Minor and Ancient Cereals: Exploitation of the Nutritional Potential Through the Use of Selected Starters and Sourdough Fermentation

C H A P T E R

35 Minor and Ancient Cereals: Exploitation of the Nutritional Potential Through the Use of Selected Starters and Sourdough Fermentation Erica Pontonio, and Carlo Giuseppe Rizzello Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Bari, Italy

O U T L I N E Introduction: Key Terms and Definitions

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Current Trends

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Nutritional Characteristics

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Cereal-Based Fermented Foods Wheat-Related Cereals

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Other Cereals Pseudocereals

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Conclusion

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References

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INTRODUCTION: KEY TERMS AND DEFINITIONS Despite much genetic and archeological data on the origins of agriculture, from gathering to cultivation to domestication to breeding, surprisingly there is no universal definition for modern or ancient grains. The classifications, as well as the definition assigned to each category, are research based and scientifically sound. Ancient grains are represented by populations of primitive grains, which were subjected to less intense breeding or selection processes compared, for example, to wheat, rice, and maize (the most cultivated cereals in the world). Since they are less important than these latter from the economic/industrial point of view, they are often designated as minor cereals. Many of these grains retained the character of their wild ancestors, such as large individual variability, ear height, brittle rachis, and low harvest index.1 Ancient and minor cereals might be classified into several categories, including1 species closely related to wheat, like spelt (Triticum aestivum subsp. spelta), emmer (Triticum turgidum ssp. dicoccum Schrank), and einkorn (Triticum monococcum L. ssp. monococcum)2; other cereals such as rye (Secale cereale L.), foxtail millet (Setaria italica L.), oats (Avena sativa L.), sorghum (Sorghum bicolor L.), barley (Hordeum vulgare L.), common millet (Panicum miliaceum L.), and teff (Eragrostis tef (Zucc.) Trotter)2; and, from a broad point of view,3 pseudocereals, which are crops evolutionarily distant from cereals, but producing grains with similar use in food production. Pseudocereals are dicot grains that diverge into several families, such as Polygonaceae, Amaranthaceae, and Lamiaceae. Amaranth (Amaranthus caudatus L., Amaranthus cruentus and Amaranthus hypochondriacus), quinoa (Chenopodium quinoa Willd.), and buckwheat (Fagopyrum esculentum Moench.) are the best-known pseudocereals,3 while chia (Salvia hispanica L.) has been gaining interest recently due to its technological and nutritional properties.

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CURRENT TRENDS Cereals are the most important plants; from the time of the earliest seed gatherers to the present, they have been a staple food. In most countries, diets have included a single cereal as the primary staple.4 As mentioned before, the most widely used are rice, wheat, and maize, which provide more than 90% of the total cereal calories of feed and food globally.4 These cereals constitute the main staples for Asia, Europe, and the United States, respectively. The contribution of wheat to human nutrition is considered of primary importance; indeed, due to its versatility, it allows for a wide array of products, such as baked goods and pasta, included in diets all over the world. The Food and Agriculture Organization (FAO) forecasts world cereal (and especially wheat) production in 2018 at 2610 and 754.1 million tons, respectively.5 The recent increase in wheat production mostly relates to Argentina, Canada, and the United States.5 Wheat is flanked by rice; indeed, FAO has raised its forecast of world paddy production in 2017 by 2.9 million tons. to 759.6 million tons.5 The cultivation of many ancient and minor cereals progressively decreased due to their low yield, and often to their low technological properties, so they were replaced by the high-yielding modern cultivars of rice, wheat, and maize, which contributed to a decrease in genetic diversity. Nowadays, the increasing demand for healthy and natural products and the need of crops with high adaptability are among the reasons for the renewed attention paid to minor and ancient cereals.6 Overall, minor and ancient cereals, the cultivation of which is less widespread and that have been little changed by selective breeding over recent millennia, played an important role in the history of human nutrition; nowadays, they are considered essential for the economy of many developing countries. Moreover, they are gaining interest in the market of Western countries since they are considered to be healthier than modern grains, especially regarding the amount of dietary fiber (DF), high-biological-value proteins, resistant starch (RS), minerals, vitamins, and phenols.7,8 The intake of baked goods made or fortified with ancient and minor cereals having a more balanced composition and moderate glycemic index (GI)—that is, larger particle size, high ratios of bran and germ to endosperm, presence of viscous soluble fibers, and high RS content—is in good agreement with currently suitable dietary trends.9,10 The use of ancient and minor cereal blends has been shown to be well suited to making highly nutritious, modern, and innovative baked goods meeting functional and sensory standards in terms of nutritional added value, palatability (high sensory scores), convenience (extended shelf life), and easy handling during processing.7 As a result, the development of new healthy foods based on nonwheat grain blends has occurred.11 Such an approach perfectly meets the consumers’ interest in natural, novel, and innovative foods with high nutritional value and functional properties.

NUTRITIONAL CHARACTERISTICS Among the minor species mentioned before, the pseudocereals buckwheat, quinoa, and amaranth are currently largely used as gluten-free ingredients, while the minor cereal species best correlated to wheat, like einkorn, emmer, spelt, and Kamut, are the most employed in gluten-containing counterparts. Hulled wheat-related species (einkorn, emmer, and spelt) are among the most ancient cereal crops of the Mediterranean region.12 These cereals were popular within the region for hundreds of years and remained a staple food for a long time. At a certain point in time, though, their use was abandoned, and only in the late 1990s did they become popular again due to their high commercial potential. Einkorn is a diploid hulled cereal and a close relative of durum (Triticum turgidum ssp. durum) and soft (Triticum aestivum ssp. aestivum) wheats. Today, traditional einkorn crops are found in mountain areas of the Mediterranean region (Turkey, Balkan countries, southern Italy, southern France, Spain, and Morocco), while its wild progenitor, T. monococcum ssp. boeoticum, still thrives in central and eastern parts of the Fertile Crescent region, including Israel, Lebanon, Jordan, Syria, northern Egypt, Turkey, Iran, and Iraq. Einkorn has been demonstrated to have higher content of protein and bioactive compounds (e.g., carotenoids) and lower α-amylase, β-amylase, and lipoxygenase activities. Moreover, einkorn expresses very few T-cell stimulatory gluten peptides13,14 and adapts well to low-input cultivation. The ancient tetraploid cereal emmer (also known as farro) was one of the first cereals to be domesticated in the Fertile Crescent, and it was the standard daily ration of the Roman legions. But over the centuries, emmer was gradually abandoned in favor of durum wheat, which is easier to hull. However, it has made a comeback in the last century. To date, its growing has been traditionally limited to the marginal hilly areas of Italy, Turkey, and the Balkan countries, where it is used for human nutrition and animal feed.15 Although most of its supposed nutritional properties have not yet been scientifically proven, emmer seems to be particularly appreciated for its content of DF, RS, and

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antioxidant compounds.16,17 In fact, it is considered a mild but effective regulator of intestinal functions, with a positive action compared to the allergenic effect of other cereals, such as wheat and barley.18 Many of these beneficial properties may be due to secondary components, such as structural polymers, gums and mucilage, and indigestible starch fractions. Spelt is another ancient wheat-related species that was widely cultivated until the spread of fertilizers and mechanical harvesting left it by the wayside in favor of wheat that was more compatible with industrialization. It is one of the husked hexaploid cereals, which possesses a genome similar to soft wheat (T. aestivum L.).19 Among cereals, the nutritive value of spelt is recognized to be relatively high,20 due to its protein content and composition, as well as its lipids, crude fiber,21 and vitamin and mineral content.22 A trademark for the ancient khorasan wheat variety, Kamut is used to market a grain with certain guaranteed attributes. The cereal is an ancient relative of modern durum wheat, two to three times the size of common wheat, and having higher content of protein, minerals, amino acid, lipids, and fatty acids than the varieties of modern wheat. The most striking superiority of Kamut brand wheat is found in its protein level. Because of its higher percentage of lipids, which produce more energy than carbohydrates, Kamut can be described as a “high-energy grain”.23 Even before wheat, barley was largely cultivated and used; indeed, Pliny reported it as the most ancient human food, and even today, it is believed to be the oldest of all cultivated plants. Although used as human food, it evolved primarily into a feed, malting, and brewing grain, due in part to the rise in prominence of wheat and rice. However, throughout its history, it has remained a major food source for a number of cultures, principally in Asia and northern Africa.24 It is the fourth widely grown cereal and among top ten crop plants in the world.25 The Fertile Crescent has been reported as an original area of cultivation and most likely the origin of barley.26 Barley was the principal source of bread flour until the 16th century and has remained a staple food in northern European countries through the 20th century.24 Although it has a high nutritive value, barley was relegated to the status of “poor man’s bread,” mainly due to its low gluten content.24 Ancient or ethnic grains are attracting the interest of both Western and African countries, as niche products having healthier and more natural features with respect to modern wheat, as well as to decrease the costs related to importing wheat flour.27 Among them, sorghum and millets have been important staples in the semiarid tropics of Asia and Africa for centuries. These crops are still the principal sources of energy, protein, vitamins, and minerals for millions of the poorest people in these regions. They include some of the first wild species to be domesticated by humans. Sorghum was grown in Egypt before 2200 BCE and has continued as an important crop there ever since.28 It is rich in minerals, but with bioavailability varying from less than 1% for some forms of iron, to greater than 90% for sodium and potassium. Sorghum protein is generally low in the essential amino acids (EAAs) such as lysine (c. 2/100 g protein)29 and threonine,30 and like legume and oil seed meals, has some limitations due to the presence of antinutritional factors (ANFs) such as trypsin and amylase inhibitors, phytic acid, and tannins.31 Millets are small-seeded cereals including species such as pearl millet (Pennisetum glaucum), finger millet (Eleusine coracana), kodo millet (Paspalum setaceum), proso millet (Penicum miliaceum), foxtail millet (Setaria italic), little millet (Panicum sumatrense), and barnyard millet (Echinochloa utilis). The world’s production of millet grains at last count was 762,712 tons, and the top producer was India, with an annual production of 334,500 tons (43.85% of the world total).32 In addition to their cultivating advantages, millets were found to have high nutritive value comparable to that of major cereals such as wheat and rice.33 It has also been reported that millets are good sources of phytochemicals and micronutrients such as EAAs, with the exception of lysine and threonine. However, they are relatively high in methionine.34 Finger millet also is known to have several potential health benefits, and some of these attributed to its polyphenol content.35 Moreover, it has carbohydrate and protein content comparable to other cereals and millets. However, its crude fiber and mineral contents are markedly higher than those of wheat and rice, its protein is relatively better balanced, and it contains more lysine, threonine, and valine than other millets.36,37 In the northern part of Ethiopia, the ancient tropical and nutritious cereal teff finds its origin and diversity. It is considered a superior grain due to its various nutritional characteristics.38 Teff is rich in carbohydrate and fiber38 and contains more iron, calcium, and zinc than other cereals, including wheat, barley, and sorghum.39,40 Hence, the nutritional profile of teff indicates that it could be used in producing healthy cereal products. Oats, like the other cereals, belong to the Poaceae family and are known as Jai or Javi on the Indian subcontinent. Avena sativa L. (common oats) is the most important of the cultivated oats. It contains high amounts of valuable nutrients such as soluble fibers, EAAs, unsaturated fatty acids, vitamins, minerals, and phytochemicals.41 The health effects of oats have been attributed mainly to the highly viscous β-glucan fraction, which has the ability to lower blood cholesterol and the intestinal absorption of glucose.42 Moreover, oats are also useful for the control of diabetes and lipid profile. Rye is one of the major bread grains in Europe. Whereas the world average annual consumption of rye as a food is low, it is highly produced and consumed in northern Europe, the major producers being Russia, Poland, Germany,

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Belarus, and Ukraine. In Finland and Denmark, where rye is consumed mainly as whole-grain rye bread, rye is an important source of DF.43 Hemicelluloses, mainly arabinoxylans and β-glucans, represent a major group of cell-wall polysaccharides in rye.44 Along with DF, rye is a good source of bioactive compounds such as phenolic acids, alkylresorcinols, and lignans, which are concentrated in the outer layers of the grain. Ferulic acid is the most abundant hydroxycinnamic acid in rye, followed by sinapic acid and para-coumaric acid. Several studies have shown that hydroxycinnamic acid derivatives have effective radical scavenging activity.43 Quinoa, amaranth, and buckwheat are widely suggested for incorporation into the gluten-free diet, adding variety and improving its nutritional quality.45 Quinoa is a native food plant of the Andean region, dating back to 5000 BC. The Incas appreciated its high nutritional value, and its ease of milling made its use as flour possible for rural populations. In many countries, the consumption of quinoa has been introduced to deal with serious nutritional problems, including low-protein diets due to the lack of animal protein; indeed, in many areas, quinoa is still the principal protein source.46 Quinoa is also a good source of carbohydrates, essential minerals, maltose, and D-xylose. In particular, quinoa has a protein content that is higher, and an amino acid composition that is better balanced, than the major cereals.47 The water and oil absorptions are good, which enhances its potential in human food and drink formulations. Hence, quinoa is recommended as a staple food.48 The term amaranth refers to a cosmopolitan genus of annual or short-lived perennial plants consisting of approximately 60 species, which can be divided into grain and vegetable amaranths for human consumption.49 Compared to other grains, amaranth has the highest amount of protein, twice the content of lysine, more DF, and 5–20 times the content of calcium and iron.50 Amaranth, which contains fiber, protein, tocols, squalene, and compounds possessing cholesterol-lowering functionality, is a particularly important crop for developing countries.51 Buckwheat is an annual plant52 mainly cultivated in China, the Russian Federation, Ukraine, and Kazakhstan.53,54 It contains numerous nutraceutical compounds53 and is rich in vitamins, especially those of the B group.55 The amino acid composition of buckwheat protein is well balanced and has a high biological value,56 although the protein digestibility is relatively low.57 Buckwheat grains are an important source of microelements such as zinc (Zn), copper (Cu), manganese (Mn), and selenium (Se), and macroelements such as potassium (K), sodium (Na), calcium (Ca), and magnesium (Mg).58

CEREAL-BASED FERMENTED FOODS Over the years, a large loss of biodiversity and a strong decrease in food diversity has occurred due to the extreme focus on only a few crop species and the disappearance of traditional dishes, recipes, and customs in food preparation.59 Nowadays, the attention toward ancient species of grains has been renewed by the rising demand for traditional products, the request for species suitable to be grown in marginal areas, and the need to preserve genetic diversity. The origin of fermented foods is lost in antiquity. It may have been a mere accident when people first experienced the taste of fermented food.60 Fermentation, especially that operated by lactic acid bacteria (LAB), became popular with the dawn of civilization because it allowed the preservation of foods and enhancement of their nutritional, functional, and organoleptic characteristics.60 Indeed, people have realized the nutritional and therapeutic value of fermented foods and drinks, making fermented foods even more popular.60 The wide range of cereal-based fermented foods and related processes is a testament to cultural diversity and to the ability of humans to find ways to produce foods in varying contexts.59 Cereal-based fermented foods are major contributors to energy intake in developing countries.59 One of the oldest biotechnological approaches to their production is represented by sourdough fermentation, based on the fermentation of dough by LAB and yeasts.61 It has been largely reported that sourdough fermentation, through LAB metabolism, can improve the technological and functional properties, nutritional value, and sensory profile of these flours, decreasing their ANF.9,62–64 One of the main sourdough effects, which has largely been studied due to the importance for human health, is its influence on the GI. Sourdough fermentation has great potential to modify the macromolecules in dough and promotes interactions between starch and gluten, hence reducing starch bioavailability.65,66 Organic acids also have been shown to play a role in the postprandial glycemic responses. Certain acids, such as acetic, propionic, and lactic acids, have the ability to lower the postprandial blood glucose and insulin responses when included in bread meal. The high nutritional value of ancient and minor cereal flours, combined with improvements related to the activity of LAB, may be used to improve the overall quality of wheat bread through its fortification.9 Along with the enhancements related to the traditional spontaneous sourdough (Type I), literature reports the efficacy of the use of proper selected LAB starters27,63 to improve the flavor and texture of ancient and minor cereal-based foods.9 Although the majority of the selected LAB studied have been isolated from wheat flours and sourdoughs, with the aim of optimizing

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their fermentative performances, the choice of starters should be made within the autochthonous microbiota of a certain matrix that ensures their best adaptation.9 The greater interest in ancient and minor cereals as quality improvers in food preparations and the well-known potential of LAB fermentation have led to an increase of scientific reports focusing on the optimization of biotechnological protocols for the production of sourdough and sourdough baked goods using these flours (Scopus, 2018).

Wheat-Related Cereals Due to their high nutritional value, the use of einkorn and spelt has been increasing after an almost complete abandonment,67 and these grains have been included in sourdough fermentation and bread preparation.68 Despite the longer time required for processing, the use of sourdough fermentation with selected starters (i.e., Lactobacillus plantarum 98a, Lactobacillus sanfranciscensis BB12, and Lactobacillus brevis 3BHI) have accomplished a number of things: (1) preserved carotenoids and enhanced their bioavailability; (2) improved phenolic acid composition of breads and (3) increased fiber solubilization, thus suggesting that einkorn is a good candidate to produce bakery products with enhanced nutritional properties.68 Einkorn is also used for the preparation of the Bulgarian version of a popular and traditional beverage of the Balkan region, called Boza, which has a number of beneficial effects on human health.69 Indeed, it helps to balance blood pressure, improves the colonic health, lowers plasma cholesterol, increases milk production in lactating women, facilitates digestion by enhancing the production of gastric juice, and by stimulating the secretion of pancreatic and hepatic cells. The beneficial effects of Boza on the human health are due to two main properties of this drink: the prebiotic features of its production cereal source, combined with direct consumption of probiotic lactic acid bacteria.69 Among the countries where spelt is largely cultivated,70 in Germany it is widely used in the production of traditional breads67; however, only a few studies67,71,72 have investigated the potential of sourdough biotechnology on such a matrix.67,71,72 In particular, Coda et al.67 investigated the autochthonous microbiota of spelt aiming at selecting suitable strains for selected sourdough fermentation.67 A large biodiversity was found during laboratory fermentation of spelt67,71 sourdoughs. L. brevis 20S, Weissella confusa 24S, and L. plantarum 6E were selected on the basis of their rapid growth and acidification and the capacity to release free amino acids67 and to be used as a mixed starter to ferment spelt flour. Peculiar metabolic traits of the selected LAB improved the concentration of total free amino acids and the bioavailability of Fe++, Zn++, Cu++, Mg++, and P++ (ca. 20%–60%). The dietary bioavailability of these minerals, however, is decreased by phytic acid, which when acting as an ANF makes a complex with cations.73 The highest phytase activity found in spelt and emmer sourdoughs may play a role in upgrading their nutritional quality.74 A similar approach was used for emmer flour, and comparable results were obtained after fermentation with the starters L. plantarum 6E, L. plantarum 10E, and W. confusa 12E. Spelt and emmer sourdoughs were also used to fortify wheat bread, which was clearly preferred globally for its taste compared to that of wheat bread. Sourdough biotechnology based on selected starters, therefore, was indispensable to completely exploit the potential of this ancient grain.67

Other Cereals Although barley sourdough is a promising ingredient to produce improved barley-based breads with enhanced nutritional value,75 it is not commonly used for baking because of its negative effects on bread dough rheology and loaf volume. Spontaneous barley sourdoughs prepared at laboratory and bakery levels were dominated by LAB belonging to the species of Lactobacillus fermentum, L. plantarum, and L. brevis, and Leuconostoc citreum, Leuconostoc mesenteroides, W. confusa, and Weissella cibaria, respectively. When barley flour was used to partly or fully replace wheat flour in sourdough bread-making, an increase of soluble fiber content was found. Indeed, the main advantage of using barley flour in food processing lies in its unique nutritional properties (in particular, the high content of β-glucans). Moreover, barley breads had overall acceptability scores comparable to the control. These findings encourage research toward the optimization of sourdough fermentation and bread-making with barley flour.75 Food fermentation also plays a major role in combating food spoilage and foodborne diseases in Africa. Moreover, lactic acid fermentation is probably the oldest and best accepted method among African peoples,76 and it is a home-based process largely used throughout the continent.77 Several millet- and sorghum-based foods, where the preparation greatly relies on the activity of LAB, are manufactured daily in Africa. Overall, fermentation has been reported as a good option for increasing the digestibility of sorghum proteins,78 changing the properties and microstructural organization of starch,79 reducing ANFs (e.g., tannins and phytic acid),80 improving amino acid balance, and increasing vitamin content.81 Sorghum has low nutritional value due to its low starch and protein digestibility

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and poor organoleptic profile.82 The effects of spontaneous fermentation on enzyme inhibitors, phytic acid, tannin content, and in vitro protein digestibility (IVPD) of sorghum were investigated.80 During a 24-h period, spontaneous fermentation of the local sorghum varieties resulted in a significant reduction in trypsin and amylase inhibitor activities, phytic acid, and tannin content. Fermentation was also found to significantly improve the IVPD. These results clearly indicate that fermentation may be useful for improving the nutritional quality of sorghum with respect to its protein and carbohydrate utilization as well as mineral bioavailability.80 Similarly, in Ben-saalga, a thin porridge prepared by cooking the fermented sediment of pearl millet (Pennisetum glaucum), Lactobacillus fermentum, L. plantarum, and Pediococcus pentosaceus, which typically dominate the spontaneous fermentation, are responsible for the enhancement of its nutritional properties.83 In particular, starch and phytate degradation improved its digestibility and facilitated the dietary uptake of proteins and minerals.83 These traditional cereal foods are produced by uncontrolled spontaneous fermentation, with occasional usage of consecutive refreshments (or re-buildings, replenishments, back-slopping) to initiate fermentation.84 The term refreshment deals with the technique by which a dough made of flour, water and possibly other ingredients ferments spontaneously for a certain time (possibly at a defined temperature) and it is subsequently added as an inoculum to start the fermentation of a new mixture of flour and water (and possibly other ingredients).61 However, controlled fermentation, with the use of the desired pure- or mixed-starter cultures with appropriate technology85 and being capable of driving fermentation rather than spontaneous fermentation, may have a promising potential84 for the production of foods with standardized enhanced nutritional and functional features. Within this framework, Pranoto et al.81 compared the spontaneous and controlled (using L. plantarum NBRC 15891) fermentations of sorghum flour, with the aim of highlighting the enhancement of its nutritional properties. Although both fermentations improved the IVPD, contrarily to what reported for wheat and several other cereals sourdoughs, the in vitro starch digestibility (IVSD) of sorghum flour increased as result of the fermentation. The increase of IVPD has been associated with the hydrolysis of protein and tannin in sorghum; indeed, L. plantarum has tannase activity81,86 that breaks the tannin complex with protein, making it accessible to pepsin digestion. The use of L. plantarum NBRC 15891 has been recommended in order to produce sorghum-based products with high nutritional value.81 Among the wide variety of fermented foods and beverages consumed in Ethiopia, Enjerra is made from a number of cereals, including sorghum, teff, corn, wheat, barley, or a combination. Enjerra from teff is the most popular with Ethiopians. Interest in teff has increased noticeably due to its very attractive nutritional profile and gluten-free nature, making it a suitable substitute for wheat and other cereals in their food applications, as well as for people with celiac disease. Because of its small size, teff is made into whole-grain flour (bran and germ included), resulting in very high fiber content and high nutrient content in general.87 In traditional approaches of teff fermentation where the advantages of the back-slopping is appreciated and generally practiced, strains of LAB belonging to the species Pediococcus cerevisieae, L. brevis, L. plantarum, and L. fermentum participated.87 Although the enhanced health properties of teff sourdough due to spontaneous LAB fermentation have been reported,87 the benefits of starter culture application as a means of improved functionality have not yet been evaluated. The most important effect of teff fermentation is the increase in the nutritional content because of the decreasing relationships of iron to phytates and iron to tannins.88 Phytates in Enjerra are considerably reduced to 35–76 mg/100 g (91%–93% destruction) due to fermentation and the acidity nature of Enjerra.89 A study of nutritional improvement during Enjerra-making showed that ANFs such as phytic acid, tannins, and trypsin inhibitors decreased by 72%, 55%, and 69%, respectively after teff fermentation.90 Moreover, fermentation increased the bioavailability of Fe, P, and Zn up to 24%, 60%, and 43%, respectively.88 Acha (Digitaria exiliis), also known as white fonio or hungry rice, and Iburu (Digitaria iburua), also known as black fonio or petit mil, are other ancient African cereals, and their mixture has been suggested for bread-making.27 P. pentosaceus F16A and Lactobacillus curvatus F18A and P. pentosaceus 16I and L. plantarum 13I, isolated and selected within the autochthonous microbiota of acha and iburu flours, respectively,67 were used as starters for sourdough fermentation.27 High levels of free amino acids and phytase activity were achieved with sourdough fermentation, as well as increased values of IVPD in breads fortified with acha and iburu sourdoughs.27 According to the new consumer demands for food products with improved nutritional quality and health benefits, oats represent an ideal raw material for the production of highly nutritious products.91 Usually whole-grain oat flour is used to fortify wheat bread, increasing the content of bioactive compounds. However, the addition of cereal bran causes severe problems in bread quality.65 One option to improve the quality of such high-fiber bread is the use of prefermented flour such as sourdough.65 Flander et al.92 optimized the baking process, both in terms of the bread quality and the physiological functionality of oat β-glucan in bread. Tasty bread with good volume, structure, and keeping qualities was attained by the use of sourdough fermentation and improving the possibilities to use oats as a health-promoting ingredient in bread.

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Rye is an important source of whole-grain foods in Eastern and Northern European diets, with traditional uses in various soft and crisp breads based on whole-grain flour.93 Most rye-bread bakers still prepare a rye sourdough daily. During the mixing of rye dough, no gluten network is built. Pentosans, which absorb water during the rye dough development, increase due to this acidification step. This water can then be released during the baking toward the starch, resulting in softer and moister bread. Moreover, sourdough in rye bread production is used to decrease the amylase activity of rye flour. By decreasing the pH of the dough by sourdough fermentation, amylases are inhibited and the crumbs are not completely hydrolyzed during baking. Further advantages, of course, include better flavor, improved microbial shelf-life, and crumb softness.94 In rye baking, the amounts of folates and phenolic compounds increase during the fermentation phase, with the starter type being an important factor affecting the process.95 The levels of phytate alkylresorcinols (ARs) and tocopherols are reduced, whereas the levels of lignans did not change greatly during sourdough baking.96 Sourdough fermentation seems to be an optimal procedure to allow the use of these flours in bread-making, especially in such amounts that could bring health benefits. Although the protocol may be optimized to improve technological and sensory quality, collateral nutritional improvements can be expected as well.

Pseudocereals In the past several decades, there has been a significant increase in interest in researching the development of glutenfree bakery products, involving various approaches. One of these includes the use of gluten-free flours such as buckwheat, amaranth, and quinoa. On the other hand, due to their high nutritional value, such flours have been proposed to fortify a staple food such as wheat bread. Buckwheat is a rich source of starch and contains many valuable compounds, such as proteins, antioxidant substances, trace elements, and DF. Similarly, the amaranth grain is characterized as having high-quality protein and lipids97 and high content of such minerals as Ca, K, and P, as well as DF.97 Although these grain have excellent nutritional value, gluten removal often results in major problems for bakers, so many studies have focused on the improvement of the baking characteristics and sensory properties of buckwheatbased bread.64 In order to improve the technological quality of these gluten-free flours, the use of the sourdough process has mainly been explored. Ecological studies on gluten-free sourdoughs indicate that gluten-free flours harbor novel and competitive LAB and yeast strains that are not commonly isolated in traditional sourdoughs and could serve as suitable candidates for starter dough development.98 Indeed, various positive effects on the volume, texture, and shelf life of baked goods due to the metabolic activity of LAB have been reported.99 However, very limited published data on the use of sourdough to improve the nutritional value and functional properties of gluten-free flours is available.10,62,100 Coda et al.62 reported that the use of buckwheat, along with amaranth, chickpea, and quinoa blends subjected to sourdough fermentation by the γ-aminobutyric (GABA)-producing strains L. plantarum C48, and Lactococcus lactis subsp. lactis PU1, allowed the manufacture of bread enriched in this compound. Recently, Lactobacillus delbrueckii subsp. lactis has been described to increase the total phenolic content and antioxidant capacity in buckwheat sourdough.100 Strains belonging to L. plantarum, Lactobacillus rossiae, and P. pentosaceus were isolated within autochthonous microbiota of quinoa spontaneous sourdough and selected according to the best acidification and growth capabilities and release of free amino acids.10 Fermentation of quinoa with autochthonous starters increased the nutritional value of quinoa flour. Indeed, soluble fiber increased, while insoluble fiber decreased. Compared to dough that was not fermented, fermentation with selected starters caused a marked increase of free amino acids (about fourfold), phytase activity (about threefold), and IVPD (by 25%), while condensed tannins significantly decreased. Five peptides released by the selected LAB strains during quinoa fermentation were considered responsible for the increase of the antioxidant activity. A quinoa-sourdough was obtained through the fermentation of quinoa flour by L. plantarum T6B10 and L. rossiae T0A16, which were previously isolated from and spontaneously fermented quinoa doughs, and the sourdough was used to fortify wheat bread (20%, w/w). Higher concentrations of proteins (20% increase), lipids, saturated fats, ash, and total DFs (50% increase) were found in bread compared to a conventional product. Bread made with quinoa-sourdough also had the highest concentration of soluble fibers and the lowest concentration of sugars. Moreover, the addition of quinoasourdough caused an increase in the concentration of almost all the individual free amino acids. IVPD markedly improved in quinoa-sourdough bread, and the rate of in vitro starch hydrolysis, which correlates with in vivo GI, showed the lower value when quinoa-sourdough was used, with a value of 70.7%.10

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CONCLUSION In the last decade, several grain crops, not subjected to extensive genetic improvements as wheat, maize, and rice, have been reintroduced. The increasing popularity of so-called ancient and minor cereals is due to the rising demand for foods with a traditional and natural appeal, as well as being healthy thanks to higher content of protein, fiber, micronutrients, and bioactive compounds. Moreover, minor and ancient crops well satisfy the need to preserve genetic diversity and, thanks to the high adaptability to various pedoclimatic conditions, they offer an economic alternative to the expensive import of the major cereals in several developing regions. Despite the high nutritional value of these grains, the presence of different ANFs, and sometimes poor technological and sensory properties, may restrict their use as food ingredients. The application of sourdough biotechnology, through spontaneous fermentation or by the use of selected LAB as starters, has largely been reported as a suitable tool to reduce ANFs, increasing the nutritional value of sourdough baked goods. Moreover, based on the scientific evidence, the use of sourdough allows for overcoming the technological drawbacks of both high-fiber and gluten-free flours, making their use possible in baked goods. Overall, the efficacy of the use of proper selected starters in order to standardize and optimize the positive effects of the fermentation process is widely documented. Consumers’ demands for natural and healthy foods continuously drive the research interest toward the use of ancient and minor cereals in both traditional and innovative food formulations.

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