of such regional predictions within drought moni- toring and forecasting (Leisner, 2020; Mbiriri et al., 2018; Legumes, as members of the large Fabaceae (Leguminosae) Myers et al., 2017; Parsons et al., 2019; Zolina et al., 2013). family, are predominantly grown in the world's tropical and subtropical areas. The production and consumption of pulses, the edible seeds of legumes, has further greatly 1.2 | Drought/heat stress and increased over the last 15 years (Rawal & Navarro, 2019). plant growth Legumes include a number of important agricultural and food plants, such as Glycine max (soybean) and Phaseolus Stresses associated with a changing climate are predicted species (beans). They have an important function in both to severely impact plant metabolism as well as soil fertil- the diversification and sustainable intensification of agri- ity and carbon sequestration. This impact will limit plant culture. Apart from being a major dietary protein source, growth and productivity and, ultimately, availability of legumes are a rich source of minerals to humans and ani- nutritious food (Dankher & Foyer, 2018; Myers et al., mals. Stresses, associated with changing climatic condi- 2017). A higher atmospheric CO2 concentration affects, for tions, pose, however, a severe threat towards their growth, example, the nutritional composition of crops by reduc- yield potential as well as nutritional value (Foyer et al., ing the protein content of the edible plant parts and also 2016; Gepts et al., 2008; Latef & Ahmad, 2015; Nadeem lowering concentrations of important minerals (Loladze, et al., 2019; Sica et al., 2021; Vasconcelos et al., 2020). An 2014; Medek et al., 2017; Myers et al., 2014). In particular, important feature of legumes is further the ability to form soil water deficit, due to drought/heat conditions, causes root nodules allowing to fix atmospheric nitrogen. With considerable reduction in plant productivity. This reduc- the help of rhizobia, legumes reduce atmospheric nitro- tion is specifically evident in areas where the agricultural gen to ammonia in these root nodules with various genes LOSA et al. | 3 of 28 required for symbiotic nitrogen fixation (SNF) (Roy et al., a reduction in nutrient uptake particularly occur after 2020). The natural ability to add fixed nitrogen into soils exposure to drought/heat stress, (Mathobo et al., 2017; renders legumes a keystone species for natural and agri- Nadeem et al., 2019; Zadražnik et al., 2013). In addition, cultural ecosystems, injecting over 50 million tons of nitro- a shallow root system further renders common beans vul- gen into the soil per annum (Roy et al., 2020). SNF, which nerable to any shortage of soil water with the reproductive significantly contributes not only to protein production stage, which includes flowering and pod-f illing, also very but also to increase in soil fertility (Sørensen & Sessitsch, drought- sensitive (Daryanto et al., 2017). 2007; Wagner, 2011), is, however, highly drought sensitive Adaptation, particularly to drought conditions, in- (Kunert et al., 2016). cludes the improvement in the photosynthetic capacity, water- use efficiency and adaptation to different environ- ments. Such adaptation has been already found in a few 1.4 | Common beans and abiotic stress common bean genotypes, including the BAT477 race (Beebe et al., 2008; Polania, Rao, et al., 2016), and selec- Among the legumes, common bean (Phaseolus vulgaris L.; tion for drought resistance improved yield in phosphorus Figure 1), which is the focus of this review, is the most limited environments (Beebe et al., 2008). Root traits for produced and consumed food grain legume worldwide. improved water uptake include existence of more small Common beans are adapted to relatively moderate cli- fine roots, higher root length as well as higher root den- matic conditions and not to extreme climatic and edaphic sity (Fenta et al., 2020; Polania et al., 2017). In drought- environments. Day temperature exceeding 30°C or night tolerant common beans, maturity acceleration with a temperatures higher than 20°C can significantly reduce high seed filling rate further limits any drought impact seed yield due to flower abscission, development of par- (Rosales- Serna et al., 2004). Besides improved remobili- thenocarpic pods (pin pods), lower seed set per pod as zation and partitioning of photosynthates (Teran et al., well as decreased seed size (Rainey & Griffiths, 2005). Soil 2019), a change of canopy biomass and harvest index has degradation and factors, such as soil acidy and aluminium also been found to contribute in common beans to more toxicity, lead to deficiencies in nitrogen and phosphorus. drought tolerance (Assefa et al., 2015; Polania, Rao, et al., This can limit root development and consequently access 2016). Hageman et al. (2020) further provided evidence to soil moisture (Samago et al., 2018). that resource partitioning from pod walls into seeds and Growth of legumes is generally affected by several abi- the inherent sensitivity of leaflet growth rate to drought otic stresses causing as a response changes in the plant can be used as further indicators for drought sensitivity/ phenotype (Araújo et al., 2015). Among the reported tolerance. When screening 25 common bean genotypes changes in common beans due to abiotic stresses are less with contrasting drought tolerance in a phenotyping leaf expansion due to ultraviolet- B radiation (Riquelme platform under different water supply conditions, gas ex- et al., 2007), increase of production of malondialdehyde, change and osmotic adjustment together with increase in antioxidants and carotenoids, a decrease in the chlo- grain yield were also proposed as useful indicators for se- rophyll content of leaves due to heavy metal exposure lecting more drought- tolerant common bean lines (Lanna (Zengin, 2013), reduction of seedling emergence after et al., 2018). Polania et al. (2016) further reported that the low temperature treatment (De Ron et al., 2016), as well best nitrogen- fixing common bean lines under soil water as suppression of growth, photosynthesis and transpira- deficit are more drought- tolerant. But common bean gen- tion under high soil salinity (Kaymakanova et al., 2008). otypes, even more tolerant to soil water deficit, can ulti- Changes in protein expression, reduced germination, mately be severely affected by nitrogen- deficiency under stunted growth, serious damage to photosynthesis and such soil water deficit (Beebe et al., 2014). F I G U R E 1 Common bean plants (left) and effect of drought on common beans (right) (adapted from Michigan State University Department of Plant, Soil and Microbial Sciences at https://www. canr.msu.edu/beanb reedi ng/resea rch/ drought) 4 of 28 | LOSA et al. Abiotic stresses further affect the nutritional quality of common beans (Sica et al., 2021). Variability in rainfall af- fects, for example, the production of secondary metabolites, such as phenolics. This change directly impacts the bean's health- related benefits and sensory qualities (Ahmed & Stepp, 2016). Mild drought stress increases certain phenolic compounds without affecting the seed yield (Herrera et al., 2019). Studies investigating irrigation effects further found that the total fibre decreases under rain- fed conditions. Water availability, however, also influences the digestibil- ity of bean carbohydrates, extractable polyphenols and, depending on the bean variety, the antioxidant capacity (Ovando- Martínez et al., 2014). Only a few studies have so far investigated in greater detail the impact of stresses as- F I G U R E 2 Effect of drought/heat stress on minerals sociated with climate change, such as drought/heat stress, and phytic acid in common beans and the consequences of on the bean's mineral and antinutrient content with phytic biofortification acid (PA) a potent antinutrient (Hummel et al., 2018). The aim of this review is, therefore, to discuss the cur- rent existing knowledge on the link between drought/heat with the greatest production of common beans, represent- stress and content of Fe and PA in common beans. In our ing about 50% of world volume, followed by Africa with review, we will first provide a short general overview on 25% (Figure 3). In sub- Saharan Africa, common beans are the contribution of common beans to food/nutrient secu- produced on more than 3.5 million ha with production tak- rity as well as health. This will include the guidelines dic- ing place mainly in East Africa, the lakes region and the tated by countries to improve human diet- related habits highlands of Southern Africa, with a combined production and lifestyle, and the role of antinutrients. We will then of almost 1  mt (Demelash, 2018). In Latin America, per review the existing knowledge with regards to Fe and PA capita annual consumption of common beans ranges from content in common beans and how drought/heat stress 10– 18  kg, whereas in East Africa common annual bean affects the content of these two compounds. Figure 2 pro- consumption can be as high as 50 kg per capita. vides a simplified overview of the processes specifically In 2019, Myanmar, India and Brazil were further the reviewed. A discussion will follow on how breeding using top three dry bean producing countries in the world and modern “omics” approaches has so far contributed not Myanmar and India produced each over 5 mt (FAOSTAT, only to more drought/heat stress tolerance in common 2020; Table 1). In Latin America, Brazil was in 2019 the beans but also to identify genes involved in drought/heat main producer of dry beans, with about 2.8 mt, followed by stress tolerance as well as increase in Fe content and re- Mexico with about 0.9 mt. In Europe, only about 544,330 ha duction in the PA content. Finally, we will discuss areas were cultivated with beans, with a production of about for possible future exploration of existing knowledge in 1.9  mt (https://www.pulse sincr ease.eu/crops/ commo n- common beans regarding increasing Fe and antinutrient bean; accessed August 2021). Although having the lowest content particularly under drought/heat stress conditions. production area of all top dry bean producers, the United States of America (Table 1) achieved the highest bean yield in 2019 (1979 kg ha−1). This was most likely due to a better 2 | FOOD AND NUTRIENT technological input and also better seed quality. However, in SECURITY India, despite having the greatest cultivation area, bean yield is still very low (418 kg ha−1; Table 1). Such low yields in 2.1 | Food security countries, such as India, Mexico and Kenya, are very likely due to a low technological input by resource poor farmers, Globally, common beans are grown on 23 million ha (http:// irregularities of rainfall as well as poor seed quality. www.cgiar.org/ our- research/crop- factsheets/beans) and Low input agricultural systems further account for the global common bean production has now risen to 12 the majority of common bean production and small- scale million tons (mt) per year (FAO, 2014, 2018; Heinemann farmers particularly depend on beans for food and income et al., 2016). The bean greatly contributes to overall food (Kermah et al., 2017). They use, however, poor quality and nutrient security particularly in sub- Saharan Africa seed material caused by poor storage, seed-b orne fungal and in Central and Southern American countries (Beebe, infection as well as sowing and harvesting under unfa- 2012; Broughton et al., 2003). Latin America is the region vourable environmental conditions (Oshone et al., 2014). LOSA et al. | 5 of 28 F I G U R E 3 Impact of climate change on the suitability of bean production (adapted from Beebe et al., 2011). White areas represent areas where common beans are either not extensively grown or where climate change might have very little impact on bean growth T A B L E 1 Top common bean Total producing countries in the world Production production Area (ha) (kg/ha) (tons) Myanmar 3.201.135 1826 5.845.272 India 12.690.696 418 5.309.787 Brazil 2.610.585 1113 2.897.749 China 745.936 1739 1.297.182 United Republic of Tanzania 893.570 1340 1.197.383 Uganda 539.660 1815 979.482 United States of America 470.890 1979 931.891 Mexico 1.207.395 728 878.983 Kenya 1.167.543 639 746.059 Note: Source: Food and Agriculture Organization Statistical Databases was used to develop this table; FAOSTAT, 2020). They further grow beans in association, or in rotation, with improved production, especially under soil water deficit maize with minimal production inputs (Rurangwa et al., (Kibido et al., 2020; Samago et al., 2018). Overall, all these 2018). Cereals are thereby grown on more fertile fields problems ultimately limit bean yields to low as ≤0.5 t ha−1. and legumes on soils depleted in nutrients (Chekanai This not only greatly affects smallholder systems (FAO, et al., 2018; Kelly et al., 1998). Due to its existing SNF ca- 2014; Rao et al., 2016), but prevents the realization of the pacity, although lower when compared to soybean and bean's full yield potential and causes production instabil- faba beans (Peoples et al., 2009), common beans can grow ity from 1 year to the other. Most worrying, based on crop on such marginal lands. Although common bean variet- modelling, the majority of current common bean growing ies with high SNF capacity and environmental resilience areas, especially in south- eastern Africa, will be in 2050 would be, therefore, of great benefit (Wilker, 2021), com- unsuitable for bean cultivation greatly affecting food and mon bean breeding seldom includes selection for the SNF nutrient security (Hummel et al., 2018). trait. In addition, modern bean production practices in- As much as one-t hird of bean production areas are fur- volve the application of nitrogen- fertilizer which causes ther influenced by drought/heat stress. This greatly affects not only SNF downregulation but also environmental the contribution of common beans to food and nutrient pollution (Wilker et al., 2019). To solve this problem, security (Beebe et al., 2014; Kazai et al., 2019). Common moderate phosphorus fertilization in combination with bean production areas particularly subjected to frequent an appropriate more affordable Rhizobium inoculation droughts are highland Mexico, the Pacific coast of Central as a nitrogen source might be one potential option for America, northeast Brazil, and eastern and southern 6 of 28 | LOSA et al. Africa from Ethiopia to South Africa (Beebe et al., 2013). Fe and Zn (Beebe et al., 2000; Castro- Guerrero et al., 2016; More than 60% of the world's common beans are cultivated Drewnowski, 2010; Graham et al., 2007; Hall et al., 2017; under non-i rrigated conditions in areas where seasonal Mitchell et al., 2009). For a general overview of the nutri- rainfall is erratic and beans grow under rain-f ed condi- tional value of common beans, see https://feedt ables.com/ tions (Seidel et al., 2016; Smith et al., 2019). Drought/heat conten t/commo n- bean and also Celmeli et al. (2018). Fe stress can cause yield losses of up to 80% in these rain- fed and Zn deficiency further affects over 30% of the world's production systems (Kazai et al., 2019), Specifically, inter- population (Bailey et al., 2015). Common bean has, there- mittent or terminal drought stress causes severe yield loss fore, the potential to not only reduce poverty but also to (Beebe et al., 2013), although drought stress towards the increase nutrient security, particularly on smallholder end of the growing season might not cause much harm for farms (De Luque & Creamer, 2014). The access to diverse, grain yield (Mathobo et al., 2017). Irrigation would, there- nutrient- dense food sources is consequently a priority in fore, allow to increase common bean production. Indeed, order to improve sustainable nutrient security, especially in Brazil yields of around 2900 kg ha−1 have been already in low- income countries and to prevent hidden hunger obtained by irrigation (Alves Souza et al., 2020). (Nelson et al., 2018; Petry et al., 2015). Hidden hunger is Recent modelling studies raise further concern for fu- generally concerned with a deficiency of nutrients and oc- ture food and nutrient security. They predict a significant curs when the food quality in a person's diet is insufficient decrease in the future suitability to grow common beans for normal growth and development. Minerals, such as Fe due to increased drought and also heat stress (Heinemann and Zn, are thereby key determinants in staple crops and et al., 2017). In Africa, for example, where an estimated foods for sufficient dietary micronutrient uptake (Díaz- 682,000 ha of beans are currently cultivated, annual yield Gómez et al., 2017). loss due to drought/heat conditions is already in the range Common beans further present a much better source of 781,000 t. Simulation models to characterize bean pro- for these minerals in comparison to cereals (Castro- duction in Brazil in rain- fed environments also indicate Guerrero et al., 2016). In common beans, the Fe con- that climate change will cause more frequent but less se- centration ranges from 35 to 90  µg/g with an average vere drought conditions (Heinemann et al., 2017). A pre- of 55  μg/g and is higher when compared to crops like vious ecological diversity study with wild common bean rice (6.3– 24.4 µg/g), wheat (25 µg/g–5 6 µg/g) or maize accessions covering a habitat from Mexico to Argentina (9.6– 63.2 µg/g). Breeding approaches have recently even further found that accessions are distributed among differ- achieved a Fe concentration of 130  μg/g (Kimani & ent precipitation regimes following a latitudinal gradient. Warsame, 2019). Common beans also have a relatively The habitat ecological diversity of the collection sites was high Zn seed content (21– 54 µg/g), with an average of further associated with natural sub- populations (Cortés 35 μg/g. Environmental and genotypes can, however, in- et al., 2013). Finally, current common bean areas might fluence seed mineral concentrations as recently found also shift to colder regions of the Northern Hemisphere, with landraces and improved common bean varieties such as Canada, the Nordic countries and Russia, as indi- (Caproni et al., 2020; Hummel et al., 2018; Murube cated by recent model projections (Ramirez- Cabral et al., et al., 2021; Philipo et al., 2020). Although there is no 2016). How these changes will actually affect overall bean statistically significant correlation between Fe and Zn production has still to be investigated in more detail. content of seeds and the geographical distribution of bean (Caproni et al., 2020), previous studies provided evidence for a tendency for Andean pools to contain 2.2 | Nutrient security more Fe (Beebe et al., 2000) and Mesoamerican pools more Zn (Islam et al., 2002). Moreover, in a more recent In contrast to the industrialized world, common bean is study, new multi- parent populations were developed at the most important grain legume consumed in areas with the University of Nairobi. Lines harbouring different a low income where health is influenced mainly by dietary tolerance traits (drought, low soil fertility, major bean deficiencies rather than by excesses. Common beans are diseases) were combined with lines with high mineral therefore also regarded, as other pulses, the “poor man's traits (Fe and Zn). Eighty- four selected lines were more meat”. As a food staple, common beans contribute up to drought- tolerant and had more than 90% better yield 35% of the protein and 340 calories/100 grams to the daily compared to their parents. Forty- six promising lines had diet of resource poor urban and rural families. Food, how- further higher grain Fe and also Zn concentrations com- ever, not only needs to satisfy the caloric requirements, pared with their parents. These lines can possibly now but has ultimately to provide sufficient amounts of nutri- contribute to increased bean productivity and also com- ents such as minerals and vitamins (Muller et al., 2017). bating micronutrient deficiencies in eastern Africa and Common beans are an important source for the minerals other parts of Africa (Kimani & Warsame, 2019). LOSA et al. | 7 of 28 3 | HEALTH 2017; Haas et al., 2016). However, how these lines per- form with regards to yield as well as nutrition under 3.1 | Impact on health drought/heat stress conditions associated with climate change still remains to be investigated. Pregnant women and children are specifically at risk in A previous study on diet modelling also found an their health due to high mineral needs but poor mineral association between bean consumption, improvement intake. While minerals are required by humans in small of nutrient intakes and healthy eating index scores quantities, minerals participate in a wide variety of (Hornick, 2007). Low- quality diets often lack dietary metabolic processes. Fe is, for example, required for the diversity along with high amounts of saturated fat and synthesis of haemoglobin and several hormones. A con- low vegetable, fruit, as well as fibre intake that can con- ventional breeding programme developed in Rwanda tribute to disease risk (Hiza et al., 2013). Consuming dry and in the Democratic Republic of Congo (DRC) already beans results in higher intake (10% or more) of fibre, resulted in the selection of high Fe- containing common protein, folate, Zn, Fe and Mg with lower intake of satu- bean lines. These lines were also well adapted to the local rated fat and total fat which provides an improvement in conditions and suited both the farmers' and consumer the overall diet quality (Mitchell et al., 2009). Replacing preferences (Mulambu et al., 2017). The programme refined carbohydrates in the diet with protein sources HarvestPlus of the Consultative Group for International that are low in saturated fat, as in beans, reduces, for Agricultural Research (CGIAR) particularly focuses example, the risk of cardiovascular diseases (Hu, 2005; on the selection of such Fe bio- fortified common bean Mobley et al., 2014). People following a Mediterranean- lines (Asare- Marfo et al., 2013). African countries, fol- style diet, richer in plant foods, including bean, have, lowed by countries in Latin America, the Caribbean as indeed, a lower risk of cardiovascular disease and mor- well as Asia, rank, therefore, high on the list of coun- tality (Estruch et al., 2006; Serra-M ajem et al., 2006). The tries targeted under the Biofortification Priority Index Dietary Guidelines for Americans (DGA, 2015– 2020) (HarvestPlus, 2020) (Figure 4). Such Fe- biofortified bean (available at https://health.gov/our- work/food- nutri lines have already improved the Fe status and health of tion/previ ous- dietar y- guide lines/2 015, accessed May women in several African countries (Andersson et al., 2021) further consider the beans' nutritional content F I G U R E 4 Common bean Bio- fortification Priority Index. Picture courtesy of HarvestPlus (https://bpi.harves tplus.org/bpi_cropma ps. html?id=c12021) 8 of 28 | LOSA et al. and benefit as both a protein and a vegetable. Beans can, enzyme inhibitors, phenolic compounds, complex poly- therefore, be regarded as either in order to appropriately phenols (tannins) as well as saponins. The presence meet the recommended dietary intakes. The Guidelines of these compounds has promoted the nutraceutical on Nutrition and Physical Activity for Cancer Prevention use of legumes (Carbonaro, 2021). In spite of the well- advocates the consumption of poultry, fish and beans documented antinutritional effects of some legumes, as an alternative to pork, lamb and beef while stress- residual (i.e. below their toxic level) amounts of most bi- ing the importance of vegetables (Kushi et al., 2012). ologically active compounds help in the prevention and The American Heart Association further recommends management of severe diseases, such as cardiovascular consuming 360  g of beans per week for adults for the diseases. These diseases mainly affect the world popu- prevention of cardiovascular diseases (Van Horn et al., lation of industrialized countries (Padhi & Ramdath, 2016). However, the large consumption of bean seeds, as 2017). Hypercholesterolemia (Zhang et al., 2010), type- 2 a “meat replacement” staple food in many countries of diabetes (Mattei et al., 2015) and cancer (Mitchell et al., Africa, Central and South America and Southern Asia, 2009) are diseases which can be prevented. Selection has already contributed to nutritional problems. to decrease the antinutritional substances have been Finally, it should not be overlooked that common bean already done for common bean varieties that are gen- seeds are also an important protein source (16– 30%), de- erally consumed. Cooking and processing are two spite being deficient in sulphur amino acids (methionine methods that also inactivate trypsin inhibitors that are and cysteine). In particular for geographic areas, where a relevant antinutritional factors. These inhibitors re- large part of the dietary protein is obtained from legumes, duce the digestion and absorption of dietary proteins there is a need to increase the content of sulphur con- (Avilés- Gaxiola et al., 2018). Removing antinutritional taining amino acids in legume proteins. Increasing the substances may, however, result in yield reductions as concentration of S- containing amino acids is, therefore, a they also play an additional protective role in patho- current major research task (Saboori- Robat et al., 2019). gen or insect resistance (Boulter, 1982). Varieties with Several legume proteins, including those of common bean a high content of heat- stable (non- protein) compounds, seeds (e.g. 7S globulins, protease inhibitors, lectins), are such as tannins and PA, pose further concern. This is now regarded not only as, but also functional ingredients because protein digestibility is lowered by high molecu- (Carbonaro et al., 2015). Common bean seeds further lar weight tannins (Mr 500– 5000), especially condensed contain no cholesterol and only low amounts of total and tannins (proanthocyanidins). They form strong insolu- saturated fats. They are rich, however, in carbohydrates ble complexes with proteins. Moreover, the reactivity of (up to 60%), especially starch and several vitamins (bio- some tannins, in particular those in common beans, in- tin, folic acid, niacin, thiamine and riboflavin). They are creases after thermal treatment (Carbonaro et al., 1992). further an important source of dietary fibre (up to 37%) Tannins further adversely affect the absorption of trace (Trinidad et al., 2010). Distinctive physiological roles have elements, especially of Fe, but also of Zn and Cu, as a been attributed to the two different fibre fractions: soluble result of tannin– metal complex insolubilization, par- vs. insoluble. Soluble fibre, making up only a small part ticularly after cooking (Carbonaro et al., 2001). As dis- of the total dietary fibre, can assist in lowering cholesterol cussed below, it is now also well documented that the levels as well as decreasing the risk of heart diseases in reg- other major cation chelator in the seed is PA (reviewed ulating blood glucose levels. The regulation of intestinal by Petry et al., 2015). Finally, tannins, PA and saponins function is affected by the insoluble fibre fraction. Studies also interact with the absorption of fat- soluble com- have also produced evidence showing the protective effect pounds including fat-s oluble vitamins and carotenoids. of legume fibres against risk of developing colon cancer (Zhu et al., 2015, Wang et al., 2013; Campos- Vega et al., 2013). Due to this high fibre content, common beans can 4 | MINERALS/PA AND significantly contribute to the recommended dietary fibre DROUGHT/HEAT STRESS intake of adult women (25 g/day) and adult men (38 g/ day) (Dahl & Stewart, 2015). 4.1 | Mineral/PA content In order to provide sufficient minerals to millions of con- 3.2 | Antinutrients sumers, relying on common beans as part of their diet, a better understanding is needed of the effect that particu- Common beans are also a source, as other legumes, of larly drought/heat stress has on bean yield as well as on bioactive compounds. Bioactive compounds in common the bean's mineral and antinutrient content. In this re- bean seeds include oligosaccharides, lectins, phytates, gard, some knowledge already exists from characterizing LOSA et al. | 9 of 28 lentils. Lentil plants exposed to drought and/or heat stress accumulates in the bean seed and in the cotyledons (95– had lower amounts of vital minerals (K, P, Ca, Fe, Mn and 98%), with only a small quantity found in the embryo and Zn). This decrease was further associated with a reduction the seed coat (Blair, Herrera, et al., 2012). PA is further of root biomass under heat stress and a negative effect, due negatively charged and a strong mineral cation chelator. to drought stress, on transpiration, stomatal conductance Any increase in the PA amount due to drought/heat con- as well as root function. When both stresses (drought and ditions is, therefore, of great concern. In experiments car- heat) acted simultaneously on lentil plants, the effect was ried out in the field with different common bean varieties even more profound (Sehgal et al., 2019). Choukri et al. under rain- fed and drought conditions, representing con- (2020) also analysed 100 lentil genotypes from a global ditions forecasted by 2050 for south- eastern Africa by the collection grown under normal, heat and combined heat– EcoCrop climate impact modelling system, a significant drought conditions. Fe, Zn and crude protein content was increase in the PA amount in common beans exposed to significantly reduced under these stress conditions. The drought stress was already found. This increase was from effect of combined heat– drought stress was, however, 0.96% under rain- fed conditions to 1.16% under drought more severe than by heat stress alone. A significant posi- conditions. Fe, Zn and PA under drought stress conditions tive correlation also existed in lentils between Fe and Zn at the field site were further influenced by weather condi- concentrations under both non- stress and stress condi- tions rather than genotype (variety) (Hummel et al., 2018). tions (Choukri et al., 2020). The underlying physiological basis for the PA increase Most efforts to improve the nutritional quality of under drought stress is, however, not well studied. common beans have up to now focused on developing Since data are overall still contradicting and only based varieties with lower amounts of antinutritional com- on a small number of lines and varieties tested, more in- pounds, such as lectins (phyto- hemagglutinin L, phyto- depth investigations are urgently required to more exactly hemagglutinin E), phaseolin and phytates, and a higher determine how drought and heat- associated reductions Fe and Zn content (Cominelli et al., 2020; Samtiya et al., in yield also affects the nutrient quality of common bean 2020; Vasconçelos & Oliveira, 2004). For common beans, seeds and the PA content. Such more detailed investiga- genotypic variation in the content of Mg, sulphur and Fe tions should be carried out, however, not only under com- in bean leaves, and Ca and Fe in seeds have been reported bined drought and heat stress conditions in a greenhouse in response to drought (Beebe et al., 2000). Smith et al. but also under natural field conditions to more precisely (2019) also found, by analysing a small number of 10 bred determine the effect of intense natural drought/heat con- lines developed by CIAT, that drought can decrease the ditions on minerals and antinutrients. amount of minerals in the common bean soluble leaf fraction, but not within the seeds. A reduction in the con- centration of Fe as well as phosphorus and Zn by 5– 20% 4.2 | Mineral uptake and bioavailability have been also reported for a still rather small number of bean lines/varieties under drought conditions (Hummel Fe accumulation is highest in leaves with increasing et al., 2018; Sehgal et al., 2018; Smith et al., 2019). A first ferritin synthesis during plant development (Zielińska- multi- year field trial at a climate analogue site experienc- Dawidziak, 2015). Ferritin functions as the main Fe- ing weather conditions, similar which has been predicted storing protein in the seeds of legumes, which has in year 2095 for Malawi, has also provided strong evidence traditionally been the source of plant- derived ferritin that the amount of Fe significantly declines in common (Marentes & Grusak, 1998). Relatively little is, however, beans under drought conditions (Hummel et al., 2018). In currently known about Fe uptake and regulation in leg- contrast, when 20 bean varieties were tested, a significant umes, in particular under drought/heat stress conditions. increase in Zn, due to drought stress, has been measured This is despite several articles having recently reviewed (Hummel et al., 2018). While changing climatic condi- Fe uptake and transportation in plants in general (Curie tions might, therefore, result in increased Zn- levels in fu- & Mari, 2017; Kobayashi & Nishizawa, 2012; Thomine & ture bean servings, these servings possibly have a lower Fe Vert, 2013). A large number of likely transport protein can- content and a higher amount of undesirable antinutrients, didates have been already identified in legumes as more such as PA (Hummel et al., 2018; Nelson et al., 2018). genome and transcriptome data of various legumes are PA is the most abundant phosphorylated derivative of becoming available. Members of the NRAMP, YSL, VIT myo- inositol and the main storage form of phosphorus and ZIP transport families have higher expression in leg- in the seed. PA also plays an important function in reg- ume root nodules. These members likely play a role in the ulating different cellular processes and also limits oxida- transport of Fe across symbiotic membranes (Brear et al., tive stress (Sparvoli & Cominelli, 2015). The amount of 2013). The application of fertilizers, either to the soil or as a PA, dependent on the phosphate concentration, mainly foliar spray, also significantly increases the accumulation 10 of 28 | LOSA et al. of nutrients in the seed, but transport is hampered by lim- Fe biofortification in common beans is, therefore, low ited mobility in the phloem sap (Bindraban et al., 2015). Fe absorption due to the presence of polyphenol(s) Nutrients can be further relatively immobile, not only (Ganesan & Xu, 2017). Different subclasses of such poly- in plant tissues, but also in the soil. This immobility af- phenols are present in common beans, mainly located fects their transport within the phloem. A greater rooting in the seed coat. Although some polyphenols, such depth is generally required for plants to access from the as kaempferol, kaempferol 3- glucoside, catechin and soil sufficient amounts of minerals (Maillard et al., 2015). 3,4- dihydroxybenzoic acid, are able to promote Fe up- Transporters, which are essential for the uptake of miner- take, at least in an in vitro system, others have a strong als from the rhizosphere, have been characterized in com- inhibitory effect. This outweighs the effect of those mon beans (Castro- Guerrero et al., 2016). Fe and ferritin compounds promoting an increase in Fe uptake (de further accumulate in separate cellular locations in bean Figueiredo et al., 2017; Hart et al., 2015). Unfortunately, seeds. Fe primarily accumulates in the cytoplasm of cells to our knowledge, a serious gap is still the lack of any surrounding the pro- vascular tissue, while ferritin, the bean breeding programme specifically targeting poly- major Fe- storing protein in legume seeds, accumulates in phenols for reduction of any negative effects these poly- the amyloplast, as found for peas (Cvitanich et al., 2010; phenols have particularly on Fe bioavailability and how Marentes & Grusak, 1998). In common bean seeds, only drought/heat stress can affect this process. 15% to 30% of total Fe is, however, ferritin bound. An ex- cess of Fe and osmotic stress increases ferritin expression in common beans (Hoppler et al., 2014), but ferritin does, 5 | BREEDING USING “OMICS” overall, not contribute much in the provision of Fe. TOOLS IRT- like transporters are further involved in the uptake of both minerals that are then mobilized to the shoots via Previous common bean research work, particularly on the xylem and then delivered to developing tissues, includ- drought/heat tolerance, focused mainly on investigating ing seeds, exclusively via the phloem (Hindt & Guerinot, and characterizing agro- morphological traits to identify 2012; Khan et al., 2014; Sinclair & Krämer, 2012). Fe up- bean lines with better plant growth under these stresses. take regulation is under the control of two transcriptional Several different traits, for example pod harvest index, networks, FIT (At2g28160) and PYE (At3g47640), while were thereby found to be associated with drought toler- Zn uptake requires bZIP transcription factors (Hindt & ance (Polania, Rao, et al., 2016). “Omics” tools (genom- Guerinot, 2012; Sinclair & Krämer, 2012). The common ics, transcriptomics and proteomics) have been, or are bean genome contains putative homologs for the com- currently, applied to identify and characterize genes and ponents of the networks (Phvul.005G130500/FIT1- like; genome sequences in common bean plants that are in- Phvul.002G099700/IRT1- like; Phvul.003G086500/OPT3- volved in drought/heat stress tolerance or mineral pro- like; Phvul.011G035700/bZIP23- like) (Castro- Guerrero duction. These activities are aimed to produce improved et al., 2016). Furthermore, an Arabidopsis protein local- common bean material for drought/stress tolerance and ized in the phloem, OPT3, is a component of the shoot-t o- higher mineral content. A recent review has highlighted root signalling network. This protein, not yet characterized the achievements in common beans by applying “omics” in more detail in common beans, passes on the Fe status in tools (Nadeem et al., 2021). leaves to roots and opt3 mutants accumulate more Fe and Most of the recent/current advances made by applying Zn in roots and leaves (Mendoza- Cózatl et al., 2014). “omics” tools were/are only achievable due to the publi- The presence of antinutritional compounds, such as cation of the common bean genome sequence (Schmutz PA and polyphenols, limits the bioavailability of min- et al., 2014; Vlasova et al., 2016). In contrast to the Andean erals (Glahn et al., 2017; Petry et al., 2010; Tako et al., common bean genome with an estimated size of 587 mega 2014). By adversely affecting the absorption of minerals, base pairs (Mbp) with ~27 thousand genes (91% clustered PA decreases the bioavailability of these minerals and, in synteny blocks with Glycine max), the Mesoamerican as a consequence, negatively impacts the nutritional genome is 549.6 mega base pairs in size with ~30 thousand value of seeds (Petry et al., 2015). The amount of PA genes and 94% of which has been functionally annotated has been further positively correlated with amounts of (Vlasova et al., 2016). The availability of the common bean non- ferritin bound Fe (DeLaat et al., 2014). Polyphenols sequence in 2014 has further offered the opportunity for are also highly interconnected with mineral amounts better understanding drought adaptation and tolerance in (e.g. Fe). They are further involved in resistance to dif- common beans. However, previous studies never focused ferent types of stresses, in part due to their antioxidant on a deeper level on any possible link between mineral properties (Herrera et al., 2019). A major obstacle to accumulation and availability and drought/heat stress. LOSA et al. | 11 of 28 5.1 | Quantitative trait loci (QTL) (Valdisser et al., 2020). Finally, a stable QTL related to identification yield (Yd4.1) has been recently identified in a common bean BAT881 × G21212 RIL population tested in field tri- 5.1.1 | QTLs for drought tolerance als across four different locations in Colombia. This QTL is not only associated with drought stress, but also to phos- Advances in genetic investigation using genomics paved phorus and Al stress. The molecular function of Yd4.1 is, in common beans the way not only to better understand however, still unknown (Diaz et al., 2018). genetic variation, for example within the European com- Further, SNPs determination in common beans al- mon bean germplasm and to trace its divergence from lowed to annotate a SNP to a gene related to drought tol- the American germplasm (Bellucci et al., 2021; Caproni erance. This SNP is related to biosynthesis of proline, a et al., 2020; Lioi & Piergiovanni, 2013) but also for the well- known osmotic protector (Villordo- Pineda et al., identification and characterization of quantitative trait 2015). A most recent SNP analysis under drought con- loci (QTL) related to agronomic and nutrient traits. QTL ditions also identified SNPs for processes responsive to analysis generally links phenotypic and genotypic data. In drought stress. These processes included stomatal reg- particular, numerous QTL studies in common beans have ulation, protein translocation across membranes, redox been carried out to identify specific traits linking abiotic mechanisms, hormone as well as osmotic stress signalling stresses— including drought— to agronomic traits of inter- (Leitão et al., 2021). A further more recent whole- genome est such as plant size, seed yield and flowering time. These resequencing- derived SNP dataset applied for a genome- approaches rely on the genetic analyses on crosses of sus- wide association analysis identified 12  loci. These loci ceptible x tolerant parental common bean genotypes, be- were significantly associated with survival after drought longing to either a single gene pool, or both the Andean stress at the seedling stage. They also confirmed the and Mesoamerican gene pools (Nadeem et al., 2021). The drought- related function of an aquaporin gene (PvXIP1;2) resulting population is then used to construct genetic link- located at Locus_10 (Wu et al., 2021). Finally, a good ex- age maps. The resolution of these maps has considerably ample of what can be achieved by applying the QTL tech- improved over the years. Based on these maps, an increas- nology in legumes has been recently shown for chickpea ing amount of genetic markers including microsatellites and cowpea. Genetic physical maps were developed and and single- nucleotide polymorphisms (SNPs), a variation QTLs including “QTL- hotspot” regions containing QTLs at a single position in a DNA sequence, have been recently for several drought tolerance traits were identified. This developed (Leitão et al., 2021; Sedlar, Kidrič, et al., 2020; analysis has already resulted in 29 new cowpea varieties Sedlar, Zupin, et al., 2020). Particularly, mining in com- developed and the production of 20,353 t of certified seeds mon beans QTLs affecting field performance and nutri- which have been planted on about 508,825 ha (Varshney ent value under drought will be still crucial in the future et al., 2019). design of molecular tools for marker- associated selection (MAS). Mining will also be crucial for the identification of possible molecular targets important for gene editing 5.1.2 | QTLs for mineral (Fe) content (GE) approaches, as recently described for wheat grown in dry and hot environments (Tura et al., 2020). QTLs re- Studies about the genetic basis of common bean seed lated to yield, flowering time as well as days to maturity, composition have so far mainly focused on minerals, such were specifically identified in common beans based on as phosphorus, Fe and Zn, due to their problems related the genetic analysis of a Mesoamerican x Mesoamerican to deficiency in human diets. Identification of QTLs was drought- tolerant x susceptible cross (Blair, Galeano, et al., thereby based on the application of both inter and intra- 2012). In addition, QTLs related to seed yield and flower- gene pool populations (Casañas et al., 2013). A recent ing time have been recently identified after crossing two genome-w ide association studies (GWAS) resulted in the Andean genotypes reacting differently to drought stress identification of quantitative trait nucleotides (QTNs) as- (Dramadri et al., 2019). Three loci related to seed yield sociated with seed content of nitrogen, phosphorus, Ca, per plant (Syp1.1, Syp1.2, Syp2.1) are of specific interest Mn and Zn, while no significant associations were found for yield- oriented MAS under drought stress with Syp1.1 for Fe content (Gunjača et al., 2021). In contrast, Blair, emerging as a master regulator of yield under drought Galeano, et al. (2012) found numerous QTLs, also related (Sedlar, Zupin, et al., 2020; Trapp et al., 2015). Moreover, to Fe, although usually found to be population or environ- a great number (189) of QTLs have been found related to ment specific. QTLs associated to seed phosphate content seed weight and 33 QTLs related to yield. Many of these have been identified in a RIL common bean population QTLs are within— or in proximity— to genes known (intragene pool Andean x Andean) on chromosomes Pv02, to be involved in primary or specialized metabolism Pv05, Pv06, Pv05 and Pv11, with additional PA-r elated 12 of 28 | LOSA et al. QTLs on Pv04 and Pv08 (Cichy et al., 2009). P- QTLs de- known, due to an available sequenced common bean ge- rived from the analysis of intergene pool populations nome with 94% of genes functionally annotated (Vlasova (Mesoamerican x Andean). Loci associated to seed phos- et al., 2016) allowing to identify target genes for any de- phate and total phytates were identified on Pv02, Pv03, sirable trait modification, efficient bean transformation Pv04, Pv06, Pv10 and Pv11 (Blair, Galeano, et al., 2012). An to obtain transformed modified plants has still technical intergene pool study based on a Mesoamerican × Andean limits. Common bean transformation is by far not a rou- cross further identified QTLs associated with both Fe and tine approach, as in other species (De Paolis et al., 2019). Zn content. QTLs were scattered along chromosomes However, first examples of possible successful genetic Pv03, Pv04, Pv06, Pv07, Pv08, Pv09, with a cluster of 5 on modification of common beans include overexpression Pv11 (Blair et al., 2010). Furthermore, overlapping Fe and of a methionine- rich storage albumin from Brazil nut Zn- QTLs were identified on a linkage group located on in transformed bean plants after particle bombardment Pv06, alongside QTLs located on Pv03, Pv04, Pv07, Pv08 of the apical meristematic region of embryos for gene and Pv11 (Blair et al., 2010). A recent meta- analysis, con- transfer (Aragão et al., 1999). Expression of the barley ducted on the cited literature, finally reduced the origi- (Hordeum vulgare) late embryogenesis abundant protein nal set of detected QTLs into a set of 12 QTLs, with two (HVA1) in transformed common beans is a further ex- QTLs specific for Fe and Zn, and 8 QTLs related to both ample where the method of particle bombardment of the (Izquierdo et al., 2018). shoot meristem for transformation was applied (Kwapata Interestingly, a recent study has presented the first et al., 2012). Produced transformed plants were more common bean MAGIC population of the Mesoamerican drought- tolerant due to longer roots. These examples gene pool (Diaz et al., 2020). The study allowed the iden- provide overall evidence that plant transformation is, in- tification of different genomic regions associated with deed, applicable for bean biofortification. yield, mineral accumulation, phenology and physiological traits under drought conditions. Moreover, major QTLs controlling more than one trait, even in different seasons, 5.2.1 | Genes and drought/heat and candidate genes for major QTLs were identified. This stress tolerance study now provides interesting data for the development of advanced breeding tools. In a further recent develop- Blair et al. (2011) already characterized 4219 uni- ment, optimal contributions selection was applied to de- genes from cDNA libraries prepared from contrasting sign common bean crossings within four market groups drought- treated common bean genotypes. By apply- with relevance for East Africa. Genomic estimated breed- ing suppression subtractive hybridization (SSH) and ing values were thereby predicted for grain yield, cooking a whole-g enome protein database for target hits, tran- time, Fe, and Zn in an African bean panel of 358 genotypes scription factors (NAC and AP2- EREBP family) and in a two- stage analysis. Such genomic selection using genes involved cell metabolic processes and present in optimal contributions selection will possibly accelerate photosynthesis were further identified to be involved breeding of high- yielding, biofortified, and rapid cooking in the drought response of common bean (Müller et al., African common bean cultivars (Saradadevi et al., 2021). 2014; Recchia et al., 2013; Wu et al., 2016). Table 2 shows a selection of genes which have been so far investigated regarding drought stress in common beans. When fur- 5.2 | Biotechnology ther drought responsive genes in leaf and root tissue of common bean were investigated by RNA- Seq, genes “Biotechnology” to improve common beans was already were predominantly involved in oxidative stress. This suggested in 2003 (Svetleva et al., 2003). Plant biotech- suggests a tolerance mechanism based on reduction nology generally allows precise genetic changes by in- of damage from reactive oxygen species (Pereira et al., tegrating, for example, an identified and characterized 2020). Orthologues of the soybean Hsp20 genes are fur- gene providing a beneficial trait into the plant genome ther up- regulated in response to drought and salinity or to change a gene inside a plant by genome editing (Du stress (Lopes- Caitar et al., 2013). López- Hernández and et al., 2016). The process to obtain either a transgenic Cortés (2019) recently identified in common beans by genetically modified plant (GMO) or gene- edited plants coupling genome–e nvironment associations with last- generally involves as tools application of plant trans- generation genome wide association study algorithms formation to insert a gene sequence, in vitro culture of candidate genes including HSP20, but also MED23, transformed plant tissues as well as whole plant regen- MED25, HSFB1 and HSP40 that are directly linked to eration. Although potential genes for transformation are heat- responsive pathways. Additional candidate genes LOSA et al. | 13 of 28 T A B L E 2 Stress responsive genes and their function in common beans Dry bean Homologue Study Function Description accession accession/ species Transcriptome analysis of differentially NAC transcription NAC domain protein, |75749297| |224088037| Populus expressed genes in roots of BAT 447 factor (TF) IPR003441 trichocarpa under drought stress during development (Recchia et al 2013) NAC4 protein |75748424| |62546189| Glycine max NAC domain protein |75749318| |224088037| P. trichocarpa NAC domain protein |75748418| |187940303| G. max DREB TF Fe- S cluster assembly protein |75749717| |292630743| G. max DRE2 homolog DREB |75748469| |32480821| G. max ERF TF Ethylene- responsive element |75749028| |190361165| G. max binding factor 4 Transcription factor EIL2 |75749407| |18643339| Vigna radiate bHLH TF Coiled- coil- helix- coiled- coil- |75749257| |66947630| Medicago helix domain containing truncatula protein bZIP TF Transcription factor bZIP70 |75749123| |145652341| G. max Leucine- rich repeat protein |75748580| |223452524| G. max TGA- type basic leucine |75748298| |15148922| Phaseolus zipper protein vulgaris F- box/LRR- repeat protein, |75748883| |255558466| Ricinus putative communis MYB MYB transcription factor |75748729| |110931684| G. max MYB185 GATA-f actors GATA transcription factor, |75748743| |255572876| R. putative communis WRKY family WRKY36 |75748775| |151934195| G. max Ubiquitous factors Transcription initiation |75748702| |255566898| R. TFIIA e Sp1 factor ia, putative communis IAA (auxin- Auxin- responsive protein |75748737| |255552973| R. responsive) IAA1, putative communis Auxin- responsive family |75748789| |15226425| Arabidopsis protein thaliana GRAS GRAS family transcription |75748648| |224106445| P. factor trichocarpa GRAS family transcription |75749650| |224106445| P. factor trichocarpa Heteromeric Transcription factor CCAAT |75748712| |193237557| Lotus factors japonicas eIF2—a lpha Translation initiation factor |75748325| |255544025| R. family EIF- 2b communis Eukaryotic translation |75748617| |20138704| Manihot initiation factor 5A esculenta Zinc finger C2- H2 zinc finger protein |75749674| |161087182| G. max ( Continues) 14 of 28 | LOSA et al. T A B L E 2 (Continued) Dry bean Homologue Study Function Description accession accession/ species Transcriptome analysis of differentially Uncharacterized protein |351721030| G. max expressed genes in BAT 447 under drought LOC100305788 stress during flowering (Müller et al. 2014) Oxygen- evolving enhancer |358344003| M. protein truncatula Chlorophyll a/b binding |16805332| G. max protein type II Hypersensitive induced |354683205| G. max reaction protein 1 Invertase/pectin |297310623| Arabidopsis methylesterase inhibitor lyrata family protein Auxin- repressed protein |357446689| M. truncatula Predicted: 40S ribosomal |356521554| G. max protein S17- 4 Transcriptome analysis of differentially Predicted: 40S ribosomal |356524632| G. max expressed genes in BAT 447 under protein S16- like drought stress during grain filling Leucine zipper protein |357491217| M. (Müller et al. 2014) truncatula Unknown |388517649| L. japonicus Predicted: cell wall/vacuolar |502150782|Cicer inhibitor of fructosidase arietinum 1- like NAD- dependent isocitrate |3790188| Nicotiana dehydrogenase tabacum Predicted: RING-H 2 finger |356539989| G. max protein ATL66- like Transcriptional analysis of drought induced Cellular Pyruvate decarboxylase, |255579310| R. genes in the roots of BAT 477 (Recchia metabolism putative communis et al. 2013) Malate dehydrogenase-l ike |83283965| Solanum protein tuberosum Glyceraldehyde-3 - phosphate |255638912| G. max dehydrogenase Glutaredoxin-1 , grx1, |255540625| R. putative communis Biological Spliceosomal complex |224094081| P. processes trichocarpa Methionine |75304713| Phaseolus adenosyltransferase lunatus S- adenosylmethionine |156181612| P. vulgaris decarboxylase Methionine |75304713| P. lunatus adenosyltransferase Abiotic stress Interferon- related |42571665| A. thaliana response developmental regulator family protein Light- inducible protein |192910730| Elaeis ATLS1, guineensis LOSA et al. | 15 of 28 T A B L E 2 (Continued) Dry bean Homologue Study Function Description accession accession/ species Group 3 late embryogenesis |75708857| P. vulgaris abundant protein Proline- rich protein |806310| G. max LEA5 |1732556| G. max LEA protein |1350522| Picea glauca LEA5 |1732556| G. max Biotic stress Isoflavone synthase 1 |184202203| Vigna response unguiculate Isoflavone synthase 1 |184202203| V. unguiculata PvPR2 |130835| P. vulgaris Transport Plastidic phosphate |61651606| translocator- like protein1 Mesembryanthemum crystallinum Cation:cation antiporter |255587991| R. communis ATP binding protein, |255552798| R. communis Calcium ion binding |255637247| G. max Transcriptional response to drought stress in Aquaporin NIP Phvul.006G171000 roots and leaves of drought- susceptible Peripheral- type Phvul.001G205900 and drought tolerant common bean benzodiazepine receptor genotypes (Pereira et al. 2020) and related proteins DNAj homolog subfamily c Phvul.006G060700 member Beta- fructofuranosidase Phvul.005G158500 Class IV chitinase, Phvul.005G155800 insoluble isoenzyme WINV1- related Protein phosphatase 2C Phvul.001G075400 Glutathione S- transferase Phvul.008G113700 Heat shock transcription Phvul.007G061800 factor Late embryogenesis Phvul.007G259400 abundant (LEA) group 1 Linoleate 13S- lipoxygenase. Phvul.002G228700 MYB- like DNA- binding Phvul.002G184600 domain No apical meristem (NAM) Phvul.005G084500 protein NADH Phvul.003G131500 oxidoreductase- related Peroxidase Phvul.009G140700 Glycosyl hydrolase family 10 Phvul.009G120500 involved in the response of common bean to water defi- 5.2.2 | Genes and mineral (Fe) content cit (drought) conditions were very recently identified from a collection of more than 150 Portuguese common “Omics” tools have also been applied in order to increase bean accessions (Leitão et al., 2021). the mineral content and bioavailability of common 16 of 28 | LOSA et al. beans. The first important step in lowering the pro- develop beans with increased mineral bioavailability duction of PA in common beans has been the isolation and mineral content as well as lower concentrations of and sequencing of genes involved in PA biosynthesis certain polyphenolic compounds (Hummel et al., 2020). and transport (Fileppi et al., 2010; Panzeri et al., 2011). Molecular markers for the lpa1 and also lpa12 bean mu- Recently, additional putative biosynthesis and transport tants have been already developed. Such markers can genes have been further identified (Cominelli et al., 2017; now be applied in marker-a ssisted selection of common Cominelli, Pilu, et al., 2020). The availability of this data bean breeding lines as well as the evaluation of the per- will now allow new cutting-e dge innovative research, formance of such lines with either individual or com- including epi- genomics and translatome analysis. Two bined traits (Cominelli et al., 2018; Panzeri et al., 2011). identified allelic common bean mutants, affecting the However, some concern with the use of lpa beans still PvMRP1 PA transporter, caused a 75– 90% reduction in exists. PA, as a broad- spectrum antineoplastic agent, can the PA content (Campion et al., 2009; Cominelli et al., act in cancer development and progression (Vucenik, 2018; Panzeri et al., 2011). Particularly, the mutant bean 2019), despite the fact that no phytate has been detected line, lpa1, has a 25% reduction in raffinosaccharides, the in human biofluids (Wilson et al., 2015). Consequently, sugars causing flatulence. The biosynthesis of these sug- lpa beans may be particularly useful in areas where mi- ars is strictly linked to the biosynthesis of PA. A study cronutrient deficiencies are prevalent. In contrast, crops with human volunteers further found that seeds from with high amounts of phytates can also be beneficial for the lpa1 mutant line provides better Fe absorption, com- health in societies that have in their diet sufficient Fe pared to a non- mutant line (Petry et al., 2014). When ap- available, but where both obesity and cancer are on the plied in common household recipes, lpa1 mutant seeds rise (Blair, 2013). had, however, a lower retention of Zn. Due to a hard- The exact role and function of PA in drought/heat to- cook phenotype, associated with the increased ther- tolerance is, however, still unclear. So far only known mal stability of lectins in the lpa1 mutant lines, adverse is that some low phytic acid (lpa) mutants are more gastrointestinal symptoms occurred (Petry et al., 2016). drought sensitive (Cerino Badone et al., 2012). An The effect of the lpa1 mutation on thermal stability of Arabidopsis thaliana mrp5 mutant (an lpa mutant; Nagy seed lectins is, however, only problematic in a genetic et al., 2009) and common bean lpa1 mutants, affected in background which contains phyto- hemagglutinin L. In the AtMRP5 and PvMRP1 orthologous genes, have so far contrast, no significant effect on thermal stability has found to have some better drought tolerance (Chiozzotto been found when the genetic background contains both et al., 2018; Colombo et al., 2020; Klein et al., 2003). phyto-h emagglutinin- L and phyto- hemagglutinin E, Arabidopsis mrp5- 1 mutant rosette leaves have, in this which most common bean genotypes have (Cominelli, regard, closer stomata to prevent water loss, and have Galimberti, et al., 2020; Cominelli, Pilu, et al., 2020). a reduced transpiration rate and improved water use When developing lpa mutants, the essential role of efficiency (Klein et al., 2003).. More drought tolerance PA as regulator of cellular processes in plant vegetative of the common bean lpa1 mutant is also evident under tissues has to be considered in order to avoid important symbiosis. Transcriptional data provide evidence of undesirable pleiotropic effects (Sparvoli & Cominelli, higher expression of stress- related genes in the nodules 2015). Importantly, the common bean lpa1 mutant has and bacteroids of lpa1 mutants when compared to nod- no reduced germination or any reduced plant growth ules from non-m utant plants (Chiozzotto et al., 2018). and fertility. Still lacking is, however, a much more de- Finally, results with the lpa1 mutant plants now open tailed morphological/physiological evaluation of such a new perspective in obtaining mineral improved com- common bean lpa1 mutants. Cereal lpa mutants, the mon bean varieties. These varieties should not only bet- first lpa mutants isolated, have received so far very little ter cope with drought/heat stress but also provide beans interest. They are affected in the transporter orthologues with a low PA content (Raboy, 2020). Introgression of of PvMRP1 (Colombo et al., 2020; Sparvoli & Cominelli, these mutations into cultivated bean varieties is, conse- 2015). These cereal mutants have further a reduced yield quently, a current major research task (Campion et al., (5– 10% decrease) and non- optimal field performance 2009; Cominelli et al., 2018; Mulambu et al., 2017). This (Raboy, 2020). In contrast, the lpa1 common bean mu- task also includes the evaluation of the performance of tant has no such negative agronomic effects under field such lines, with either individual or combined traits, conditions (Campion et al., 2009; Chiozzotto et al., under environmental stress conditions. Common beans 2018). However, field studies are urgently required to cooking and nutritional properties will also be evalu- assess the potential of this mutant particularly under ated in more depth in a quest to develop bio- fortified field conditions in much more depth. They would be common bean lines devoid of negative traits (Cominelli, also interesting for breeding programmes aimed to Galimberti, et al., 2020). LOSA et al. | 17 of 28 5.2.3 | Gene editing protein than modern varieties (Celmeli et al., 2018) and how to produce more efficiently GMOs should also be part Genome editing (GE) applying the clustered regula- of the research activities. In addition, production of more tory interspaced short palindromic repeats editing annotated genomes will be very helpful to support any (CRISPR)/Cas system have already been applied to edit future transcriptomic, proteomic as well as epi-g enomic certain target genes in legumes (Bhowmik et al., 2021; data- mining efforts (Li et al., 2017). Finally, exploring the Ji et al., 2019; Liu et al., 2019). GE is currently an ef- interesting idea of common bean rewilding, which is the fective “omics”- based tool in the manipulation of traits reintroduction of specific traits from wild lines into the in crops (Du et al., 2016; Tiwari et al., 2020). While genetic background of commercial cultivars, should be CRISPR is usually considered as a tool to generate dou- part of the activities. Although whole- genome sequence ble strand breaks, and consequently generate knock- out data exist for numerous legume species, including com- mutations, the modular nature of the CRISPR technol- mon bean, next-g eneration sequencing (NGS)- driven im- ogy allows alteration of transcriptional activity, or epi- provements have not kept pace with that of cereal crops genetic status, at a chosen target site (Lee et al., 2019). (Rehman et al., 2019). NGS would, for example, support This can be achieved with a nuclease- deficient version the rewilding idea. Rewilding will specifically address the system (dCas9), which can be tied to a diverse array of loss of diversity during the bean's domestication process epigenetic effector domains for site- specific epigenetic and will possibly allow improving the bean's nutritional modifications (Pulecio et al., 2017). The current ad- value and tolerance to stresses (Cowling et al., 2015). vancements and limitations of GE, particularly in or- phan crops, have been recently discussed by Venezia and Creasey Krainer (2021). Innovative techniques, 6.1 | Exploring drought/heat such as GE and speed breeding, might effectively also stress tolerance shorten the time to develop drought- resilient common beans and consequently limit any risk of global food in- For most grain legumes, breeders mainly investigated in security (Bhowmik et al., 2021). In particular, the de- the past consequences of drought/heat stress on above- velopment of alternative lpa common bean mutant lines ground traits. However, investigating the relationship be- by applying GE could prove valuable in the pursuit of tween below and above- ground traits by studying in the improving specifically the nutritional value of common future in more depth will be an important aspect (Sofi beans. Mutations in the rice OsSULTR3;3 gene, encod- et al., 2021). The application, specifically of proteomics as ing type-3 sulphate transporters, have already resulted an “omics tool”, will particularly allow to explore proteins in rice lpa mutants that, in addition to reduced levels involved in drought/heat tolerance and mineral produc- of PA, had changes in the amount of a broad spectrum tion. Such proteomics studies will allow us to also investi- of compounds such as amino acids, organic acids (e.g. gate how these proteins are regulated (Zargar et al., 2017). citric acid) and other nutritionally relevant compounds Furthermore, specific target genes require more in depth including γ- aminobutyric acid (Zhou et al., 2018). investigation. Genes include the orthologous forms of the Arabidopsis thaliana and Vitis vinifera MYB60 genes. These genes, not well characterized in common beans, 6 | AREAS FOR FUTURE have been already extensively characterized for their EXPLORATION specific role in the modulation of stomatal movement (Cominelli et al., 2005; Galbiati et al., 2011). Other possi- To achieve the overall goal of higher common bean yield ble target genes to explore are regulatory genes controlling and dietary quality under changing climatic conditions the expression of DREB genes and that are activated by will certainly require the establishment and application of drought stress (Marcolino-G omes et al., 2014). an integrated research framework. This framework should consist of genomics, systems biology, physiology, as well as modelling and breeding (Palit et al., 2020). Recent ad- 6.2 | Improving mineral availability vances in sequencing and phenotyping methodologies, the rapidly emerging genetic and genomic resources as well as An important future research priority is increasing min- integrated crop modelling and predictions of climate im- eral (Fe)- bioavailability in common beans. Fe biofortifi- pacts, supports the establishment of a framework also for cation in common beans requires, however, adequate Fe common beans. Exploring in more depth how landraces partitioning between plant tissues. The Fe, and also Zn, cope with drought/heat stress and why they seemingly uptake mechanism as well as mobilization to allocate have a higher mineral content (especially Fe and Zn) and more Fe and Zn into bean seeds is, therefore, an area to 18 of 28 | LOSA et al. be explored in more depth, particularly under drought/ excellent approach to also capture the complexity of a diet heat stress conditions. Specifically, IRT- like transport- as a whole (Mertens et al., 2017). Another important com- ers involved in the mineral uptake can be thereby in- ponent is evaluating the effect of traditional cooking prac- vestigated. Since these transporters are also under the tices on the chemical- and nutritional composition of any control of two transcriptional networks, these networks selected bean lines. Further, evaluating how ingredients can be specifically characterized for how drought/heat of traditional recipes can contribute to the composition stress affects these networks. Furthermore, isolation and of a balanced and a high nutritional- quality dish with a characterization of the protein OPT3, a component of the particular emphasis on minerals would be interesting to shoot- to- root signalling network passing on the Fe status explore (Durazzo et al., 2019; López et al., 2013). in leaves to roots, is a worthwhile target for more in depth investigation. Different possible bio- fortification strategies to increase 6.3 | Controlling antinutrients amounts of minerals have been already reviewed by White and Broadley (2009). Fe biofortication might also include A future challenge is to explore how to obtain more Fe the future isolation of common bean genotypes low in without affecting the amount of antinutrients and of non- PA content. To our knowledge, no extensive variability essential toxic elements, e.g. cadmium and nickel. These for the PA trait, as found in mung beans (Dhole & Reddy, toxic elements, naturally present in trace amounts in the 2015), has been so far described for common beans. Only soil, enter the roots via the Fe- regulated transporter-1 me- two lpa mutants have been isolated and characterized in diated Fe/Zn uptake mechanism (Khan, Bouraine, et al., common beans (Campion et al., 2009; Chiozzotto et al., 2014). If any possible increases in the Fe content will also 2018; Cominelli et al., 2018; Panzeri et al., 2011). Selection affect the PA content, particularly under abiotic stress con- of more low PA bean mutant lines would, therefore, be ditions, has to be answered. Very few studies have so far a promising strategy to increase bioavailability of Fe, and investigated this aspect (Campos- Vega et al., 2010; Carbas also Zn (Petry et al., 2016; Raboy, 2020). et al., 2020). In addition, breeding material with specific Efficient Fe accumulation in a bioavailable form is an polyphenol and tannin profiles should be developed with interesting area to explore. Biofortification of edible plants the aim to reduce their negative effect on Fe bioavailabil- by overexpression of a native ferritin gene applying the ity and to more clearly define their function in Fe bioavail- GMO technology is an interesting strategy to increase the ability. Also explored should be if antinutritional proteins, Fe content in bean seeds. But, as shown in banana, a high such as protease inhibitors, which are expressed as a re- ferritin concentration has to be achieved sufficient for food sponse to environmental stress, will influence the Fe con- fortification (Yadav et al., 2017). In vacuoles, small Fe and tent of common bean seeds (Farooq et al., 2018). Giuberti Zn binding molecules, such as nicotianamine and organic et al. (2019) already found that absence of phaseolin, the acids (malate and citrate), have been further found as pos- main reserve globulin in seeds, with presence of the α- sible further targets for mineral biofortification (Hoppler amylase inhibitor is a potential determinant for raising et al., 2014). Mineral (Fe) bioavailability can, however, also Fe, and also Zn, concentrations in common bean seeds. be enhanced through improved processing procedures in- Introgression of the lpa mutation into the above genetic cluding soaking, thermal treatments, fermentation and/ background is thereby an interesting idea to even allow or germination. Combining popular traditions with inno- greater improvement of Fe availability. vative treatments, such as germination, is, therefore, an In summary, any mineral (Fe) optimized beans, which interesting alternative strategy to pursue. Germination are developed in future bio-f ortification programmes, and fermentation are thereby useful for increasing the ac- should ultimately also resilient to stresses associated with tivity of polyphenol- degrading enzymes and endogenous climatic changes currently threatening future common phytases, which limit the PA content (Carbonaro et al., bean production. Such newly developed common bean 2001). Heating promotes, for example, denaturation and varieties should ideally maintain high yields but also have hydrolysis of proteins, influencing chelating capacity and high amounts of minerals while having low amounts of significantly modifies the bio- accessibility of minerals (de antinutrients, such as PA, under drought/heat stress con- Oliveira et al., 2018). More research is, however, needed ditions. So far, the impact of drought/heat stress on com- to establish the effect of such processing procedures on mon bean yield in combination with the effect of stress mineral (Fe) bioavailability. also on the mineral content of beans has, unfortunately, Modification in protein solubility and digestibility is a not been extensively investigated, particularly not under further process which can be explored. Such modification any field conditions. Lack of such field investigations is will affect mineral bioavailability (Carbonaro et al., 2005; a major hurdle in the development of common bean va- Iddir et al., 2019). Diet modelling would, likewise, be an rieties improved in drought/heat stress tolerance as well LOSA et al. | 19 of 28 mineral content. Such field investigations are, therefore, HarvestPlus Working Paper. No. 11. International Food Policy urgently required. Research Institute (IFPRI). Assefa, T., Wu, J., Beebe, S. E., Rao, I. M., Marcomin, D., & Claude, ACKNOWLEDGEMENTS R. J. (2015). Improving adaptation to drought stress in small red common bean: Phenotypic differences and predicted ge- KK and JV were funded by NRF incentive funding. Partial notypic effects on grain yield, yield components and harvest funding was also provided to EC from the Knowledge index. Euphytica, 203, 477– 489. https://doi.org/10.1007/s1068 Hub on Nutrition and Food Security under ERA- NET 1- 014- 1242- x ERA- HDHL (No. 696295) for project “SYSTEMIC: An Avilés- Gaxiola, S., Chuck- Hernández, C., & Serna Saldívar, S. O. integrated approach to the challenge of sustainable food (2018). Inactivation methods of trypsin inhibitor in legumes: systems: adaptive and mitigatory strategies to address A review. Journal of Food Science, 83, 17– 29. https://doi. climate change and malnutrition” and by the European org/10.1111/1750- 3841.13985 Regional Development Fund to FS and EC for project Bailey, R. L., West, K. P. Jr, & Black, R. E. (2015). 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