Barley: a potential cereal for producing healthy and functional foods

La Geng, Mengdi Li, Guoping Zhang, Lingzhen Ye, Barley: a potential cereal for producing healthy and functional foods, Food Quality and Safety, Volume 6, 2022, fyac012, https://doi.org/10.1093/fqsafe/fyac012

Abstract

Barley is the fourth largest cereal crop in the world. It is mainly used for feeding, beer production and food. Barley is receiving more attention from both agricultural and food scientists because of its special chemical composition and health benefits. In comparison with other cereal crops, including wheat, rice and maize, barley grains are rich in dietary fiber (such as β-glucan) and tocols, which are beneficial to human health. It is well proved that diets rich in those chemicals can provide protection against hypertension, cardiovascular disease, and diabetes. Barley has been widely recognized to have great potential as a healthy or functional food. In this review, we present information about studies on the physical structure of the barley grain and the distribution of its main chemical components, nutrient and functional composition of barley grain and their health benefits, and the approaches of improving and utilizing the nutrient and functional chemicals in barley grain. With the development of processing technologies, functional components in barley grains, especially β-glucan, can be efficiently extracted and concentrated. Moreover, nutrient and functional components in barley grains can be efficiently improved by precise breeding and agronomic approaches. The review highlights the great potential of barley used as healthy and functional foods, and may be instructive for better utilization of barley in food processing.

Introduction

Barley is the fourth largest cereal crop in the world. Wild barley was collected and used by human ancestors as early as 10 000 years ago, and evolved into a cultivated crop around 7000 years ago ( Dai et al., 2012; Haas et al., 2019). In comparison with other cereal crops, such as wheat, rice, and maize, barley is characterized by higher barren, salt, and drought tolerance, allowing it to have wide environmental adaptability and distribution across the world. Barley is well known for its multiple uses, and at present is mainly used as feed and brewing material, although it is still a staple food for humans in some areas, including Tibet, China ( Sakellariou and Mylona, 2020). In the food industry, naked (hulless) barley is considered more valuable than hulled barley, as the absence of the hull increases the nutrient content (including starch, protein, and β-glucan) in barley grains ( Pejcz et al., 2017; Sterna et al., 2017). The highland barley planted on the Qinghai–Tibet Plateau, called ‘qingke’ locally, is unique in its growth habits and chemical components in grains, rich in nutrients such as bioactive carbohydrates, polyphenols, minerals, vitamins, phenols, flavonoids, and β-glucan ( Obadi et al., 2021). Therefore, the highland barley attracts great attention as a potential healthy food. Moreover, with better understanding of the chemical composition in barley grains and their functions in human health, the use of barley as a health food has been intensively addressed. In 2006, the U.S. Food and Drug Administration gave the final approval of a health claim for barley, based on research demonstrating that regular consumption of barley could prevent or control cardiovascular disease by lowering blood cholesterol ( FDA, 2006). The healthy functions of barley are mainly attributed to its higher contents of dietary fiber (such as β-glucan) and tocols. Barley is characterized by its high grain β-glucan content, almost 10-fold higher than wheat on average ( Geng et al., 2021). Indeed, it is well documented that diets rich in β-glucan can improve immunity of human bodies, providing protection against hypertension, stroke, cardiovascular disease, and type 2 diabetes ( Maheshwari et al., 2019; Tosh and Bordenave, 2020).

Currently, the challenges issued to barley and other cereal crop researchers are to develop varieties with high content of these healthy chemical components or produce crops suitable for utilization of healthy foods, and to food scientists to produce barley food with high nutrition which is commonly accepted in markets. The improvement of barley quality is helpful for producing better healthy food, while understanding of the chemical and functional components as well as their genetic regulation in barley grains and their health benefits is fundamental to improve relevant quality and meet the requirement by market. Therefore, in this paper we review the chemical components and healthy functions of barley grains, and some possible ways to improve the functional components, addressing the viewpoint that barley is a potentially ideal crop for producing healthy food.

Physical Structure of the Barley Grain

Generally, the barley grain (kernel) is spindle-shaped and 7–12 mm in length ( Jadhav et al., 1998). The mature barley kernel consists of hull, caryopsis, and rachilla, and its transverse section is shown in Figure 1.

The transversal section of mature barley grain. (A) Detailed description of the whole grain from outside to inner; (B) The structure of embryo and attached scutellum.

Hull

At a late stage of barley grain development, the lemma and palea develop into the hull, the outermost component of the mature grains, which mainly consists of cellulose, lignin, and silicon. The hulls are closely adhered to the caryopsis in hulled barley, whereas they are separated in naked barley.

A cementing layer is generated during the late grain milk stage, at 9–29 d after pollination (DAP), which adheres the hull to the caryopsis ( Brennan et al., 2017). There are abundant octadecanol, tritriacontane, campesterol, and beta-sitosterol in the cementing layer, and the composition and quantity of these chemicals are related to adhesive ability ( Brennan et al., 2017). Moreover, the adhesive ability is dependent on the environmental conditions during grain development due to their influence on the synthesis of these chemicals. Warm pre-anthesis and cool post-anthesis conditions cause the decrease of the adhesive ability ( Brennan et al., 2017).

Caryopsis

The caryopsis accounts for the major part of the whole mature cereal grain ( Evers et al., 1999). Barley caryopsis mainly comprises embryo and endosperm, which is in turn surrounded by the nucellar layer, testa (seed coat), and pericarp (fruit coat; Evers et al., 1999; Figure 1). The interval of the nucella layer and testa is the thinnest, while the interval between the testa and pericarp is the thickest ( Brennan et al., 2017).

Endosperm

Endosperm occupies most of grain composition, and consists of aleurone, sub-aleurone, and starchy endosperm ( Zheng and Wang, 2014). Barley aleurone comprises multilayered cells, generally three cell layers ( Bacic and Stone, 1981; Becraft and Yi, 2011). Aleurone is rich in nutrients such as lipids, proteins, minerals, B-type vitamins, such as niacin and folates, and some other micronutrients ( Brouns et al., 2012; Zheng and Wang, 2014; Li DQ et al., 2021). Storage protein is accumulated in the form of aleurone granules in aleurone cells ( Zheng and Wang, 2014). Starch granules are primarily accumulated in the inner starchy endosperm, while more proteins are accumulated in the intermediate sub-aleurone between the outer aleurone and the inner starchy endosperm ( Zheng and Wang, 2014).

Embryo

The embryo is the most important component of grains for filial generation ( Evers and Millar, 2002), which attaches to one side of the rachis and is located on the dorsal side of the caryopsis ( Figure 1B). The embryo mainly consists of embryonic axis, plumule, and radicle, supplying nutrients for the growth and development of plants ( Evers and Millar, 2002). The embryo is well-protected and surrounded by the coleoptile and coleorhiza. The scutellum is a flat-shaped and external recessed protective tissue, connecting with the embryonic axis and endosperm on both sides ( Evers and Millar, 2002).

Chemical Composition of Barley Grain

The chemical composition of barley grains is directly related to its end use. Barley with high protein content is suitably used for human food and animal feed, while low protein content is expected for barley used for malting or brewing. On the whole, the major constituents of barley grains are carbohydrates, proteins, lipid, and minerals, in addition to various secondary metabolites, such as vitamin and phenolic compounds ( Table 1).

Constituents of barley grains

Constituents of barley grains

Carbohydrates

Carbohydrates occupy the most composition in barley grains, generally about 78%–83% of total dry weight ( Henry, 1988). Barley carbohydrates are mainly categorized into low molecular weight carbohydrates, non-structural polysaccharides, and cell wall polysaccharides ( Henry, 1988). Low molecular weight carbohydrates include glucose, fructose, sucrose, maltose, and raffinose. Non-structural polysaccharides consist of fructans and starch, and cell wall polysaccharides are mainly cellulose, β-glucan, and arabinoxylans (AXs).

Low molecular weight carbohydrates

Monosaccharides, disaccharides, and oligosaccharides are known as the low molecular weight carbohydrates. Monosaccharides are the simplest carbohydrates, including glucose and fructose, and normally they represent 3%–8% of the total sugar content in barley mature grains ( Henry, 1988). Sucrose and maltose are the main representatives of disaccharides, consisting of two sugar molecules with glycosidic linkage ( Evers et al., 1999). Sucrose, as the most important disaccharide involved in photosynthesis, is converted into starch as a storage substance ( Evers et al., 1999). There is no maltose during starch synthesis; it is considered to be produced during germination of barley ( Henry, 1988). Oliogosaccharides may be defined as carbohydrates consisting of 2–10 monomeric residues linked by O-glycosidic bonds ( Henry, 1988). In barley mature grains, raffinose accounts for about 25% of the total sugar content, and it declines rapidly during germination ( Henry, 1988).

Non-structural polysaccharides

In barley grains, the non-structural polysaccharides mainly consist of fructans and starch. Starch, as a main source of energy, is synthesized in the endosperm, and functions for grain germination and plant growth ( Collins et al., 2021). Starch is the largest constituent in barley grains, and its content is largely controlled by genetic factors, although environmental conditions also have a dramatic impact on starch synthesis and accumulation ( Savin and Nicolas, 1996; Cuesta-Seijo et al., 2019). Asare et al. (2011) reported that starch content of 10 hulless barley genotypes varied from 58.1% to 72.2%. We measured 100 barley genotypes collected from different areas in the world, and found the total starch content ranged from 50.36% to 72.46% ( Li MD et al., 2021).

The starch in barley grains is mainly divided into amylose and amylopectin according to their structures. Amylose consists of 100–10 000 glucose residues linked by linear chains of α-(1–4) linkage ( Martin and Smith, 1995; Blennow et al., 2013) and accounts for 20%–30% of the total starch in the non-waxy grains ( Collins et al., 2021). Amylose is mainly synthesized by adenosine diphosphate (ADP)-glucose pyrophosphorylase (AGPase) and granule-bound starch synthase (GBSS; James et al., 2003; Crofts et al., 2017). Waxy gene encoding GBSS is responsible for amylose synthesis in barley and the mutated waxy gene affects amylose content and starch granules morphology ( Li et al., 2019). The high amylose mutant Glacier AC38 was first reported by Merritt (1967), and amo1 is responsible for the high amylose phenotype ( Schondelmaier et al., 1992). Barleys containing high amylose content are always characterized by shrunken kernels with much lower kernel weight ( Morell et al., 2003; Clarke et al., 2008).

Amylopectin is highly branched by 20 α-(1–4)-linked glucose residues and branched by α-(1–6) linkages ( Martin and Smith, 1995; Blennow et al., 2013). Amylopectin accounts for the majority of the total starch, usually 70%–80% ( Collins et al., 2021). Amylopectin biosynthesis requires the coordination of a series of enzymatic reactions involving AGPase, soluble starch synthases (SS), starch branching enzymes (SBE), and starch de-branching enzymes (DBE; James et al., 2003; Crofts et al., 2017). The loss of SSIIa enzyme activity (referred to sex6 mutants) leads to a decrease in amylopectin synthesis and shortened chain length distribution ( Morell et al., 2003). RNA interference method was used to silence SBE genes, resulting in a novel amylose-only starch ( Carciofi et al., 2012).

The quantity and proportion of amylose and amylopectin can be changed through genetic manipulation according to the requirement of the end use for barley ( Sarka and Dvoracek, 2017). In wheat, bread made of high-amylose wheat flour showed greater hardness and springiness, and brighter appearance ( Li JY et al., 2021). Waxy rice, also called glutinous rice, is more suitable for thickening soups, sauces, gravies, baby foods, and puddings because of its stickiness ( Sarka and Dvoracek, 2017). Waxy barley is favorable for processing food as its flour has freeze–thaw and anti-staling properties ( Sarka and Dvoracek, 2017).

In terms of size of starch granules, there are the large A-type and small B-type granules in barley grains, with diameters of 10–25 μm and less than 6 μm, respectively ( Morrison et al., 1986; Andersson et al., 1999). Small granules are much more abundant, accounting for 97% of the total granules ( De Schepper et al., 2020). The mutation of the Waxy gene can change the shape of starch granules, leading to shrunken and irregular B-type starch granules ( Li et al., 2019). The size distribution of starch granules greatly affects the end use of barley ( Sarka and Dvoracek, 2017; Jaiswal et al., 2020). During malting, the hydrolysis rate of small starch granules is faster than in the large starch granules ( De Schepper et al., 2020). Barley with more small starch granules in the endosperm is suitable for making paper and cosmetics, while barley with more large starch granules is favorable for malting and brewing ( Wei et al., 2008). In food use, small starch granules can produce a creamy and smooth texture for making low-fat and fat-free frozen desserts, cookies, and cheesecakes ( Lindeboom et al., 2004).

Fructan is one of the main storage carbohydrates in cereal grains ( Lim et al., 2020). In comparison with starch, fructan content in barley grains is quite small, only 0.9%–4.2% of the total dry weight ( Burton and Fincher, 2012; Nemeth et al., 2014). Fructans typically consist of 10 fructose residues in barley. Fructans are synthesized based on sucrose as a substrate ( Krahl et al., 2009) and it has been intensively highlighted in health food production ( Vijn and Smeekens, 1999) because it is recognized as dietary fiber and prebiotics ( Verspreet et al., 2015). In barley, fructans are widely associated with malting and brewing quality. Cozzolino et al. (2016) found the fructan content in malts is higher than that in raw grains, and the fructan content in malt was positively correlated with hot water extract rate (HWE) and negatively correlated with viscosity. However, different results were reported that fructans content had little change during malting and brewing ( Krahl et al., 2009).

Non-starch polysaccharides (NSPs)

NSPs in barley grains belong to the structural compounds, distributed over the whole caryopsis, aleurone layer, and endosperm cell wall. AXs and mixed linkage (1,3;1,4)-β-glucan (MLG) are the major components of the NSPs in barley grains ( Singh et al., 2017). AX content in barley grains ranges from 4.30% to 9.75% ( Messia et al., 2017). AXs consist of a linear β-(1→4)-linked xylan backbone, which is linked with α-l-arabinofuranose units at the position of O-2 and/or O-3 linkages as side residues ( Izydorczyk and Biliaderis, 1995; Messia et al., 2017). Much research has been done on isolation and evaluation of AXs ( Yadav and Hicks, 2015; Acar et al., 2020), but still little is known about its genetic regulation and the relevant genes encoding the enzymes of AX synthesis. β-(1,4)-Xylosyltransferase (XylTase) is reported to be involved in AX synthesis in barley endosperms ( Urahara et al., 2004).

MLGs are linear polymers of high molecular weight consisting of d-glucose molecules linked by β-(1–4) and β-(1–3) linkages ( Messia et al., 2017). MLG content differs greatly among barley genotypes and analysis methodology, ranging from less than 2.0% to over 10% ( Zhang et al., 2002; Geng et al., 2021). On the whole, the waxy varieties, with a low amylose content, contain higher MLG content ( Messia et al., 2017; Fastnaught et al., 1996; Li et al., 2019). The key enzyme involved in MLGs synthesis is generally considered to be cellulose synthase-like (CSL) enzyme ( Houston et al., 2014). In addition, environmental conditions also have a great impact on MLG content ( Stuart et al., 1988; Narasimhalu et al., 1995; Zhang et al., 2002). Higher temperature and less rainfall during the grain filling stage, and water stress post-anthesis could result in increased MLG ( Fastnaught et al., 1996; Zhang et al., 2001).

Protein and lysine

In barley grains, proteins are responsible for many functions, such as structural functions, metabolic activity, and providing nitrogen for the developing embryo. A survey of more than 1000 barley genotypes showed that the total protein content in barley grains ranged from 7% to 25% ( Lorz, 2003). The barley protein content is highly affected by both genotype and environment ( Zale et al., 2000; Lorz, 2003; Qi et al., 2006).

According to the biological functions of proteins, the barley grain proteins are mainly divided into seed storage proteins and structural proteins. Non-storage proteins are found primarily in aleurone and embryo, while storage proteins are mainly located in endosperm. The major storage protein in barley grains is hordein, which accounts for 35%–50% of the total protein ( Tanner et al., 2019). Hordein can be divided into A, B, C, and D groups on the basis of molecular mass and amino acid composition ( Shewry et al., 1984; Pan et al., 2007).

Like other cereals, lysine is the most limited amino acid in barley. Thus, increasing lysine content has been an important objective in the breeding of food barley. High-lysine cultivars of different cereals have been developed. In contrast with the normal maize and sorghum of 2% lysine content, high lysine maize reached 3.4% and high lysine sorghum contains 3.33% lysine content ( Mertz et al., 1964; Singh and Axtell, 1973). In barley, the high lysine cultivars, Hiproly and Risø Mutant 1508, contain 4.1% and 5% lysine content, respectively, while the normal barleys were 3.5% ( Munck et al., 1970; Newman et al., 1990).

Lipids

Lipids are a group of biomolecules distributed throughout all plant tissues. They play different roles in the composition of the cell membrane, storing molecules of metabolic energy, and responding to stresses ( Kuczynska et al., 2019). In plants, lipids usually exert functions as triacylglycerol (TAG) droplets for offering dietary phytochemicals ( Kuczynska et al., 2019). The lipids concentration in barley grains is around 3.0%–3.5% ( Price and Parsons, 1974), although some mutants had much higher lipid content. For example, the lipid content of the high-lysine mutant Risø 1508 is 4.1% ( Tallberg, 1977). In barley, the lipid distribution in embryo, endosperm, and hull fractions account for 17.9%, 77.1%, and 5% of total lipid content, respectively ( Price and Parsons, 1979). Lipids can be divided into neutral lipid, glycolipid, and phospholipid, and their distributions vary greatly in the grain tissues, with neutral lipids being predominant in all fractions, and glycolipids rich in hull and phospholipids rich in endosperm ( Price and Parsons, 1979).

Plant lipid transfer proteins (LTPs) have the function of delivering lipids intercellularly and intracellularly, and maintaining the lipid composition of organelles and membrane ( Vignols et al., 1997). For instance, LTP2 protein, belonging to the pathogenesis-related (PR) protein family, have the ability to bind to linear lipid molecules and sterols.

Vitamins

Generally, vitamins are classified into two groups, i.e. fat-soluble and water-soluble vitamins. Fat-soluble vitamins are vitamins A, D, E, and K, and water-soluble vitamins include inositol, and vitamins C and B. In general, vitamin B is abundant in cereals. Vitamin E (also called tocols), one of the antioxidants, is considered to be beneficial to human health in lowering the risk of diseases ( Do et al., 2015; Idehen et al., 2017). Vitamin E is a collection of eight isomers, including four tocopherols and four tocotrienols ( Pryma et al., 2007). Barley is rich in vitamin E compared to other cereals ( Moreau et al., 2007; Temelli et al., 2013). Moreover, the content varies greatly with genotypes, ranging from 8.5 to 68.8 μg/g dry weight ( Andersson et al., 2008; Do et al., 2015). Compared with hulless barley, hulled barley contains higher tocols content ( Cavallero et al., 2004). However, a hulless waxy variety, Washonubet, has high tocols content, even higher than hulled barley varieties ( Ehrenbergerova et al., 2006). In general, tocotrienol and tocopherol occupy 76.8% and 23.2% of total tocols, respectively ( Andersson et al., 2008). In barley grains, the majority of tocopherols is located in embryo, whereas tocotrienols are mostly present in endosperm and pericarp ( Sen et al., 2006; Idehen et al., 2017).

Minerals

In general, ash content of barley ranges from 2.5% to 3.1% ( Cieslik et al., 2017). Mineral elements are distributed over the whole grain, but are mainly concentrated in the outer layers of grains ( Liu et al., 1974; Weaver et al., 1981; Marconi et al., 2000). Therefore, the mineral content is much higher in hulled barley than the hulless type. On the basis of concentration in plant tissues, minerals are divided into two groups, i.e. macro- and micro-elements. The macro-elements are Ca, P, K, Mg, Na, Cl, and S, and the micro-elements are Co, Cu, Fe, I, Mn, Se, and Zn.

K and P are the most abundant mineral elements in barley grains, accounting for 0.37%–0.50% and 0.33%–0.60% of dry matter, respectively ( Rasmusson et al., 1971; Cieslik et al., 2017). K is an essential macronutrient for maintaining electrical potential, hydrostatic pressure, and biochemical activity for many enzymes ( Britto and Kronzucker, 2008). P is another essential macronutrient and its scarcity can affect growth and development of plants. Phytic acid (PA) is the main storage form of phosphorus in barley and cereal grains, accounting for 65%–85% of the total phosphorus in seeds ( Raboy et al., 2001). PA is a nutrition-limiting factor of feed for animals, and moreover excrements with PA may cause contamination of water ( Erdman, 1981; Raboy, 2001). Thus, low grain PA content is expected for feed barley. Mutants with low phytic acid (lpa) have been isolated in barley ( Larson et al., 1998; Dorsch et al., 2003; Oliver et al., 2009).

Phenolic acids

Phenolic compounds, such as phenolic acid, flavonoid, and proanthocyanidins, are the major source of antioxidant compounds in whole grains ( Shao and Bao, 2015; Tohge et al., 2017). In barley grain, these compounds are mainly distributed in husks, pericarp, testa, and aleurone ( Nordkvist et al., 1984). The total phenolics content ranged from 130 to 481 mg gallic acid equivalents (GAE)/100 g dry weight ( Han et al., 2018; Shen et al., 2018). The total flavonoid and total proanthocyanidin content ranged from 50 to 150 mg rutin equivalents (RE)/100 g and 29–65.26 mg/100 g dry weight, respectively ( Nordkvist et al., 1984; Verardo et al., 2015; Han et al., 2018; Shen et al., 2018). Ferulic acid (FA) and p-coumaric acid (p-CA) are the major phenolic acids in barley and account for 1.13–4.04 μg/g and 0.19–3.53 μg/g ( Cai et al., 2016), respectively. As important secondary metabolites in plants, phenolic compounds not only play an important role in plant growth and development and resistance to stress, but are also beneficial to human health due to their strong antioxidant effect ( Cheynier et al., 2013; Patel et al., 2017). In the brewing industry, phenolic compounds affect the quality of beer, such as taste, flavor, haze stability, and appearance ( Mikyska et al., 2002; Vanderhaegen et al., 2006).

Functional Compounds of Barley and Their Health Benefits

Barley grains are rich in a variety of health beneficial functional compounds, such as β-glucan, tocols, and resistant starch. Barley β-glucan can reduce serum cholesterol and blood glucose levels and improve intestinal function. Tocols have the effect of lowering serum cholesterol, and resistant starch can lower blood sugar and promote intestinal function. The schematic is shown in Figure 2. The detailed health beneficial functions and special chemicals of barley grains are listed in Table 2.

Health benefits of barley grain

LDL, low-density lipoprotein.

Health benefits of barley grain

LDL, low-density lipoprotein.

Health beneficial components and functions of barley grain.

Cholesterol-lowering effect

High blood cholesterol is a major risk factor for cardiovascular disease. It is well documented that soluble dietary fiber, especially β-glucan, is associated with the prevention of heart disease ( Maheshwari et al., 2019; Tosh and Bordenave, 2020). Barley and oats contain much higher β-glucan content than other cereals, such as rice, maize, and wheat. Many clinical trials showed that barley is the same as or even better than oats as a cholesterol-lowering food. Delaney et al. (2003) reported an increase in fecal neutral cholesterol and a decrease in aortic cholesterol levels in hamsters fed with 8 g/100 g β-glucan from barley or oats. A study on 44 high cholesterol men showed substituting barley meal (7 g β-glucan per day) for rice could reduce visceral organ fat as well as low-density lipoprotein (LDL) cholesterol and total cholesterol levels ( Shimizu et al., 2008). These studies suggest that barley foods have the same health benefits as oatmeal foods in reducing the risk of coronary heart disease. Foods made from suitable barley should contain 0.75g of β-glucan (soluble fiber) per serving. As mentioned above, β-glucan is thought to have cholesterol-lowering effects. It increases the viscosity in the small intestine, thus slowing the absorption of used oils. In addition, β-glucan can bind to bile acids and excrete them, eventually breaking down and replacing cholesterol in the body. Intake of pure β-glucan, extracted from oats or barley seeds, may lower blood cholesterol levels, particularly LDL levels ( Tosh and Bordenave, 2020).

The cholesterol-lowering effect of tocopherol and tocotrienol has been proven in chickens ( Qureshi et al., 1991a), pigs ( Qureshi et al., 1991a), and humans ( Chin et al., 2016). These compounds have been observed to significantly lower serum cholesterol levels. They also have the function in the prevention and treatment of cardiovascular diseases and cancer in the application of health food. Tocols content in barley and oats is much higher than that of other cereals, although there is a significant difference among barley varieties ( Suriano et al., 2020). Extract barley oil and brewery barley waste have higher tocols content than the whole grains, and are also recommended as sources of tocols for additive food use. In addition, rolling and grinding produce oil- and tocols-rich fragments, which are also potential sources of these compounds. Cholesterol content in the egg yolk of the chicken was reduced by feeding laying hens with barley oil ( Walde et al., 2014). Qureshi et al. (1991b) showed that people fed with 200 mg palm vitamin E showed obvious reduction of serum total cholesterol, LDL cholesterol, and glucose concentrations during a 4-week treatment period. Moreover, a separate hypocholesterolemia group fed with 200 mg γ-tocotrienol showed greater total cholesterol reduction. A study of 19 patients with type 2 diabetes and hyperlipidemia who were supplemented with tocotrienol-rich ingredients (3 mg/kg body weight) for 60 d showed that tocotrienol-rich ingredients can reduce total lipids, total cholesterol, and LDL cholesterol ( Baliarsingh et al., 2005). In short, tocols have a significant effect on lowering cholesterol content. Barley food with high tocols content has a great potential for preventing and controlling the related diseases.

Blood sugar-lowering effect

In recent years, many studies have shown that intake of barley foods has positive effects on glucose metabolism in humans ( Fuse et al., 2020). The glycemic index (GI) of barley (34–70) is generally lower than other cereals (55–85 for rice, 52–75 for wheat, and 46–80 for maize), although the GI value of food can be affected by processing or combining with other foods ( Lal et al., 2021). Research has shown that barley grains have a high potential to produce foods with very low GI, especially amylose-only barley grains containing a 99% amylose starch ( Sagnelli et al., 2018).The effect of barley foods in lowering blood sugar is attributed to both β-glucan and amylose/amylopectin ratio. In many cases, the glycemic response to barley foods is the result of a combination of these two factors. Ikegami et al. (1991) examined the glycemic response of normal and diabetic mice to barley feeding, and found all mice increased glycemic tolerance, and diabetic mice had normal fasting glucose levels after being fed the diet consisting of 70.83% barley. Narain et al. (1992) studied the response of healthy people to barley meals in India. The result showed that the increase in the area of the 3-h blood glucose curve declined from 107.9 to 91.5 mg/dL after 4 weeks of consuming 100 g whole barley flour. Minehira et al. (2001) investigated the mechanism of β-glucan in regulating prandium-glucose metabolism in healthy men. They suggested that the reduced glycemic response and increased intestinal viscosity finally caused delayed or decreased glucose absorption after eating a β-glucan diet ( Minehira et al., 2001). Foods containing β-glucan slow down carbohydrate absorption by affecting intestinal viscosity, so that the corresponding blood sugar peak is low and flat.

In addition, the amylose/amylopectin ratio can also significantly affect blood glucose levels, resulting in changes of insulin responses. Resistant starches are macromolecular polymer-like starch combinations that have antidigestive enzymes and remain intact in the large intestine of healthy humans ( Lockyer and Nugent, 2017). The resistant starch content of barley breads was consistent with a decrease in blood sugar content ( Lal et al., 2021). Obviously, the effect of barley foods in lowering blood sugar is attributed to the functions of β-glucan and resistant starch in slowing digestion and absorption.

Improving intestinal function

Amylose and amylopectin, the main types of starch, are organized into semicrystalline structures with amorphous and crystalline zone. The crystalline zone of starch particles is due to the linear portion of the amylopectin chain. The semicrystalline characteristic of starch granule is an important determinant of its digestibility ( Perla et al., 2017). Starch was classified into three types based on its digestion rate in the small intestine: rapidly digestible starch, slowly digestible starch, and resistant starch ( Englyst et al., 1992). Slowly digestible starch and resistant starch have been widely studied due to their beneficial health effects. The benefits of slowly digestible starch have been explained by its low GI, because slowly digestible starch is slowly digested throughout the small intestine, resulting in a slow and prolonged release of glucose into the blood ( Bello-Perez et al., 2020). Resistant starch resists digestion in small intestine; instead, it reaches the large intestine ( Perla et al., 2017). β-Glucan and resistant starch are fermented in the large intestine to produce short-chain fatty acids (SCFA), especially butyrate and propionate. The effect of these fatty acids on the intestine is to provide an energy source for epithelial cells that form a healthy colonic mucosa ( Demartino and Cockburn, 2020). A mouse feeding study showed that all mice fed with high-amylose barley and whole barley grains (containing 50 g/100 g barley extrudates) had better growth and intestinal quality than the control group fed with a commercial highly resistant corn starch ( Gerhard et al., 2002). Bird et al. (2008) found the indices of bowel health (stool weight, concentrations of butyric acid and fecal p-cresol, SCFA excretion) differed significantly between the two groups of participants feeding with barley and wheat, respectively, and the persons who ate barley food including 103 g of the test cereal showed improvement in gastrointestinal integrity ( Bird et al., 2008). These benefits are mainly attributed to the fermentation properties of resistant starch.

Heart disease, diabetes, metabolic syndrome, and cancer have become public health challenges. These diseases are not only occurring in the elderly, but are rising in the younger age group. Clinical trials demonstrated that lifestyle choices, including food choices, have a profound impact on the prevention or control of these diseases. A large body of evidence has shown that barley has a positive effect on blood cholesterol and blood sugar control as well as colon integrity ( Gustavo et al., 2019).

The Pathways for Improving Health Components in Barley Grains

Breeding approaches

Along with the deeper understanding of the mechanisms for genetic controlling of the health or nutrition components in barley grains, it has become possible for breeders to develop barley varieties with high nutrition or health qualities ( Loskutov and Khlestkina, 2021). Wild barley germplasm may contribute to improvement of nutritional qualities by crossbreeding, as it showed lower glycemic loads in the form of lower relative starch content with higher relative protein, fiber, and mineral contents compared with domesticated barley ( Hebelstrup, 2017). In recent years, molecular markers and genetic mapping have been widely used for improvement of barley grain nutritional qualities. Association mapping and favorable allele discovery of barley physicochemical properties including total phenolics, amylose content, and β-glucan content have provided the foundation for the improvement of barley breeding strategies using molecular markers ( Mohammadi et al., 2014). Mahalingam et al. (2020) conducted genome-wide association studies (GWAS) to identify marker-trait associations (MTAs) and key candidate genes involved in the biosynthesis of tocols. The related results provided a valuable resource for barley breeding programs targeting specific isoforms of grain tocols. GWAS have also been widely used to map loci and genetic regions responsible for total starch, amylose, amylopectin, and β-glucan content, which can highlight markers for breeding of barley varieties with suitable content of amylose and β-glucan ( Geng et al., 2021; Li MD et al., 2021). It was found that overexpression of the CslF6 gene in transgenic increased β-glucan content by at least 80% ( Burton et al., 2011). By silencing all the SBE genes, Carciofi et al. (2012) found that only amylose was produced in barley grain endosperm, and resistant starch content (90%) was dramatically increased. Moreover, the use of chemical mutagenesis can also improve the quality of barley varieties. For example, a naked barley variety with high resistant starch named Himalaya292 was developed by the use of chemical mutagenesis ( Bird et al., 2004). In addition, the genetic control of tocopherol synthesis in barley has also been intensively investigated. The gene encoding the geranylgeranyl transferase (HGGT) required for tocotrienol synthesis was isolated and cloned in barley ( Cahoon et al., 2003). Overexpression of barley HGGT gene in maize can result in a sixfold increase in tocotrienol content in seeds ( Cahoon et al., 2003). Recently, multiple quantitative trait loci (QTLs) associated with barley tocopherol have been identified through analysis of parental mapping populations and genome-wide association analysis ( Oliver et al., 2014; Mahalingam et al., 2020). With the completion of barley genome sequencing and rapid development of gene-editing technologies, the precise breeding of improving the specific nutrient and functional components will be efficiently performed to develop the barley varieties required by functional food production.

Cultivation approaches

In order to meet the market demand for barley, it is particularly important to use suitable cultivation practices to regulate barley quality. First of all, selection of a suitable variety is a prerequisite based on the end use of barley. For processing health foods, the varieties should be rich in functional nutrients, including protein, β-glucan, and tocols. As environmental conditions have a great impact on nutrition and health components, planting areas and soils should also be reasonably selected. Grains of barley growing at low soil water content and high air temperature, in particular during the filling stage, have high protein and β-glucan content ( Hong and Zhang, 2020; Ni et al., 2020). In general, the content of protein and β-glucan in barley grains increased with nitrogen fertilizer level ( Conry, 1994; Guler, 2003; Wroblewitz et al., 2013). In addition, potassium (K) fertilizer also has a great impact on protein and β-glucan content in barley grains. In general, a high K level tends to increase both protein and β-glucan content in barley grains. Protein content in barley grains is affected by sowing time, and late sowing may increase protein content in winter barley grains ( Yin et al., 2002; Xue et al., 2008).

Processing approaches

According to the location of various nutrients in barley grains, people can enrich and semi-separate these nutrients by conventional grain processing methods. As a food ingredient, hulled barley is usually required to remove the outermost fiber layer. A variety of nutrients in the products are enriched by skin grinding and fine grinding. For example, as phenolic compounds are rich in the outside of grains, high quantities can be found in the bran produced from barley flour and the fine grinding powder ( Andersson et al., 2003). Barley bran also contains high levels of other nutrients such as non-starch polysaccharides, starch, and protein ( Tufail et al., 2021). Air classification and screening are effective ways to produce nutrient (mainly protein and β-glucan) from coarse milling powder, a dry milling form used to produce whole grain flour and whole grain foods. As β-glucan is known for its functions in the control and prevention of cardiovascular disease in humans, many investigators have enriched β-glucan using conventional dry milling processes, such as air classification ( Messia et al., 2020). In the process of fine grinding and skin grinding, the outer seed coat and endosperm are separated, and the products are enriched in these two parts of the grain, which can be further air-classified and screened. Air classification separates coarse ground powder into powders with large, medium and small particle sizes, and each type of powder has different nutritional composition. By further air classification and screening of the three powders, the products rich in certain nutrients can be produced. Larger particles tend to contain more dietary fiber, while smaller particles often contain higher levels of starch and protein.

Many researchers have tried to extract, separate, and purify the health components (mainly β-glucan and tocols) from barley grains. At present, four methods are commonly used to isolate β-glucan from barley grains: HWE, alkaline extraction, acid extraction, and enzyme extraction ( Maheshwari et al., 2017). Among these methods, the order of barley β-glucan extraction rate is hot water>enzyme>acid>alkaline ( Maheshwari et al., 2017). High purity of β-glucan can be extracted by the hot water method. The temperature of extraction is generally higher than 90 °C, which makes the starch polymer to be extracted along with it. Thus, a heat-resistant α-amylase is added to remove starch during HWE ( Papageorgiou et al., 2005). The acid method can easily make cereal starch over hydrolysis, causing a large amount of glucose to be mixed into β-glucan products and increasing the difficulty of separation process ( Ahluwalia and Ellis, 1984). In the alkaline hydrolysis process, partial seed coat fibers will be decomposed, and more β-glucan combined with cellulose is dissociated into aqueous solution, increasing the yield of β-glucan. However, pectin may be easily formed in the extraction process, which affects the extraction rate and properties of β-glucan. β-Glucan can also be enzymatically extracted from barley grains, but many other enzymes should be simultaneously added during extraction to remove impurities such as starch and protein ( Ahmad et al., 2009). Furthermore, the molecular weight of β-glucan extracted by enzymatic methods is the highest ( Babu and Joy, 2016). In addition, ultrasound has also been used in the extraction of β-glucan. It was reported that the extraction rate of β-glucan could be improved by using ultrasonic-assisted extraction ( Liu et al., 2021). Although these methods have been commonly used in the laboratory to extract barley β-glucan, there are still many problems to be solved in order to realize the industrialization of barley β-glucan extraction and processing. The imperfect industrial extraction technology, low extraction rate, and high cost restrict production of barley β-glucan.

Compared with β-glucan in barley grains, tocols is less studied in its extraction and concentration in barley grains. Supercritical fluid extraction is a new extraction and separation technology developed in recent years. This technique has been widely used to extract tocopherol ( King et al., 1996; Ibanez et al., 2000). Tocols are lipid-soluble; therefore, they can be extracted together with lipids. Lipids mainly exist in the outer layers of barley kernel. Temelli et al. (2013) showed that tocols content in pearl flour was higher than that in whole grains ( Temelli et al., 2013). They also found that naked varieties contained higher levels of tocols in pearl flour than shelled varieties. Obviously, barley pearl powder is a suitable raw material for the recovery of tocopherol-rich oil.

Summary

Barley is a major cereal crop with multiple uses, and has been receiving more attention from both agricultural and food scientists because of its special chemical composition and health benefits. In particular, barley can serve as a food that meets the needs of a diet low in calories, high in fiber, and rich in probiotics, which has led to barley being listed as a desirable healthy food. The constituent characters, nutritional components and health beneficial components of barley grain have been well understood. Further effort should be concentrated on the better utilization of these traits in barley food processing, development of the new food products well accepted by markets and consumers, and improvement of barley quality more suitable for food processing. Important physical characters to be considered in the barley food processing include grain weight, size, hardness, etc. The important chemical components closely associated with functional food processing include starch, protein, minerals, β-glucan, tocols, etc. With the development of processing technologies, functional components in barley grains, such as β-glucan and tocols, can be efficiently extracted and concentrated, and with the development of barley genome sequencing and gene-editing technologies, the barley varieties rich in nutrient and functional components can be precisely obtained.

Author Contributions

La Geng, Mengdi Li, and Linzhen Ye conceived and designed the research. L. Geng, M.D. Li, L.Z. Ye, and G.P. Zhang wrote the article. In detail, M.D. Li wrote Sections 2 and 3, L. Geng wrote Sections 4 and 5. G.P. Zhang and L.Z. Ye directed and revised the review. All authors read and approved the final article.

Funding

This work was funded by the Science and Technology Program of Zhejiang Province of China (LGN20C130007, 2021C02064-3, 2020C02002), the National Natural Science Foundation of China (No.32171917), and the earmarked fund for China Agriculture Research System (CARS-05).

Conflict of Interest

The authors declare no conflict of interest.