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Cereal Foods World, Vol. 64, No. 5
DOI: https://doi.org/10.1094/CFW-64-5-0054
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Sorghum as a Healthy Global Food Security Crop: Opportunities and Challenges
Tadesse F. Teferra1,2 and Joseph M. Awika1,3

1 Department of Soil and Crop Sciences and Department of Nutrition and Food Science, Texas A&M University, College Station, TX 77843, U.S.A.

2 School of Nutrition and Food Science, Hawassa University, Hawassa, SNNPR, Ethiopia. Facebook: Tadesse Fikre Teferra; LinkedIn: www.linkedin.com/in/tadesse-fikre-teferra-phd-449b9817.

3 Corresponding author. E-mail awika@tamu.edu


© 2019 AACC International, Inc.

Abstract

Climate change is an enormous challenge facing humanity. To meet this challenge, a shift toward more climate resilient, but underdeveloped and underutilized, crops such as sorghum is of great interest. Sorghum performs relatively well under water scarcity and elevated temperature conditions compared with the major cereal crops wheat, rice, and maize (corn). From a nutritional perspective, a major advantage of sorghum as a healthy and nutritious crop is its higher proportion of slowly digestible and resistant starch components compared with other staple cereal crops. This property of sorghum reduces postprandial hyperglycemia in humans and could potentially be manipulated to reduce overall calorie intake from products made with sorghum. Sorghum also is uniquely rich in diverse bioactive polyphenols and other beneficial compounds that are associated with reduced risk of nutrition-linked chronic diseases, including type 2 diabetes, cardiovascular disease, and some types of cancer. Some of the bioactive compounds found in sorghum, such as high molecular weight tannins, also have technological benefits due to their ability to modify protein and starch functionality, which can be used to produce new bioactive ingredients or enhance food quality. The key challenges associated with use of sorghum as a food ingredient are its lower endosperm functionality and relatively low protein digestibility; both attributes are related to the tendency of the hydrophobic sorghum endosperm protein kafirin to cross-link during processing. Recent developments in the utilization of traditional genetics to alter the structure and functionality of the kafirin protein in sorghum show a lot of promise for unlocking the full food use potential of sorghum. These improved sorghum lines have demonstrated enhanced food use quality and protein digestibility. This review summarizes emerging opportunities and challenges associated with sorghum production and utilization as a healthy food ingredient.





Opportunities for Sorghum as a Food Crop

Sorghum (Sorghum bicolor) is an important food crop that is consumed by millions of people as a staple food source in arid and semi-arid areas of the developing world, especially Africa. In the developed world, including Australia and the United States, sorghum is primarily produced for livestock feed and industrial uses such as bioethanol production. However, due to the increasing body of evidence and awareness of its beneficial health-promoting properties (18), there is growing demand for and use of sorghum in the food markets of the developed world (8). The emerging evidence indicating sorghum has beneficial properties, such as slowly digestible starch (SDS) (29); unique bioactive flavonoids (41,42); and activity against inflammation (2), oxidative stress, and cardiovascular disease (7), is expected to expand the opportunities for utilization of sorghum as a food source. Given the dominant role played by obesity in noncommunicable chronic diseases globally, as well as other undesirable consequences of excess calorie intake, the beneficial attributes of sorghum should make the crop more attractive as a food grain. Nevertheless, sorghum remains primarily a food consumed by the poor; thus, strategies to enhance its key nutritional attributes (especially its protein and micronutrient qualities) to meet the dietary needs of these populations are critically important. Based on the latest FAOSTAT report, the estimated global production of sorghum in 2017 was only 57.6 million metric tons, whereas 770–1,134 million metric tons of the three largest cereal crops (wheat, maize [corn], and rice) were produced. These statistics suggest that with innovative value chain development to take advantage of its unique properties, sorghum production and use for food could expand considerably in the future. This would not only benefit consumer health, but also the environment, because sorghum is one of the most drought-tolerant food crops and has relatively low input requirements.

Sorghum as a Sustainable “Crop of the Future” and Its Role in Global Food Security

Suitability for the Changing Climate. Climate change is recognized as one of the greatest challenges facing humans with regard to global food security and environmental sustainability (21). The yields of many major staple crops have been shown to decrease under the expanding desertification conditions associated with climate change in Africa (12). The International Food Policy Research Institute (IFPRI) has projected that sorghum is one of only a few crops with increased yield potential in sub-Saharan Africa under such conditions (28). The IFPRI projection suggests that the yields for other major cereal crops, such as wheat and maize, as well as root and tuber crops, such as sweet potato, yam, and cassava, will be reduced by 5–25%, while sorghum yield will increase (Fig. 1). Based on the model projections for sub-Saharan Africa, it is clear that sorghum remains one of only a few crops that is adapted to the changing climate in a world continuously facing scarcity of water for crop production and rising temperatures. Sorghum is, therefore, a crop well-suited for the future and as a food and feed security crop for an increasing proportion of the global population.

Improving sorghum quality for food applications, both traditional and new, is important to ensure broad and sustainable market appeal for the crop. In global sorghum improvement efforts, breeders, processors, and nutritionists must work hand in hand to make sorghum more relevant to consumers in both developed and developing regions of the world. Research endeavors should focus on increasing yield, improving processing quality and sensory attributes, and enhancing the nutritional properties of sorghum.

Low Cost of Production and Higher Net Return. Compared with other staple cereal crops such as maize, sorghum generally has a lower cost of production (e.g., cost of seed, fertilizer, land rent, pesticides, etc.) and higher net income (31). In a comparative water-deficit irrigation trial of sorghum and maize reported by Farré and Faci (16), sorghum performed better than maize in terms of aboveground biomass, harvest index, and water use efficiency. This indicates that the return from sorghum is better than that from maize in water-deficit, arid, and semi-arid regions of the world.

A meta-analysis reported by Zereyesus and Dalton (43) indicated that the social returns on research investment in sorghum and millets are positive and high, at about 20% per year. The report pointed out that research is generating large producer and consumer benefits for billions of individuals living in the traditional sorghum-producing agricultural belt (arid and semi-arid regions) around the globe. It is obvious that sorghum has great potential as a sustainable and profitable crop production system with significant resilience to environmental stresses caused by climate change.

Health Benefits of Sorghum as a Food

“Good” Carbohydrates. Starch is the most abundant storage polysaccharide on earth, and it supplies the majority of calories to humans and other forms of life. Starch used for food and industrial applications is primarily obtained from cereal grains. In cereal grains, starch digestibility is largely impacted by endosperm properties and processing methods. Sorghum is generally known to contain “good” carbohydrates because it has a higher proportion of resistant starch (RS) and SDS components (27), which have been associated with beneficial properties in human studies (5,29). The higher proportion of RS and SDS in sorghum can help consumers experience satiety for a longer time, potentially cutting the frequency of snacking and caloric intake, which in turn contributes to a low glycemic index (29) and reduced risk of developing chronic health conditions, such as type 2 diabetes and overweight. Although the precise mechanisms for the slow digesting property of sorghum starch is not well understood, it may be related to sorghum polyphenols and endosperm protein properties (4,13,44). The ability of sorghum-based diets to reduce hyperglycemia makes sorghum one of only a few “ancient grain” crops (33) with demonstrated health benefits that consumers are seeking.

Bioactive Compounds. Sorghum contains relatively high levels of phytochemicals that are beneficial to health, including phenolic compounds, phytosterols, and policosanols (9,18). The dominant phytochemicals found in sorghum are phenolic compounds, including phenolic acids and flavonoids. The phenolic acids found in sorghum are mainly benzoic and cinnamic acid derivatives, while the flavonoids are categorized into several subclasses, including 3-deoxyanthocyanins (unique to sorghum), flavones, flavanones, and condensed tannins (proanthocyanidins) (9,15,18). Interest in phytochemicals as functional components of human diets has grown because they play important roles as antioxidants and anti-inflammatory agents and have other potential health-promoting effects. For example, a recent study involving healthy human subjects showed that pasta containing red whole grain sorghum significantly improved antioxidant status by increasing plasma polyphenols, antioxidant capacity, and superoxide dismutase activity, while decreasing a marker of protein oxidation compared with a control pasta made from durum wheat semolina (22). Apart from their antioxidant activities, polymeric tannins from sorghum have been reported to reduce in vitro digestibility of partially gelatinized starch by forming well-organized complexes with the starch (3,4). This property could potentially lead to the development of new starch-based ingredients and products with reduced calories. We recently reviewed the latest evidence-related, health-beneficial effects of sorghum polyphenols in great detail (18). In general, the evidence indicates that sorghum contains a unique mixture of bioactive compounds that can play an important role in chronic disease prevention when regularly consumed in the diet.

Technological Appeal of Sorghum Phytochemicals. Sorghum polyphenols are important functional ingredients that can serve as natural food additives (18). The high molecular weight condensed tannins (proanthocyanidins) from sorghum have been reported to improve dough rheology by interacting with gliadin and glutenin fractions of wheat proteins, which increase dough strength and resistance to overmixing (19,20). It was shown in the same research that proanthocyanidins from sorghum performed better than oligomeric tannins from grapes, indicating the potential for use of sorghum as a food ingredient with both nutritional and functional benefits. Sorghum tannins are also being studied for their potential to retard lipid oxidation in meat products due to their powerful antioxidant properties. The 3-deoxyanthocyanin pigments are unique to sorghum and have been shown to have a high potential as natural food colorants due to their stability under food processing and handling conditions relative to other water-soluble natural colorants such as anthocyanins (17,24). Technologies to exploit these unique functional sorghum pigments are currently being explored.

In addition to the health-beneficial bioactive compounds found in whole sorghum, by-products of grain milling, such as bran, can be a source of extractable phytochemical components that can be utilized as high-value functional food ingredients. For example, sorghum is rich in flavones, a group of highly bioactive flavonoids most commonly associated with cereal grains, which are their primary dietary source (10,41). These compounds can be extracted from sorghum bran for use in various health-promoting applications. The pericarp of sorghum varies widely in color (Fig. 2), depending largely on the phenolic composition and content of the sorghum (8,32), and this variation can add to the desirability and diversity of products made from sorghum.

Sensory Appeal. Despite the misconception among some consumers that sorghum is bitter or astringent due to the presence of tannins in some varieties, sensory evaluation in controlled studies has revealed that this is not the case. Scores for sorghum products generally are similar to or better than scores for other cereal grain products. For example, a sorghum-based whole grain cereal was recently shown to have an appealing flavor, with better overall consumer acceptability compared with a wheat-based whole grain cereal (6). Furthermore, contrary to common perceptions, sorghum tannins do not affect the flavor of most sorghum-based products (36), because during processing sorghum tannins strongly bind to proteins and/or carbohydrates, making them unavailable to interact with salivary proteins and taste receptors. This implies that sorghum varieties that are high in bioactive polyphenols can be processed into products that will meet consumer expectations for flavor, while delivering health benefits. A major limitation of sorghum-based foods, however, is a gritty or sandy texture that is primarily caused by hydrophobic sorghum endosperm proteins that limit starch hydration and swelling during cooking. Thus, sorghum generally requires adjustment of processing conditions to properly gelatinize starch and produce a desirable product texture.

Challenges to Sorghum Use as a Food Ingredient

Protein Quality. Sorghum proteins, also known as kafirins, belong to a group of grain proteins called prolamins. Sorghum kafirins have higher hydrophobicity compared with maize zein protein, rice proteins, and wheat prolamins (11). There are three major subclasses of sorghum kafirin proteins based on molecular weight: α, β, and γ-kafirins. The relative abundance of the α, β, and γ-kafirin subclasses are 80, 13, and 7%, respectively (39). Kafirin protein bodies are organized into small globular protein bodies in such a way that the more protease-resistant and hydrophobic β and γ-kafirins enclose the more digestible and less hydrophobic α-kafirin component (39). Thus, sorghum proteins have 40–60% lower digestibility compared with proteins from other cereal grains (14), and digestibility decreases further during cooking due to formation of disulfide cross-linking of the kafirin proteins (1). This means that sorghum has relatively poor protein quality in food applications, which reduces its nutritional value to humans, especially those who rely on sorghum as a staple food source.

Similar to most cereal grains, sorghum has a low concentration of some essential amino acids, with the most limiting being lysine. Except for some success regarding the development of high-lysine maize, also known as quality protein maize, the protein quality of many cereals, including sorghum, has not been substantially improved. Some trials focused on developing a high-digestibility, high-lysine (hdhl) sorghum variety and its associated shortcomings will be discussed later.

Endosperm Functionality. Sorghum has reduced endosperm functionality in many food systems relative to other cereal grains, limiting its use in commercial food processing. The hydrophobic kafirin proteins limit hydration of sorghum starch, requiring higher cooking temperatures and resulting in a dry and sandy product texture (40) and reduced product shelf life. These attributes of sorghum-based foods are usually not appealing to consumers. The shorter shelf life of sorghum products is due to the limited interaction of the proteins and starches with water, which results in faster moisture migration and staling.

Reduced endosperm functionality limits the use of sorghum in gluten-free and other product lines targeting modern food applications. Use of additives such as hydrocolloids and emulsifiers may help improve the functionality of sorghum flour in high-moisture and minimally leavened products such as pancakes and muffins and needs to be studied. Obviously, for sorghum to be a competitive alternative ingredient in modern food applications, the limitations related to its endosperm functionality must be addressed in fundamental ways, either through genetic- or process-based innovations.

Current Developments in Enhancement of Sorghum Functionality and Competitiveness

The low protein digestibility of sorghum was recognized in the early 1960s (30,37), and research to improve kafirin protein digestibility has been a major focus area over the past several decades. The discovery of a high-lysine (hl) sorghum line was reported by Singh and Axtell (30), and it was believed it would improve sorghum protein quality and biological value. However, sorghum protein digestibility remained a challenge. Lines with high uncooked and cooked digestibility were later discovered in a population of inbred, high-lysine Ethiopian sorghum varieties (38). The highly digestible (hd) proteins had irregularly shaped folded proteins (25,26). It was later established that the proteins in mutant sorghum varieties with better digestibility also had improved interaction with water and overall functionality in batter-based systems (11,34). The original hd sorghum line, however, was not commercially viable because it has an extremely soft endosperm that limits grain handling and processing. The soft endosperm also generally makes the crop more susceptible to attacks by insects and mold in the field.
Breeding efforts to improve the endosperm hardness of hd sorghum have been ongoing (34,35). The irregularly shaped hd protein body (Fig. 3) has successfully been transferred into well-established hard-endosperm sorghum hybrids, with recent evidence indicating that improved protein digestibility (25–40% higher than for wild-type sorghum) and flour functionality generally are maintained (34). Another advantage observed for the new hd sorghum lines is an average increase in lysine content of 50% versus wild-type sorghum. Along these lines, the new clustered regularly interspaced short palindromic repeats (CRISPR) gene-editing technique recently was used successfully to create sorghum variants with reduced kafirin levels and improved protein quality (increased lysine content) and digestibility (23). This presents a new opportunity for more rapid and precise sorghum improvement for protein quality and endosperm functionality. Because sorghum endosperm functionality is a major bottleneck to sorghum use in food applications, these genetic techniques targeting sorghum proteins have great potential to enhance broader use of sorghum as a food ingredient. Such techniques also could potentially be used to enhance the levels of specific bioactive compounds in sorghum for targeted food and health-promoting applications.

Future Directions

Future efforts to genetically improve sorghum for food applications should include important traits such as high protein digestibility and quality (e.g., hdhl) as a matter of routine to ensure sorghum becomes and remains a competitive food crop. The composition of bioactive compounds in sorghum is important to consider for potential development of health-promoting food applications. Research efforts demonstrating the specific benefits of different sorghum bioactive profiles in humans are critical to ensuring sorghum is positioned to have a maximum impact on human health through genetic and food processing innovations. New product and processing technologies that improve sorghum functionality and the sensory acceptability and shelf life of products are of interest and need to be considered. Government agencies involved in public health should be targeted in sorghum research dissemination to influence policies that promote sorghum use and, eventually, healthy food choices by consumers.

Summary

Sorghum is one of only a few crops that is well adapted for tolerating global climate change and the water scarcity associated with it. Nutritionally, sorghum has a key advantage over other cereal grains in that it has a higher proportion of RS and SDS compared with many staple cereals, improving satiety and glycemic control. Sorghum also contains high levels of diverse bioactive compounds that have significant positive effects on human health. On the other hand, sorghum use in human food is limited, largely by the nature of its proteins. The protein bodies in sorghum endosperm (kafirins) are relatively hydrophobic, which restricts the interaction of the endosperm with water and, thus, the ability of starch to swell and form a gel network. This commonly results in sorghum-based foods with a gritty texture and dry mouthfeel. The new genetically improved sorghum varieties with enhanced endosperm functionality, developed from hd mutants, show a lot of promise for unlocking the food use potential of sorghum.


 

Tadesse Fikre Teferra is an assistant professor of food science and postharvest technology at Hawassa University, Ethiopia. He received his B.S. degree in food science and postharvest technology from Hawassa University; M.S. degree in food engineering from Haramaya University, Ethiopia; and Ph.D. degree in food science and technology from Texas A&M University, TX, U.S.A., in 2019. Tadesse’s research interests include development of indigenous food processing technologies in Africa to reduce postharvest losses and benefit farming communities to ensure food availability. Tadesse also envisions bringing batch-processed, healthy traditional foods from village kitchens in Africa to continuous and mass-processing schemes on the floors of industrial food manufacturers. Tadesse also is working with his colleagues at Hawassa University and fellow Ethiopian food technologists to establish a professional society at the national level.

Joseph M. Awika is professor of food science at Texas A&M University. He received his Ph.D. degree from Texas A&M, TX, U.S.A., in 2003 and B.S. degree from Egerton University, Kenya. He joined the Texas A&M faculty in 2008 after previously working at the University of Missouri (2006–2008) and Arkansas State University (2004–2005). Joseph teaches courses in grain processing and carbohydrate chemistry, as well as the capstone course for the Food Science and Technology undergraduate program. Joseph’s research is focused on generating knowledge to improve the quality of grain-based foods to ensure disease prevention and optimal human health. He collaborates extensively with international programs in multiple countries. His pioneering work on the chemistry and bioactive properties of polyphenols from sorghum has led to considerable food industry interest and use of sorghum for healthy foods. He currently serves as editor of the Journal of Cereal Science.

References

  1. Aboubacar, A., Axtell, J. D., Huang, C.-P., and Hamaker, B. R. A rapid protein digestibility assay for identifying highly digestible sorghum lines. Cereal Chem. 78:160, 2001.
  2. Agah, S., Kim, H., Mertens-Talcott, S. U., and Awika, J. M. Complementary cereals and legumes for health: Synergistic interaction of sorghum flavones and cowpea flavonols against LPS-induced inflammation in colonic myofibroblasts. Mol. Nutr. Food Res. 61(7). DOI: https://doi.org/10.1002/mnfr.201600625. 2017.
  3. Amoako, D. B., and Awika, J. M. Polymeric tannins significantly alter properties and in vitro digestibility of partially gelatinized intact starch granule. Food Chem. 208:10, 2016.
  4. Amoako, D. B., and Awika, J. M. Resistant starch formation through intrahelical V-complexes between polymeric proanthocyanidins and amylose. Food Chem. 285:326, 2019.
  5. Anunciaçãoa, P. C., de Morais Cardoso, L., Gomes, J. V. P., Della Lucia, C. M., Carvalho, C. W. P., Galdeano, M. C., Vieira Queiroz, V. A., de Cássia Gonçalves Alfenas, R., Stampini Duarte Martino, H., and Pinheiro-Sant’ana, H. M. Comparing sorghum and wheat whole grain breakfast cereals: Sensorial acceptance and bioactive compound content. Food Chem. 221:984, 2017.
  6. Anunciação, P. C., de Morais Cardoso, L., Vieira Queiroz, V. A., de Menezes, C. B., Carvalho, C. W. P., Pinheiro-Sant’ana, H. M., and de Cássia Gonçalves Alfenas, R. Consumption of a drink containing extruded sorghum reduces glycaemic response of the subsequent meal. Eur. J. Nutr. 57:251, 2018.
  7. Arbex, P. M., de Castro Moreira, M. E., Lopes Toledo, R. C., de Morais Cardoso, L., Pinheiro-Sant’ana, H. M., dos Anjos Benjamin, L., Licursi, L., Carvalho, C. W. P., Vieira Queiroz, V. A., and Stampini Duarte Martino, H. Extruded sorghum flour (Sorghum bicolor L.) modulates adiposity and inflammation in high fat diet-induced obese rats. J. Funct. Foods 42:346, 2018.
  8. Awika, J. M. Sorghum: Its unique nutritional and health-promoting attributes. Page 21 in: Gluten-Free Ancient Grains: Cereals, Pseudocereals, and Legumes: Sustainable, Nutritious, and Health-Promoting Foods for the 21st Century. Woodhead Publishing Series in Food Science, Technology and Nutrition. J. R. N. Taylor and J. M. Awika, eds. Woodhead Publishing, Sawston, U.K., 2017.
  9. Awika, J. M., and Rooney, L. W. Sorghum phytochemicals and their potential impact on human health. Phytochemistry 65:1199, 2004.
  10. Awika, J. M., Rose, D. J., and Simsek, S. Complementary effects of cereal and pulse polyphenols and dietary fiber on chronic inflammation and gut health. Food Funct. 9:1389, 2018.
  11. Belton, P., Delgadillo, I., Halford, N., and Shewry, P. Kafirin structure and functionality. J. Cereal Sci. 44:272, 2006.
  12. Chijioke, O. B., Haile, M., and Waschkeit, C. Implication of climate change on crop yield and food accessibility in sub-Saharan Africa. Published online at www.zef.de/fileadmin/downloads/forum/docprog/Termpapers/2011_1_Oyiga__Haile_Waschkeit.pdf. Centre for Development Research, University of Bonn, Bonn, Germany, 2011.
  13. Dunn, K. L., Yang, L., Girard, A., Bean, S., and Awika, J. M. Interaction of sorghum tannins with wheat proteins and effect on in vitro starch and protein digestibility in a baked product matrix. J. Agric. Food Chem. 63:1234, 2015.
  14. Duodu, K., Taylor, J., Belton, P., and Hamaker, B. Factors affecting sorghum protein digestibility. J. Cereal Sci. 38:117, 2003.
  15. Dykes, L., Seitz, L. M., Rooney, W. L., and Rooney, L. W. Flavonoid composition of red sorghum genotypes. Food Chem. 116:313, 2009.
  16. Farré, I., and Faci, J. M. Comparative response of maize (Zea mays L.) and sorghum (Sorghum bicolor L. Moench) to deficit irrigation in a Mediterranean environment. Agric. Water Manag. 83:135, 2006.
  17. Geera, B., Ojwang, L. O., and Awika, J. M. New highly stable dimeric 3-deoxyanthocyanidin pigments from sorghum bicolor leaf sheath. J. Food Sci. 77:C566, 2012.
  18. Girard, A. L., and Awika, J. M. Sorghum polyphenols and other bioactive components as functional and health promoting food ingredients. J. Cereal Sci. 84:112, 2018.
  19. Girard, A. L., Bean, S. R., Tilley, M., Adrianos, S. L., and Awika, J. M. Interaction mechanisms of condensed tannins (proanthocyanidins) with wheat gluten proteins. Food Chem. 245:1154, 2018.
  20. Girard, A. L., Castell-Perez, M. E., Bean, S. R., Adrianos, S. L., and Awika, J. M. Effect of condensed tannin profile on wheat flour dough rheology. J. Agric. Food Chem. 64:7348, 2016.
  21. Godfray, H. C. J., and Garnett, T. Food security and sustainable intensification. Philos. Trans. R. Soc. B Biol. Sci. 369(1639). DOI: https://doi.org/10.1098/rstb.2012.0273. 2014.
  22. Khan, I., Yousif, A. M., Johnson, S. K., and Gamlath, S. Acute effect of sorghum flour-containing pasta on plasma total polyphenols, antioxidant capacity and oxidative stress markers in healthy subjects: A randomised controlled trial. Clin. Nutr. 34:415, 2015.
  23. Li, A., Jia, S., Yobi, A., Ge, Z., Sato, S. J., Zhang, C., Angelovici, R., Clemente, T. E., and Holding, D. R. Editing of an α-kafirin gene family increases, digestibility and protein quality in sorghum. Plant Physiol. 177:1425, 2018.
  24. Ojwang, L. O., and Awika, J. M. Stability of apigeninidin and its methoxylated derivatives in the presence of sulfites. J. Agric. Food Chem. 58:9077, 2010.
  25. Oria, M. P., Hamaker, B. R., Axtell, J. D., and Huang, C.-P. A highly digestible sorghum mutant cultivar exhibits a unique folded structure of endosperm protein bodies. Proc. Natl. Acad. Sci. U.S.A. 97:5065, 2000.
  26. Oria, M. P., Hamaker, B. R., and Shull, J. M. Resistance of sorghum α, β, and γ-kafirins to pepsin digestion. J. Agric. Food Chem. 43:2148, 1995.
  27. Poquette, N. M., Gu, X., and Lee, S.-O. Grain sorghum muffin reduces glucose and insulin responses in men. Food Funct. 5:894, 2014.
  28. Ringler, C., Zhu, T., Cai, X., Koo, J., and Wang, D. Climate change impacts on food security in sub-Saharan Africa. Insights from comprehensive climate change scenarios. International Food Policy Research Institute, Washington, DC, 2010.
  29. Simnadis, T. G., Tapsell, L. C., and Beck, E. J. Effect of sorghum consumption on health outcomes: A systematic review. Nutr. Rev. 74:690, 2016.
  30. Singh, R., and Axtell, J. D. High lysine mutant gene (hl) that improves protein quality and biological value of grain sorghum. Crop Sci. 13:535, 1973.
  31. Staggenborg, S. A., Dhuyvetter, K. C., and Gordon, W. Grain sorghum and corn comparisons: Yield, economic, and environmental responses. Agron. J. 100:1600, 2008.
  32. Taleon, V., Dykes, L., Rooney, W., and Rooney, L. Environmental effect on flavonoid concentrations and profiles of red and lemon-yellow sorghum grains. J. Food Compos. Anal. 34:178, 2014.
  33. Taylor, J. R. N., and Awika, J. M., eds. Gluten-Free Ancient Grains: Cereals, Pseudocereals, and Legumes: Sustainable, Nutritious, and Health-Promoting Foods for the 21st Century. Woodhead Publishing Series in Food Science, Technology and Nutrition. Woodhead Publishing, Sawston, U.K., 2017.
  34. Teferra, T. F., Amoako, D. B., Rooney, W. L., and Awika, J. M. Qualitative assessment of ‘highly digestible’ protein mutation in hard endosperm sorghum and its functional properties. Food Chem. 271:561, 2019.
  35. Tesso, T., Ejeta, G., Chandrashekar, A., Huang, C.-P., Tandjung, A., Lewamy, M., Axtell, J. D., and Hamaker, B. R. A novel modified endosperm texture in a mutant high-protein digestibility/high-lysine grain sorghum (Sorghum bicolor (L.) Moench). Cereal Chem. 83:194, 2006.
  36. Vieira Queiroz, V. A., da Silva Aguiar, A., de Menezes, C. B., de Carvalho, C. W. P., Paiva, C. L., Costa Fonseca, P., and da Conceição, R. R. P. A low calorie and nutritive sorghum powdered drink mix: Influence of tannin on the sensorial and functional properties. J. Cereal Sci. 79:43, 2018.
  37. Virupaksha, T., and Sastry, L. Protein content and amino acid composition of some varieties of grain sorghum. J. Agric. Food Chem. 16:199, 1968.
  38. Weaver, C. A., Hamaker, B. R., and Axtell, J. D. Discovery of grain sorghum germ plasm with high uncooked and cooked in vitro protein digestibilities. Cereal Chem. 75:665, 1998.
  39. Winn, J. A., Mason, R. E., Robbins, A. L., Rooney, W. L., and Hays, D. B. QTL mapping of a high protein digestibility trait in Sorghum bicolor. Int. J. Plant Genomics 2009(2). DOI: http://dx.doi.org/10.1155/2009/471853. 2009.
  40. Wong, J. H., Lau, T., Cai, N., Singh, J., Pedersen, J. F., Vensel, W. H., Hurkman, W. J., Wilson, J. D., Lemaux, P. G., and Buchanan, B. B. Digestibility of protein and starch from sorghum (Sorghum bicolor) is linked to biochemical and structural features of grain endosperm. J. Cereal Sci. 49:73, 2009.
  41. Yang, L., Allred, K. F., Dykes, L., Allred, C. D., and Awika, J. M. Enhanced action of apigenin and naringenin combination on estrogen receptor activation in non-malignant colonocytes: Implications on sorghum-derived phytoestrogens. Food Funct. 6:749, 2015.
  42. Yang, L., Allred, K. F., Geera, B., Allred, C. D., and Awika, J. M. Sorghum phenolics demonstrate estrogenic action and induce apoptosis in nonmalignant colonocytes. Nutr. Cancer 64:419, 2012.
  43. Zereyesus, Y. A., and Dalton, T. J. Rates of return to sorghum and millet research investments: A meta-analysis. PloS One 12(7). DOI: https://doi.org/10.1371/journal.pone.0180414. 2017.
  44. Zhang, G., and Hamaker, B. R. Low α-amylase starch digestibility of cooked sorghum flours and the effect of protein. Cereal Chem. 75:710, 1998.