Received: 27 January 2020 Revised: 30 March 2020 Accepted: 15 April 2020

DOI: 10.1111/1541-4337.12572

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

Effects of edible plant polyphenols on gluten protein functionality

and potential applications of polyphenol–gluten interactions

Audrey L. Girard1 Joseph M. Awika1,2

1 Department
of Soil and Crop Sciences, Texas
A&M University, College Station, Texas
2 Department
of Nutrition and Food Science,
Texas A&M University, College Station,
Texas
Correspondence
Audrey L. Girard, Department of Soil and Crop
Sciences, Texas A&M University, 370 Olsen
Blvd, College Station, TX 77843.
Email: agirard@tamu.edu
Abstract
Expanding plant-based protein applications is increasingly popular. Polyphenol
interactions with wheat gluten proteins can be exploited to create novel functional
foods and food ingredients. Polyphenols are antioxidants, thus generally decrease
gluten strength by reducing disulfide cross-linking. Monomeric polyphenols can
be used to reduce dough mix time and improve flexibility of the gluten network,
including to plasticize gluten films. However, high-molecular-weight polyphenols
(tannins) cross-link gluten proteins, thereby increasing protein network density and
strength. Tannin–gluten interactions can greatly increase gluten tensile strength in
dough matrices, as well as batter viscosity and stability. This could be leveraged
to reduce detrimental effects of healthful inclusions, like bran and fiber, to loaf
breads and other wheat-based products. Further, the dual functions of tannins as
an antioxidant and gluten cross-linker could help restructure gluten proteins and
improve the texture of plant-based meat alternatives. Tannin–gluten interactions may
also be used to reduce inflammatory effects of gluten experienced by those with
gluten allergies and celiac disease. Other potential applications of tannin–gluten
interactions include formation of food matrices to reduce starch digestibility; creation
of novel biomaterials for edible films or medical second skin type bandages; or
targeted distribution of micronutrients in the digestive tract. This review focuses
on the effects of polyphenols on wheat gluten functionality and discusses emerging
opportunities to employ polyphenol–gluten interactions.

KEYWORDS
bioactive compound, plant protein, polyphenol, tannin, wheat gluten

1 I N T RO D U C T I O N to form leavened bread and flatbreads. The viscoelasticity

Wheat gluten proteins, gliadins and glutenins, interact when
hydrated and with addition of mechanical energy to form
a viscoelastic protein network. This network allows for a
dough that can be stretched (extensibility) and will spring
back together (elasticity): it allows for doughs to be sheeted,
manipulated, formed into a variety of products, and to leaven.
No other grain proteins have equivalent properties. Though
wheat gluten proteins comprise less than 20% of wheat flour,
they are largely responsible for wheat flour’s unique ability
Compr Rev Food Sci Food Saf. 2020;1–36.
of gluten is an important function in an array of products
including pretzels, bagels, pastries, noodles, and pastas.
Wheat gluten has properties that make it amenable to a
wide range of applications outside of commonly considered
bakery products. Viscoelasticity is the defining feature of
unmodified gluten. Other characteristics that make gluten
highly functional include that it is water insoluble and binds
about twice its weight in water. Gluten also has a light,
off-white color and a rather bland flavor. Further, compared
to other protein sources including soy and whey protein
wileyonlinelibrary.com/journal/crf3 © 2020 Institute of Food Technologists® 1
2 EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
isolates, gluten is a less expensive ingredient for meat
mimetics. Isolated gluten is used to fortify bakery products
and to create meat extenders and mimetics, among other
applications.
However, gluten has its limitations. Principally, gluten
quality is highly influenced by wheat genetics and growing
environment; that is, not all gluten is equal. Gluten proteins
interact primarily through disulfide cross-linking, which
creates large protein networks (Jazaeri et al., 2015). Thus,
to ensure consistent gluten properties for intended use, the
functionality of gluten is often modulated with oxidizing
or reducing agents to strengthen or weaken the dough,
respectively, by altering disulfide–sulfhydryl interchange
reactions (Lagrain, Thewissen, Brijs, & Delcour, 2007). The
low water solubility of gluten also gives it poor foaming and
emulsion properties (Joye & McClements, 2014; Takeda,
Matsumura, & Shimizu, 2001). Gluten can be hydrolyzed or
deamidated to improve solubility, foaming, and emulsifying
qualities (Yong, Yamaguchi, & Matsumura, 2006).
Polyphenols are often added to wheat-based foods, not
because of their effect on gluten, but rather for potential
health benefits (Sivam, Sun-Waterhouse, Waterhouse, Quek,
& Perera, 2011; Sui, Zhang, & Zhou, 2016a) or inadvertently
as part of another ingredient like bran or fruit pieces (Fu,
Chang, & Shiau, 2015; Khalid, Ohm, & Simsek, 2017;
Snelders, Dornez, Delcour, & Courtin, 2014). Monomeric
polyphenols include ubiquitous phenolic acids and flavonoids
found in cereal and pulse grains, fruits, and various vegeta-
bles. Polymeric polyphenols (tannins) are found in fruits such
as grapes and apples, cocoa, and some varieties of cereal and
pulse grains.
As antioxidants, polyphenols generally weaken gluten
through their redox reaction on gluten disulfide cross-linkages
therefore reducing the size of network-forming polymeric
proteins (Dunn, Yang, Girard, Bean, & Awika, 2015; Han &
Koh, 2011b; Sivam, Sun-Waterhouse, Perera, & Waterhouse,
2012). The antioxidant properties of monomeric polyphenols
could be used in products that do not benefit from strong
gluten development but require high mechanical energy
inputs. For instance, cookies that are sheeted and die-cut
or flatbreads that are hot-pressed will exhibit shrinkage if
the dough is too elastic. By reducing the gluten strength via
antioxidant effect, monomeric polyphenols reduce elasticity
(Girard et al., 2016; Lin & Zhou, 2018).
However, high-molecular -weight polyphenols (tannins)
can mitigate the antioxidant effect by cross-linking gluten
through extensive hydrogen bonds and hydrophobic interac-
tions, which can strengthen gluten by increasing density of
the protein matrix (Girard, Castell-Perez, Bean, Adrianos, &
Awika, 2016; Zhang et al., 2010). This property can also be
leveraged for novel applications. Tannins could be used as
nonsynthetic (naturally derived) ingredients to improve gluten
strength in weak gluten flour, or to improve network strength
when fortifying components (e.g., bran or other dietary fiber
ingredients) are added to wheat flour formulations. The
gluten-strengthening effect of tannins could be used to create
novel biomaterials such as edible, biodegradable, or active
packaging, as well as plant-based, compostable dishware to
replace plastic or Styrofoam containers. By having both an
antioxidant effect and cross-linking gluten, tannins could
help restructure proteins and improve gluten texturization for
use as a meat mimetic. Better texturization would increase
consumer desirability of meat mimetics, which could reduce
animal product consumption; plant-based protein sources
are more sustainable than many animal products (Eshel,
Shepon, Makov, & Milo, 2014; Searchinger et al., 2019;
Whitmee et al., 2015). Tannin–gluten complexes could be
used to produce barriers that block enzyme access to starch
in a food matrix, further enhancing ability of tannins to
slow starch digestion (Amoako & Awika, 2016; Barros,
Awika, & Rooney, 2012; Dunn et al., 2015). Consequently,
tannin–gluten interactions could be used to produce products
with increased satiety effect, which may contribute to reduced
overall caloric intake.
This review summarizes recent research on the effects
of polyphenols on wheat gluten in relation to how the
effects can be manipulated to expand gluten applications.
Discussion includes phenolic acids, monomeric flavonoids,
and polymeric tannins that are endogenous to wheat and
those commonly added to wheat-based foods. The impact
of these polyphenols on gluten rheology and functionality,
and subsequent potential applications of polyphenol–gluten
interactions are discussed.
2 OVERVIEW O F W H EAT
G LUTEN P ROTEINS
Wheat flour is unique in its ability to form a cohesive and
stretchable dough because of its gluten proteins. Wheat flour
typically contains 8% to 14% protein, and the gluten-forming
proteins account for 80% to 85% of the wheat proteins
(Delcour et al., 2012). Unlike other cereal grain proteins,
wheat gluten proteins form a viscoelastic film network.
Because of this, gluten dough is extensible and elastic, which
allows wheat flour dough to be manipulated, capture gas
during yeast fermentation, and hold its structure.
Gluten viscoelasticity is well studied through rheological
and baking tests, though it is not yet fully understood at a
mechanistic level. Readers are referred to recent reviews
and book chapters for a more in-depth discussion of gluten
viscoelasticity (Barak, Mudgil, & Khatkar, 2015; Delcour &
Hoseney, 2010; Delcour et al., 2012). Briefly, gluten proteins
have approximately 2 mol% cysteine residues (Ewart, 1967;
Rombouts et al., 2009), which can form intermolecular disul-
fide cross-links to create macropolymers. This leads to a large,
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
strong matrix structure. Furthermore, gluten proteins are rich
in glutamine (approximately 33 mol%) and proline (approx-
imately 14 mol%) (Ewart, 1967; Rombouts et al., 2009),
which promote hydrogen bonds and hydrophobic interactions,
respectively, and help stabilize the gluten structure (Hoseney
& Rogers, 1990; McCann & Day, 2013). Tyrosine cross-links
also aid in structure development, though their influence is
dwarfed by disulfide cross-links (Pena, Bernardo, Soler, &
Jouve, 2006; Tilley et al., 2001). Finally, ionic bonding helps
to ensure protein aggregation and subsequent covalent and
noncovalent interactions (McCann & Day, 2013).
2.1 Gluten composition
Gluten is composed of two types of proteins: glutenins and
gliadins. Glutenins are large molecular weight (MW) proteins
with elongated structures that are alcohol soluble only when
reducing agents are applied to break disulfide cross-links (Fu
& Sapirstein, 1996). Based on their size and the alleles on
which they were coded, glutenins are further subdivided into
high- and low-molecular-weight glutenin subunits (HMW-
GS and LMW-GS, respectively). The HMW-GS range in size
from 65 to 90+ kDa, whereas LMW-GS range from 30 to
60 kDa (Delcour & Hoseney, 2010). Glutenins have a three-
domain primary structure: the central domain with small N-
and C-terminal domains on either side. HMW-GS are more
elongated because of their rather large central domains with
600 to 850 amino acid residues, whereas LMW-GS have a
smaller central domain with a relatively globular structure
similar to gliadins (Delcour et al., 2012). Glutenins, especially
HMW-GS, create macropolymers through intermolecular
disulfide bonds and noncovalent interactions (i.e., hydro-
gen bonding, hydrophobic interactions, and ionic bonds).
These macropolymers give the gluten structure strength
and elasticity (Shewry, Popineau, Lafiandra, & Belton,
2000).
Gliadins are relatively smaller MW, globular proteins
that are alcohol soluble (Fu & Sapirstein, 1996) and impart
extensibility to gluten (Fido, Bekes, Gras, & Tatham, 1997).
Gliadins can be further subdivided into 𝛼-, 𝛾-, and 𝜔-gliadins
based on their electrophoretic mobility (Schalk, Lexhaller,
Koehler, & Scherf, 2017). The 𝛼- and 𝛾-gliadins have an
average MW of 30 to 35 kDa and are sulfur rich, whereas 𝜔-
gliadins are 44 to 88 kDa and sulfur poor (Barak et al., 2015).
Gliadins do not readily interact via intermolecular disulfide
bonds, but primarily form intramolecular disulfide bonds.
They mostly interact with glutenins via the aforementioned
noncovalent interactions.
2.2 Gluten quality and functionality
Within wheat there is a large range of “gluten quality”:
simply, the impact of gluten proteins on viscoelasticity.
3
Across wheat gluten quality literature, the subjective terms
of “strong” and “weak” are used to refer to gluten strength
(Jazaeri et al., 2015; MacRitchie, 1973; Miller & Hoseney,
1999). This designation has been used since at least 1900,
when Helen W. Atwater wrote in a USDA bulletin that flours
are classified as strong or weak based on the their quantity of
gluten and thus their bread-making ability (Atwater, 1900).
Protein quantity is of broad importance: more proteins gen-
erally tend to create a larger, more cohesive gluten network
resulting in a bread with greater volume (Finney & Barmore,
1948). However, protein quality plays a much larger role than
quantity in defining gluten functionality.
Gluten functionality is determined by the HMW-GS
present, MW distribution of polymeric proteins (HMW-
GS:LMW-GS), and ratio of glutenins:gliadins. Specific
HMW-GS located on the Glu-D1 loci correlate to better
bread quality, for example, higher volume (Payne, Corfield,
& Blackman, 1979; Payne, Corfield, Holt, & Blackman,
1981). For example, Glu-D1 5 + 10 exhibit greater tensile
strength than Glu-D1 2 + 12. All else equal, wheat lines
with Glu-D1 5 + 10 have a greater amount of unextractable
polymeric proteins, thus a larger MW distribution, than
those with Glu-D1 2 + 12 (Gupta & MacRitchie, 1994). The
greater amount of polymeric protein is possibly explained by
Glu-D1 5 + 10 possessing more cysteine residues (Shewry,
Halford, & Tatham, 1992). Glu-D1 5 + 10 subunits rather
than Glu-D1 2 + 12 is correlated with an increase in dough
strength (Gupta & MacRitchie, 1994) and bread quality
(Payne et al., 1979; Payne et al., 1981). Another indicator
of superior gluten strength is a high HMW-GS:LMW-GS
ratio, as the HMW-GS are larger and create a denser gluten
matrix than LMW-GS (Macritchie & Gupta, 1993). The ratio
of glutenins to gliadins is also important, with a balance
required to get a gluten that is elastic and extensible enough to
expand during fermentation without being too tight to allow
expansion (Macritchie, 1987; Uthayakumaran, Newberry,
Keentok, Stoddard, & Bekes, 2000).
Gluten functionality has a great impact on baked product
quality. The product that has been most extensively studied
is pan bread, because this is the most common method of
wheat consumption in the Western world (Shewry & Hey,
2015). Strong gluten refers to that which will perform well in
pan bread because it is extensively cross-linked when mixed
and offers sufficient extensibility and elasticity. Weak gluten
refers to gluten that is less elastic. Soft endosperm wheats
have weaker gluten (Jazaeri et al., 2015), thus the protein
network is not as extensive as that of hard endosperm wheats.
Products made from soft wheat (cookies, cakes, pies, etc.) do
not benefit from strong gluten and are actually superior with
undeveloped gluten that will not toughen the product. By
contrast, hard endosperm wheats are used for products like
breads and noodles that require strong gluten for the desired
organoleptic properties in finished goods. Of course, genetic
4 EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…

traits create protein quality variation within each wheat 2.4 Current gluten applications
subtype (hard vs. soft endosperm) (Carter, Garland-Campbell,
Wheat flour is the key ingredient in many bakery applications,
Morris, & Kidwell, 2012; Girard et al., 2016; Jazaeri et al.,
which is by far primary use of gluten: from loaf and flatbreads
2015; Jondiko et al., 2012). Additionally, environmental con-
to cakes and pastries, and so forth. Gluten is also employed
ditions also play a significant role in influencing gluten func-
in the form of vital wheat gluten (75 to 80% protein), a
tionality (Peterson, Graybosch, Baenziger, & Grombacher,
co-product of wheat starch production. The main use of vital
1992).
wheat gluten is to fortify weak flours. This increases the
protein content and strength of flours, thus improving dough
2.3 Manipulating gluten functionality mixing tolerance and handling properties in bakery products.
It reduces the need for a variety of different flours for bakers.
Additives are commonly used to overcome natural deficien-
For example, adjusting protein content of flours with gluten
cies including environmental variations, and to expedite the
is common practice in Europe because it creates high-protein
natural aging (oxidation) process of wheat proteins. Gluten
flours with desirable functional attributes without relying on
functionality is manipulated by ingredients added either dur-
imported flours (Day, Augustin, Batey, & Wrigley, 2006).
ing the milling or baking processes. Such ingredients are often
Another prominent use of gluten is as a meat extender
used to modify the major interactions involved in gluten pro-
and mimetic. In Western countries, nonanimal proteins are
tein network formation. For instance, oxidizing agents (e.g.,
becoming increasingly desired by consumers in response
bromates, azodicarbonamide, and dehydroascorbic acid)
to concerns of environmental impact of animal production.
strengthen gluten by oxidizing the thiol groups of cysteine
Eastern countries have a long history of enjoying wheat
residues and driving intermolecular disulfide bond formation
gluten as a protein source, especially Japan and China (Day,
(Delcour et al., 2012). This increases the macropolymer size
2011). Beyond the previously discussed unique viscoelastic
and creates a denser network. Oxidizing agents are commonly
properties of gluten, it binds fat and water effectively, which
used in loaf bread formulations. They strengthen the gluten
can improve slicing qualities of products such as sausage and
in doughs to improve machinability and final product vol-
loaf meats (Day et al., 2006; Xiong, Agyare, & Addo, 2008).
ume and texture (Joye, Lagrain, & Delcour, 2009). Reducing
As mentioned in Section 2.3, extrusion technology is used to
agents (e.g., bisulfites, L-cysteine, and various antioxidants,
texturize gluten. This texturized protein is especially good at
such as ascorbic acid) break disulfide bonds thus decreasing
mimicking the mouthfeel and bite of meat products such as
the size of protein macropolymers and weakening the gluten
chicken nuggets and hamburgers (Kumar et al., 2017).
structure (Delcour et al., 2012). These are commonly used in
Because of gluten’s viscoelasticity, binding properties, and
flatbreads, where reducing agents increase dough extensibil-
comparatively low cost as a protein source, it is also use in a
ity to limit dough shrinkage and produce flatbreads with suf-
wide variety of applications. Gluten is used to fortify protein
ficient surface area (Bejosano & Alviola, 2015).
content of breakfast cereals, in creation of imitation cheeses,
Beyond chemical methods, gluten functionality can also be
and for edible food films, among other uses (Day et al., 2006).
altered by physical methods, such as extrusion. For example,
It is also an important source of protein in animal feeds like
gluten can be extruded to restructure the polymer and mimic
pet food and aquaculture feeds. Further, gluten is used in
the texture of meat, as in textured vegetable protein. Gluten is
nonfood and feed applications, for example, adhesives and
plasticized (melted) and the protein bonds are dissociated and
personal care products (Bietz & Lookhart, 1996).
reassociated during the extrusion process. The protein associ-
ations are generally disulfide bonds initiated by hydrophobic
interactions (Li & Lee, 1996a, 1996b). Processing conditions
greatly affect the protein extrudate structure, with lower 3 D I E TA RY PO LY P H E NOL S
mechanical energy and temperature leading to a less dense R E L E VA N T TO G LU T E N
gluten network and smooth-surfaced extrudates (Redl, Morel,
Bonicel, Vergnes, & Guilbert, 1999). Polyphenols are plant secondary metabolites that function to
Enzymatic hydrolysis is another common method used to protect the plant from disease and pests, serve as signaling
modify gluten. Hydrolysis generally increases gluten solubil- molecules, or aid in structure development. For example,
ity and alters its functionality by reducing polymer size and ferulic acid and p-coumaric acid were reported to help protect
increasing availability of hydrophobic, as well as ionizable, wheat plants from diseases like Fusarium head blight (McK-
amino acid residues (Wouters, Rombouts, Fierens, Brijs, & eehen, Busch, & Fulcher, 1999). Ferulic acid also serves
Delcour, 2016). Ingredients to modify chemical interactions, as an integral cell wall component in cereal grain (Antoine
physical manipulation by processing, and enzymatic mod- et al., 2003). Among the widely distributed polyphenols
ification complement the use of wheat genetics to alter the are phenolic acids, monomeric flavonoids, and polymeric
gluten protein structure for varied and novel applications. tannins. In the diet, these polyphenols are commonly
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
Hydroxybenzoic acids:
p-Hydroxybenzoic acid; R1 = R2 = H
Gallic acid; R1 = R2 = OH
Vanillic acid; R1 = OCH3, R2 = H
Syringic acid; R1 = OCH3; R2 = OCH3
F I G U R E 1 Common dietary phenolic acids structures
derived from whole grain cereals and pulses, fruits, and
vegetables.
Polyphenols offer many potential health benefits including
anti-inflammatory effects (Agah, Kim, Mertens-Talcott, &
Awika, 2017; Mateo Anson et al., 2010), chemoprotective
properties (Amatori et al., 2016; Yang, Allred, Dykes, Allred,
& Awika, 2015), and reduction of cardiovascular disease risk
(Hertog et al., 1995; Jia, Ren, Nie, & Yang, 2017; Mendonca
et al., 2019). Polyphenols are strong antioxidants, which
is one of their modes of action to produce health benefits.
However, the antioxidant effect of polyphenols also reduces
disulfide bonds in gluten, therefore reducing polymeric
protein matrices and thus affecting gluten rheology (Dunn
et al., 2015; Han & Koh, 2011b; Sivam et al., 2012). This
reduction effect generally reduces quality of products that
rely on a strong gluten matrix such as loaf breads.
3.1 Monomeric polyphenols in cereal grains
3.1.1 Phenolic acids in cereal grains
Cereal grain polyphenols are predominantly phenolic acids
(Table 1). Like most cereal grains, wheat contains cinnamic
and benzoic acid derivatives (Figure 1) with the former
being far more abundant. Ferulic acid is the dominant
phenolic acid in cereal grains (including wheat) with minor
amount of syringic, salicylic, vanillic, p-coumaric, and
p-hydroxybenzoic acids (Kim, Tsao, Yang, & Cui, 2006; Li,
Shewry, & Ward, 2008). These phenolic acids, especially
ferulic acid, are largely esterified to hemicelluloses and are a
major component of cell wall structure.
Because 75% to 95% of cereal grain phenolic acids are part
of the cell wall and not easily extractable with organic sol-
vents (Hahn, Faubion, & Rooney, 1983; Heinio et al., 2008;
Li et al., 2008), they have a relatively low bioaccessibility.
For instance, ferulic acid in wheat bran and aleurone were
found to be less than 1% bioaccessible when tested in the
5
Hydroxycinnamic acids:
p-Coumaric acid; R1 = R2 = H
Caffeic acid; R1 = H, R2 = OH
Ferulic acid; R1 = H, R2 = OCH3
Sinapic acid; R1 = R2 = OCH3
dynamic in vitro TNO intestinal model, whereas free ferulic
acid added to flour was found to be almost 60% bioaccessible
(Anson, van den Berg, Havenaar, Bast, & Haenen, 2009).
However, colonic bacteria can release bound polyphenols,
which can then be absorbed into the bloodstream, undergo
phase II metabolism, and circulate through various tissues or
be effluxed from the system. Consuming 70 g of whole wheat
products per day for 8 weeks increased serum dihydroferulic
acid (4×), fecal ferulic acid (2×), and urinary ferulic acid
(2×) as compared to consumption of refined wheat products
(Vitaglione et al., 2014). For an in-depth discussion of bioac-
cessibility and bioavailability of cereal grain polyphenols,
the reader is referred to Angelino et al. (2017).
Conjugated phenolic acids are common in plants, usually
with sugar units esterified to the carboxyl group or associated
with a phenolic hydroxyl group (Mandal, Chakraborty, &
Dey, 2010). For example, most extractable wheat phenolic
acids are conjugated to sugars, with nonconjugated free
phenolic acids accounting for 1% or less of the total phe-
nolic acid content of the grain (Li et al., 2008). The main
extractable phenolic acids can vary by cereal. Conjugated
phenolic acids in various wheat species included mainly
sinapic acid, 2,4-dihydroxybenzoic acid, and ferulic acid
(Li et al., 2008), whereas nonbound sorghum phenolic acids
are largely caffeic acid glycerol esters (Yang, Allred, Geera,
Allred, & Awika, 2012). The conjugations may affect the
phenolic–gluten interaction, depending on how they alter the
antioxidant potential of the phenolic acid.
3.1.2 Monomeric flavonoids in cereal grains
Flavonoids are relatively minor in most cereal grains
(Table 2); those present are largely conjugated to simple
sugars and readily extractable (Awika, Ojwang, & Girard,
2018; Okarter & Liu, 2010; Ravisankar, Abegaz, & Awika,
2018). Flavonoids have a base structure of C6–C3–C6
(Figure 2). Cereal grain flavonoids include anthocyanins,
6 EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…

TABLE 1 Phenolic acids in wheat and common wheat-based product additives

Phenolic acids (𝝁g/g dm)
Source Extractable Unextractable Comments References
Cereal grains
Wheat - Whole grain 3 to 420 200 to 1,300 Phenolic acids mostly Li et al., 2008; Mattila, Pihlava, and Hellstrom,
ferulic acid derivatives 2005; Ndolo and Beta, 2014; Weidner,
Amarowicz, Karamać, and Dąbrowski, 1999
Wheat - Refined 6 to 22 58 to 600 Challacombe et al., 2012; Hatcher and Kruger,
flour 1997; Ndolo and Beta, 2014
Wheat - Bran 55 to 110 1,550 to 5,100 Kim et al., 2006; Mattila et al., 2005; Ndolo and
Beta, 2014
Rye - Whole grain 14 to 160 640 to 1,400 Andreasen, Christensen, Meyer, and Hansen,
2000; Heinio et al., 2008; Mattila et al., 2005;
Weidner et al., 1999
Rye - Refined flour 9 25 Heinio et al., 2008
Rye - Bran 20 to 99 1,170 to 4,100 Heinio et al., 2008; Mattila et al., 2005
Sroghum - Whole 50 to 500 350 to 600 Extractable phenolic acids Hahn et al., 1983; Lohani and
grain mostly caffeoyl Muthukumarappan, 2016
glycerides
Sorghum - Refined NC 100 to 400 Chiremba, Taylor, Rooney, and Beta, 2012
flour
Sorghum - Bran NC 2,300 to 4,400 Chiremba et al., 2012
Pulse grains
Cowpea 148 to 1,176 29 Cai, Hettiarachchy, and Jalaluddin, 2003;
Sosulski and Dabrowski, 1984
Lentils 1,543 to 2,554 NC Xu and Chang, 2010
Dry beans 159 to 1,506 20 to 117 Chen et al., 2015; Xu and Chang, 2009
Other dietary
sources
Grape - Whole fruit 1,550 to 2,570 NC Some varieties have very Mané et al., 2007
little phenolic acid
Grape - Skin 20 to 11,500 NC Mané et al., 2007; Rodríguez Montealegre,
Romero Peces, Chacón Vozmediano, Martínez
Gascueña, and García Romero, 2006
Grape - Seed ND ND Mané et al., 2007; Rodríguez Montealegre et al.,
2006
Apple - Whole fruit 345 to 2,954 NC Mostly hydroxycinnamic Vrhovsek et al., 2004
acid derivatives
Apple - Pomace 55 to 821 NC Cetkovic et al., 2008; Lohani and
Muthukumarappan, 2016; Suárez et al., 2010
Tea - White leaves 43,000 to NC Largely galloyl quinic acids Zhao et al., 2011
105,000 and galloylglucose
Tea - Green leaves 10,422 to 37,000 NC Del Rio et al., 2004; Zhao et al., 2011
Tea - Black leaves 8,784 NC Del Rio et al., 2004
Note. Extractable phenolic acids include both free and conjugated forms. Assumed 20% dm to convert grape phenolic acids reported on wet basis to dry basis; assumed
13% dm for apples.
Abbreviations: ND, none detected; NC, no credible data found.

3-deoxyanthocyanins, flavan-3-ols, and flavones (Awika,
Rose, & Simsek, 2018; Girard & Awika, 2018; Hernandez,
Afonso, Rodriguez, & Diaz, 2011; Pihlava et al., 2015).
Flavones are the most widely distributed flavonoid within
cereal grains (Hernandez et al., 2011; Ravisankar et al.,
2018), and cereal grains are the most significant dietary
source of flavones (Awika, Rose, et al., 2018; Girard &
Awika, 2018). Wheat contains 190 to 365 μg flavones/g
dry mass (dm), which is a similar range to that of sorghum
and maize (Hernandez et al., 2011). In wheat, like most
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION… 7

TABLE 2 Monomeric flavonoids in wheat and common wheat-based product additives

Flavonoids(𝝁g/g dm)
Source Anthocyanins Flavones Flavonols Comments References
Cereal grains
Wheat - Whole 5 to 240 190 to 365 ND Flavones primarily C-6 and/or C-8 Abdel-Aal el and Hucl, 2003; Bartl
grain glycosides of apigenin and et al., 2015; Hernandez et al.,
luteolin; Anthocyanins v. low 2011; Liu, Qiu, and Beta, 2010
except in highly pigmented
grains (e.g., blue or purple)
Wheat - Refined 2 to 20 Abdel-Aal el and Hucl, 2003
flour
Wheat - Bran 10 to 480 Abdel-Aal el and Hucl, 2003
Sorghum - 0 to 700 5 to 390 ND Flavones exist as apigenin, Dykes, Peterson, Rooney, and
Whole grain luteolin, and their glycosides; Rooney, 2011; Dykes, Seitz,
Anthocyanins as Rooney, and Rooney, 2009
3-deoxyanthocyanins
Sorghum - Bran 2,800 to 9,800 Awika et al., 2004, 2005
Sorghum - Leaf 15,100 to 64,800 Geera et al., 2012; Kayodé et al.,
sheath 2011
Pulse grains
Cowpea 875 to 2,100 ND 270 to 1,060 Anthocyanins only found in black Ojwang et al., 2012
and green varieties; Flavonols
mostly quercetin derivatives
Lentils 0 to 665 11 to 77 11 to 347 Flavonols mostly quercetin Amarowicz et al., 2009; Dueñas,
derivatives Hernández, and Estrella, 2007;
Xu and Chang, 2010
Dry beans 0 to 4,012 ND 118 to 677 Anthocyanins in red and black Chen et al., 2015; Xu and Chang,
varieties; Flavonols kaempferol 2009
glucosides and myricetin
Other dietary
sources
Grape - Whole 2,910 to 3,260 ND 132 to 508 Flavonols mostly conjugated Burns et al., 2001; Mané et al.,
fruit quercetin; Anthocyanins in red 2007
grapes, not green
Grape - Skin 15,000 to 32,500 1,000 to 1,150 Mané et al., 2007; Rodríguez
Montealegre et al., 2006
Grape -Seed ND ND Mané et al., 2007; Rodríguez
Montealegre et al., 2006
Apple - Whole 0 to 282 ND 262 to 640 Flavonols mostly quercetin Vrhovsek et al., 2004
fruit conjugates; Anthocyanins
mostly cyanidin conjugates.
Apple - Pomace 589 to 1087 Cetkovic et al., 2008; Suárez et al.,
2010
Tea - White ND 39 to 67 12,479 to 21,436 Flavonols include quercetin, Zhao et al., 2011
leaves kaempferol, and their conjugates
Tea - Green ND 39 to 89 11,509 to 19,751 Del Rio et al., 2004; Zhao et al.,
leaves 2011
Tea - Black ND ND 10,260 Del Rio et al., 2004
leaves
Note. Assumed 20% dm to convert grape phenolic acids reported on wet basis to dry basis; assumed 13% dm for apples.
Abbreviations: ND, none detected; NC, no credible data found.
8 EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
B 2004, 2005). The sorghum leaf sheath has an even higher
A C
Flavan backbone of flavonoid structure
Flavonol aglycones: Flavan-3-ol aglycone monomers:
Quercetin; R1 = H, R2 = OH (Epi)catechin; R = OH
Myricetin; R1 = R2 = OH (Epi)afzelechin; R = H
Kaempferol; R1 = R2 = H
Flavone aglycones: Anthocyanin aglycones:
Apigenin; R1 = R2 = H Cyanidin; R1 = H, R2 = OH
Luteolin; R1 = OH, R2 = H Delphinidin; R1 = R2 = OH
Peonidin; R1 = OCH3, R2 = H
Malvidin; R1 = R2 = OCH3
F I G U R E 2 Basic flavonoid structure and common dietary
anthocyanins, flavones, flavonols, and flavan-3-ols
cereal grains, the flavones exist primarily as C-6 and/or C-8
glycosides of apigenin and luteolin (Dinelli et al., 2011).
Thus, the B-ring of the flavan structure (Figure 2) is still
available for interaction with gluten proteins.
Highly pigmented varieties of cereal grains (e.g., pur-
ple wheat, black rice, and blue maize) contain significant
amounts of anthocyanins (Ficco et al., 2014; Hosseinian,
Li, & Beta, 2008; Shao, Xu, Sun, Bao, & Beta, 2014).
The anthocyanins can be added to wheat-based foods for
their natural pigments or for their bioactive properties. As
with most anthocyanins, grain anthocyanins are primarily
glycosylated (Abdel-Aal el & Hucl, 2003; Casas, Duarte,
Doseff, & Grotewold, 2014; Hosseinian et al., 2008; Shao
et al., 2014). For example, purple wheat anthocyanins are
mostly cyanidin-3-glucoside (Hosseinian et al., 2008), and
black rice anthocyanins are primarily cyanidin- and peonidin-
3-glucosides (Shao et al., 2014). Common in maize, acylation
increases the anthocyanin glycosides pigment stability
through intermolecular copigmentation (Dangles, Saito, &
Brouillard, 1993). The acylated anthocyanins in blue and
red–blue maize are mainly cyanidin-3-(6″ -malonylglucoside)
(Collison, Yang, Dykes, Murray, & Awika, 2015).
Unique among food crops, the major pigments in sorghum
are 3-deoxyanthocyanins. The bran of some red, brown,
and black sorghum varieties contains 2.8 to 9.8 mg 3-
deoxyanthocyanins/g dm (Awika, Rooney, & Waniska,
concentrations of these pigments: 15.1 to 64.8 mg/g dm
(Geera, Ojwang, & Awika, 2012; Kayodé et al., 2011).
Because this special class of anthocyanins lacks substitution
at the C-3 position (Figure 2), 3-deoxyanthocyanins are more
stable over a wider pH range and at higher temperatures than
anthocyanins (Awika et al., 2004; Ojwang & Awika, 2008).
Thus, 3-deoxyanthocyanins could provide natural hues at
relatively higher pH, and can better withstand various food
processing conditions.
In fact, there is some evidence that 3-deoxyanthocyanidins
are stable in a baked product. Within a tortilla dough
matrix, Dunn et al. (2015) found that total extractable
phenol content was not reduced from dry mix to fully
hydrated dough substituted with 15% to 25% black sorghum
bran (rich in 3-deoxyanthocyanins), suggesting that the
3-deoxyanthocyanins did not significantly interact with
the dough components (e.g., gluten). Further, when the
extractable phenolics were analyzed by HPLC, the phenolic
profile did not change from the initial ingredients to the
final baked tortilla (Dunn et al., 2015). This is evidence that
thermal degradation or interaction with dough components,
such as gluten, did not occur (Dunn et al., 2015). Thus,
3-deoxyanthocyanins added to wheat-based foods will have
the typical phenolic antioxidant effect on gluten, but they do
not appear to complex with gluten and are stable to baking
conditions.
In cereal grains, the polyphenols are concentrated in the
outer layers, including the pericarp and the aleurone (Ndolo
& Beta, 2014). These phenolic-rich layers are largely absent
in refined grain products, including wheat flour. During the
milling process, most of the aleurone layer is removed with
the pericarp. Refined wheat flour typically has less than 25%
of the polyphenols found in whole wheat flour (Beta et al.
2005). Thus, although refined wheat flours have significantly
improved functional properties during processing compared
to whole grain flours, they offer fewer health benefits asso-
ciated with phenolic compounds. Besides using whole wheat
flour, specialty whole grain flours rich in polyphenols, such
as sorghum, various millets, and dark rye, can be used in
combination with wheat flour to produce baked products
with enhanced polyphenol content.
3.2 Monomeric polyphenols in pulse grains
and other highlighted dietary sources
3.2.1 Phenolic acids in pulses and highlighted
dietary sources
Pulse grains, starchy legumes harvested principally for
their dry seeds, have diverse phenolic compounds located
primarily (up to 95%) in their seed coat (Ranilla, Genovese,
& Lajolo, 2007; Segev et al., 2010). As dicots, pulse grains
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
have a different cell wall structure than cereal grains (mono-
cots); although polyphenols (mostly ferulic acid) cross-link
hemicelluloses in the cereal grain cell walls, these structural
cross-links are not prevalent in pulse grains (Jarvis, Forsyth,
& Duncan, 1988; Vogel, 2008). Thus, pulse grains have a
high proportion of free relative to bound phenolic acids (10%
to 20% bound; Table 1) and therefore a higher proportion
of bioaccessible phenolics than cereals (Awika, Rose, et al.,
2018). Pulses are relevant to wheat-based foods because they
can be incorporated as a source of protein or complementary
amino acids to cereal grains, as a fiber source, or to increase
bioaccessible phenolic content and phenolic diversity.
Like cereal and pulse grains, phenolic compounds in fruit
and vegetables are mainly concentrated in the skin/peel and
seed coats (Khanal, Howard, & Prior, 2009; Łata, Tram-
pczynska, & Paczesna, 2009). Similar to pulses, the phenolic
components in fruits and vegetables are mostly present in
extractable (nonbound) form (Chu, Sun, Wu, & Liu, 2002;
Sun, Chu, Wu, & Liu, 2002). Fruits and vegetables are added
to wheat-based foods mostly as inclusions (e.g., dried slices,
flakes, and pellets).
3.2.2 Monomeric flavonoids in pulses and
highlighted dietary sources
Pulses, and some fruits and vegetables, are abundant sources
of dietary flavonols (Table 2) (Ojwang, Dykes, & Awika,
2012; Patil, Pike, & Yoo, 1995; Vrhovsek, Rigo, Tonon, &
Mattivi, 2004; Zhang et al., 2015). Flavonols have a similar
structure to flavones, but with a hydroxyl substitution at C-3
(Figure 2). Cowpea varieties were found to range widely in
flavonol content from as low as 270 μg/g in green and white
phenotypes up to 1,060 μg/g in red phenotypes (Ojwang
et al., 2012). Cowpea flavonols are predominantly quercetin
glycosides, with myricetin and kaempferol glycosides present
in some varieties (Ojwang et al., 2012). Common beans
(cranberry, black, pinto, among others) and lentils (brown,
grey, tan, and green) also have glycosides of the same
flavonols (Chen et al., 2015; Mirali, Purves, & Vandenberg,
2017; Xu & Chang, 2009). Onions are also high in quercetin,
with their glycosides accounting for 54 to 286 μg/g fresh
onion weight (Patil et al., 1995) or up to 26 mg/g dry weight
(Albishi, John, Al-Khalifa, & Shahidi, 2013).
Pigmented pulses, fruits, and vegetables contain var-
ious anthocyanins (da Silva, Escribano-Bailón, Alonso,
Rivas-Gonzalo, & Santos-Buelga, 2007; Lin, Harnly, Pastor-
Corrales, & Luthria, 2008; Mané et al., 2007; Ojwang et al.,
2012; You et al., 2011). For example, black beans (Phaseolus
vulgaris) and black and green cowpea (Vigna unguiculata)
have 875 to 4,000 μg anthocyanin glycosides/g dry weight
(dw) (Lin et al., 2008; Ojwang et al., 2012; Xu & Chang,
2009). Strawberries contain 200 to 600 μg anthocyanin/g
fresh weight, with 77% to 90% of that being pelargonidin
9
3-glucoside (da Silva et al., 2007). Likewise, blueberries are
significant sources of anthocyanins, primarily C-3 glycosides
of delphinidin, cyanindin, and malvidin (You et al., 2011).
Flavan-3-ols are the most abundant monomeric polyphenol
in foods such as pulses, apples, and green tea (Del Rio et al.,
2004; Ojwang, Yang, Dykes, & Awika, 2013; Vrhovsek
et al., 2004). Unlike the previously discussed flavonoids,
flavan-3-ols have two chiral centers, at C-2 and C-3, thus
form stereoisomers (Figure 2). Ojwang et al. (2013) showed
that cowpea is especially high in monomeric flavan-3-ols,
ranging from 802 to 3,228 μg/g dw. The primary form was
catechin-7-O-glucoside, which accounted for almost 90% of
the total flavan-3-ols (Ojwang et al., 2013). Catechin glyco-
sides have been found in other pulses including adzuki bean
(Amarowicz, Estrella, Hernandez, & Troszynska, 2008) and
lentils (Dueñas, Sun, Hernández, Estrella, & Spranger, 2003).
Likewise, more than 75% (82.3 mg/g dw) of green tea phe-
nolics were found to be monomeric flavan-3-ols, especially
epigallocatechin and epigallocatechin gallate (Del Rio et al.,
2004).
3.3 Polymeric polyphenols
Polymeric polyphenols (tannins) in terrestrial plants are
classified as either condensed or hydrolysable. Condensed
tannins are primarily polymerized flavan-3-ols (Figure 3).
Hydrolysable tannins are composed of phenolic acids ester-
ified to a sugar moiety, usually gallic acid or ellagic acid and
glucose (Figure 4). Condensed tannins are far more abundant
in the diet that hydrolysable tannins.
A defining characteristic of tannins is their ability to precip-
itate proteins. Within each group of tannins, there is consid-
erable structural diversity that affects their ability to interact
with proteins (Deaville, Green, Mueller-Harvey, Willoughby,
& Frazier, 2007; Harbertson, Kilmister, Kelm, & Downey,
2014; Poncet-Legrand, Gautier, Cheynier, & Imberty, 2007).
Generally, large tannin molecules with high conforma-
tional flexibility and many hydroxyl groups and hydropho-
bic regions available interact strongest with proteins (Deaville
et al., 2007; Harbertson et al., 2014; Zeller et al., 2015).
Condensed tannins are found in fruits such as grape and
apple, in teas, and in appreciable amounts in select cereal and
pulse grain genotypes (Table 3). For example, grapes have
2,200 to 4,900 μg/g dm condensed tannins, which are a mix of
procyanidins and prodelphinidins (Figure 3) (Gu et al., 2004;
Hellström, Torronen, & Mattila, 2009). These compounds are
known for causing the astringent oral sensation experienced
when consuming dry red wine due to their interactions with
salivary proteins. Dietary hydrolysable tannins are found in
nuts and fruits such as almonds (628 to 1,000 μg/g dm) and
raspberries (827 to 1,637 μg/g dm) (Gasperotti, Masuero,
Vrhovsek, Guella, & Mattivi, 2010; Xie, Roto, & Bolling,
2012).
10 EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…

TABLE 3 Tannins in wheat and common wheat-based product additives

Source Tannins(μg/g dm) Comments
Condensed
tannins
Cereal grains
Wheat Unknown Detected but not reliably quantified Mccallum & Walker, 1990
Rye ND None detected to our knowledge
Barley 777 to 843 All DP < 6, procyanidins Gu et al., 2004
Finger millet 267 to 900 Mostly monomers and dimers of B-type Chandrasekara and Shahidi, 2011; Xiang
procyanidins et al., 2019
Rice bran 8,380 to 36,150 Red and purple rice; 45% to 50% DP > 10 Chen et al., 2016
Sorghum - 0 to 21,900 Mostly highly polymeric (DP > 10), Awika, Dykes, Gu, Rooney, and Prior,
Whole grain procyanidins; Only in type II and III 2003; Girard et al., 2018; Gu et al.,
sorghum genotypes 2004
Sorghum - Bran 0 to 58,400 Awika et al., 2003; Girard et al., 2018; Gu
et al., 2004
Pulse grains
Cowpea 0 to 6300 High proportion of monomeric Gu et al., 2004; Ojwang et al., 2013
glucosides; no DP > 10 detected;
Absent in white varieties
Lentils 529 to 675 Almost exclusively DP 1 to 3 Amarowicz et al., 2009; Amarowicz et al.,
2010
Dry beans 180 to 6,500 Propelargonidins, procyanidins; Absent in Bittner, Rzeppa, and Humpf, 2013; Gu
(kidney) white varieties et al., 2004
Other dietary
sources
Grape - Whole 2,200 to 4,900 mDP >15; Mix of procyanidin, Gu et al., 2004; Hellström et al., 2009
fruit prodelphinidin, and 3-O-gallates
Grape - Seed 34,000 to 37,000 mDP < 10; proanthocyanidins Gu et al., 2004
Grape - Pomace 215,000 to 550,000 (Tannin quantified w/5% HCl–BuOH) Ky and Teissedre, 2015; Rondeau,
Gambier, Jolibert, and Brosse, 2013
Apple 3,300 to 12,800 Mostly oligomeric (DP 4 to 10), Gu et al., 2004; Hellström et al., 2009
procyanidins
Tea - White 187,279 to 223,935 All DP < 3 Zhao et al., 2011
leaves
Tea - Green 82,296 to 269,471 All DP < 3 Del Rio et al., 2004; Zhao et al., 2011
leaves
Tea - Black 1,815 to 1,820 All DP < 3 Del Rio et al., 2004
leaves
Cocoa powder 1,483 to 1,610 All procyanidin Hellström et al., 2009
Cranberries 26,836 to 38,602 Contains A-type and procyanidins; mostly Gu et al., 2004
DP > 10
Black plums 19,405 to 19,917 Contains A-type and procyanidins; mostly Gu et al., 2004
DP > 10
Peanuts 136 to 206 Contains A-type and procyanidins; mostly Gu et al., 2004; Hellström et al., 2009
DP < 7
Hydrolysable
tannins
Almonds 628 to 1,000 Ellagitannins and gallotannins Xie et al., 2012
Blackberries 847 to 1,305 Ellagitannins (majority lambertianin) Gasperotti et al., 2010
Raspberries 827 to 1,637 Ellagitannins (majority lambertianin) Gasperotti et al., 2010
(Continues)
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION… 11

TABLE 3 (Continued)
Source Tannins(μg/g dm) Comments
Mango - Peel 1,400 Gallotannins Berardini et al., 2004
Mango - Pulp 200 Berardini et al., 2004
Mango - Kernel 15,500 Berardini et al., 2004
Abbreviation: ND, none detected.

3.3.1 Condensed tannins cyanidin) and tri-hydroxy (prodelphinidin) most prominent

Condensed tannins can have a variety of structures (Figure 3).
B-type condensed tannins are linked via C4–C8 or C6–C8
interflavan bonds. In addition to the B-type linkages, A-type
condensed tannins have a 2𝛽 → O → 7 bond. This bond
may somewhat limit tannin flexibility, but it was not shown
to affect protein aggregation (Ropiak, Lachmann, Ramsay,
Green, & Mueller-Harvey, 2017). Tannin MW was the
primary factor affecting tannin–protein interactions (Ropiak
et al., 2017). The B-ring of condensed tannins can have
mono-, di-, or tri-hydroxy groups, with di-hydroxy (pro-
in dietary sources. Each subunit can differ in stereochemistry,
too. For example, procyanidin monomers are catechin (trans)
or epicatechin (cis). Tannins can also be galloylated at the
C-3 position.
The condensed tannin structure difference most relevant to
tannin–protein interactions is degree of polymerization (DP)
(Hagerman, 1989). Higher MW tannins offer more hydropho-
bic regions for stronger hydrophobic interactions with pro-
teins (Baxter, Lilley, Haslam, & Williamson, 1997). Also,
increasing polymer chain length subsequently increases ortho

F I G U R E 3 Possible interflavan bonds in dietary condensed tannins (proanthocyanidins) and select subunit types
12
Gallotannin
(Pentagalloylglucose)
Ellagitannin
(Lambertianin)
F I G U R E 4 Dietary hydrolysable tannin structure examples
mono-, di-, or tri-hydroxy groups with each subunit, thus
offering more chances for hydrogen bonding with proteins
(Harbertson et al., 2014). For example, when purified cocoa
condensed procyanidins ranging from DP 1 to 8 were individ-
ually precipitated with bovine serum albumin (BSA), there
was a clear positive relationship between tannin DP and pre-
cipitation rate (Harbertson et al., 2014). About 12% of trimers
precipitated, whereas over 93% of octomers precipitated with
equivalent concentrations of BSA (Harbertson et al., 2014).
Other condensed tannin structural features are far less
important to protein-binding efficiency than DP. Ropiak
et al. (2017) used turbidity and fluorescence quenching to
investigate the protein-binding efficiency of 35 condensed
tannins samples from a wide variety of sources with BSA and
gelatin. The tannin samples ranged from 3.0 to 25.5 mean DP
(mDP), 0% to 21% A-type linkages, 0% to 54% galloylation,
and solely procyanidins to nearly all prodelphinidins (Ropiak
et al., 2017). The only characteristics that strongly correlated
with protein aggregation and binding were mDP and average
MW (Ropiak et al., 2017). Thus, mDP is the most important
factor to consider when assessing how a condensed tannin
will interact with a protein.
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
Ellagitannin
(Punicalagin)
Only a few cereal grains are known to contain relevant
quantities of condensed tannins, including some genotypes
of sorghum, finger millet, barley, and rice (Chen, McClung,
& Bergman, 2016; Hahn & Rooney, 1986; Hellström et al.,
2009; Xiang, Apea-Bah, Ndolo, Katundu, & Beta, 2019).
For instance, specific sorghum genotypes contain primarily
highly polymerized (mDP >10) C4–C8 interflavan-linked
condensed tannins (proanthocyanidins; Figure 3) (Girard,
Bean, Tilley, Adrianos, & Awika, 2018). Red and purple rice
brans also contain high-MW tannins; polymeric proantho-
cyanidins (DP > 10) accounted for 45% to 50% of the total
condensed tannins in rice (Chen et al., 2016). Some finger
millets contain condensed tannins (267 to 900 μg/g dw), but
these are mostly epi-/catechin and procyanidin dimer B1 and
B2 (Chandrasekara & Shahidi, 2011; Xiang et al., 2019).
Similarly, barley and rice contain mostly low-MW tannins
(mDP < 5) (Hellström et al., 2009). Red wheat contains
condensed tannins, though these are difficult to extract in
mature kernels because they are probably bound to cell wall
components (Dinelli et al., 2011; Mccallum & Walker, 1990).
These condensed tannins likely produce the characteristic
pericarp pigmentation in red wheat (Mccallum & Walker,
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
1990; Miyamoto & Everson, 1958). However, because
they are poorly characterized, wheat condensed tannin
functionality and impact on health remain largely unknown.
Unlike in cereal grains, the condensed tannins are more
widely distributed in commonly consumed grain pulses,
including common beans (Phaseolus vulgare), cowpea
(Vigna unguiculata), and lentils (Lens culinaris) (Amarowicz
et al., 2009; Amarowicz et al., 2010; Díaz, Caldas, & Blair,
2010; Ojwang et al., 2013). However, the condensed tannins
in pulses are generally dominated by lower MW oligomers.
For example, 39% of cowpea flavan-3-ols were monomeric
(catechin and afzelechin glycosides), 47% dimers—octamers,
and 14% with a DP > 10 (Ojwang et al., 2013).
Condensed tannins are also found in fruits such as apples
and grapes, and cacao beans (Table 3). Tea is one of the more
prominent tannin sources in most diets, but it has mostly
low-MW tannins (DP < 3) (Zhao et al., 2011). Cranberries,
plums, and peanuts contain both A- and B-type condensed
tannins (Gu et al., 2004).
3.3.2 Hydrolysable tannins
Hydrolysable tannins are found in some fruits (e.g., rasp-
berries and mangoes) and nuts (e.g., almonds and pecans),
though they are most commonly found in nondietary source
such as wood (Berardini, Carle, & Schieber, 2004; Gasperotti
et al., 2010; Xie et al., 2012). Like condensed tannins,
larger MW hydrolysable tannins offer more hydrophobic
regions for interactions with proteins (Baxter et al., 1997;
Charlton et al., 2002). A greater number of galloylations also
offer more hydroxyl groups, which lead to greater protein
affinity through hydrogen bonding (Baxter et al., 1997; Toda,
Kawabata, & Kasai, 2001).
Hydrolysable tannin structure alters protein binding
affinity by affecting available binding sites. Ellagitannins
have intermolecular biphenyl linkages that result in restricted
conformational freedom as compared to gallotannins. Thus,
ellagitannins are less efficient at binding inflexible proteins
such as BSA, but their interactions with the relatively more
flexible gelatin were not impeded (Deaville et al., 2007).
Between condensed and hydrolysable tannins, condensed
have been shown to have a greater protein affinity (Baxter
et al., 1997; Girard, Teferra, & Awika, 2019; Hagerman,
Rice, & Ritchard, 1998), likely because of their more flexible
conformation. Thus, condensed tannins can alter gluten rhe-
ology at comparatively lower usage levels than hydrolysable
tannins (Girard et al., 2019). Condensed tannins are also
more prevalent in ingredients that are likely to be added to
wheat-based foods such as cereal and pulse grains, peanuts,
cocoa, and fruit pomaces. This gives a greater opportunity
for condensed tannin–gluten interactions to be leveraged for
innovative products.
13
4 I M PAC T S OF PO LY P H E NOL S O N
G LUTEN F UNCTIO NALIT Y
Both polyphenols naturally found in wheat, and those added
to wheat-based foods for a variety of reasons are likely to
impact gluten functionality. For example, whole grains and
cereal brans are used to increase dietary fiber, add visual
appeal, and improve nutritional profile of wheat-based
foods. Pulse grains can increase protein content and add
complementary amino acids to wheat products. Fruits and
some vegetables can add vibrant color (e.g., natural pigments
in brightly colored cheese crackers), diversify flavor (e.g.,
pumpkin bread), or increase fruit/vegetable consumption and
improve healthy image of product (e.g., spaghetti pasta with
zucchini and spinach included). Polyphenols are important
components of these ingredient sources. The profile of
polyphenols in these commodities affects how they interact
with gluten and impact product quality.
Effects of polyphenols on wheat-based food product qual-
ity have been the subject of various investigations. Available
studies on the effect of gluten–phenol interactions on gluten
functionality are summarized in Table 4 and discussed in the
following sections.
4.1 Effects of monomeric polyphenols on
gluten functionality
4.1.1 Effects of endogenous wheat monomeric
polyphenols on gluten functionality
Phenolic acid in wheat flour can affect gluten properties,
especially by reducing dough stability. During dough mixing,
disulfide bonds typically break and re-align (Weegels,
Hamer, & Schofield, 1997). As the proteins are stretched
and hydrated initially during mixing, the dough resistance to
extension increases up to a maximum; however, continued
mixing decreases dough elasticity. Part of this breakdown is
mechanical. Large and highly entangled gluten polymers can-
not disentwine fast enough under mixing strains and instead
break apart (MacRitchie, 1975). The formation of excess
free radicals is also a factor in dough breakdown. Highly
antioxidant phenolic compounds donate electrons to disulfide
bonds, thus breaking the bond and creating thiol residues
within the gluten protein chain (Danno & Hoseney, 1982)
(Figure 5). This results in decreased dough strength and
stability (Schroeder & Hoseney, 1978). In general, work on
the effect of endogenous phenolic acids on gluten rheology is
sparse; much of our understanding of their rheological effect
comes from addition of phenolic acids to wheat (see next
section).
As previously mentioned, in wheat, and other cereal
grains, the vast majority (≥75%) of phenolic acids are in
the bound form (Table 1). Ferulic acid, the most abundant
14 EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…

TABLE 4 Effect of polyphenols on gluten functionality

Polyphenol Effect on gluten functionality Reference
Crude polyphenol extracts
Blackcurrant polyphenol Decreased proportion of unextractable HMW proteins (Sivam et al., 2012)
extract (especially high in
anthocyanins)
Blackcurrant, apple, and Blackcurrant and apple reduced shear storage modulus (G′ ) and shear (Sivam et al., 2011)
kiwi polyphenol extracts loss modulus (G″ )
Green tea powder Via Mixolab: increased dough stability time, decreased starch pasting (Ning et al., 2017)
viscosity peak, and increased starch retrogradation;Decreased loaf
specific volume
Phenolic acids
Ferulic acid in water Caused breakdown in dough mixing (Schroeder &
soluble nonstarch Hoseney, 1978)
polysaccharides
Ferulic acid Decreased viscosity of gluten extracts from overmixed doughs versus (Danno & Hoseney,
control, indicating ferulic acid partially depolymerized gluten 1982)
Ferulic acid Demonstrated possibility of cysteine-ferulic acid adducts in overmixed (Jackson & Hoseney,
doughs 1986)
Ferulic acid Free ferulic acid decreased with overmixing wheat flour doughs,
suggesting ferulic acid was involved in dough breakdown
Ferulic acid and sinapic Conjugated and bound ferulic and sinapic acids were reduced with (Labat, Morel, &
acid overmixing of gluten, thus likely involved in gluten breakdown Rouau, 2000a)
Ferulic acid Ferulic acid, especially in combination with a oxidoreductase enzyme (Labat et al., 2000b)
(laccase), increased the rate of sulfhydryl group oxidation and
glutenin depolymerization in a dough matrix
Ferulic acid Reduced elasticity and mixing tolerance of a wheat flour dough; it also (Koh & Ng, 2009)
increased HMW gluten solubility;Free ferulic acid at 250 mg/kg
reduced dough strength and subsequent bread volume by 4%
Ferulic acid Free ferulic acid added to a bread formulation at 825 and 5,000 mg/kg (Nicks et al., 2013)
reduced final product volume by 5% and 21%, respectively
Ferulic acid (with and Bound and free ferulic acid increased dough extensibility and (Snelders et al.,
without arabinoxylan decreased resistance to extension 2014)
oligosaccharides)
Caffeic, ferulic, syringic, Caffeic and ferulic acids decreased mix time, mixing tolerance, (Han & Koh, 2011b)
and gallic acids resistance to extension, and bread volume; increased extensibility
Caffeic and ferulic acids decreased HMW proteins and increased
sodium dodecyl sulfate extractable proteins
Gallic acid Gallic acid acted as a plasticizer in gluten films (Hager et al., 2012)
Flavonoids
Anthocyanins (in Increased dough absorption and development time, decreased mixing (Sui, Zhang, &
anthocyanin-rich black stability Zhou, 2016b)
rice extract powder) Reduced dough resistance to extension and increased extensibility
Decreased bread volume and increased crumb hardness
Quercetin Reduced dough resistance to extension and increased extensibility (Lin & Zhou, 2018)
Increased crumb hardness and reduced bread volume
Quercetin Increased steam bread volume, produced harder crumb texture, and (Lin et al., 2018)
gave yellow-green tint to crumb
Quercetin (in onion skin) Reduced protein digestibility by complexing with proteins (Świeca,
Especially complexed with smaller proteins—size-exclusion Gawlik-Dziki,
chromatography showed complex between 14.5 to 25 kDa Dziki, Baraniak,
& Czyż, 2013)
Catechin (from green tea) Catechins were not stable in bread-making process, likely because (Wang & Zhou,
they interacted with gluten and acted as reducing agents 2004)
(Continues)
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION… 15

TABLE 4 (Continued)
Polyphenol Effect on gluten functionality Reference
Tannins
Condensed tannins (in Condensed tannins increased insoluble polymeric proteins (Dunn et al., 2015)
sorghum bran) (cross-linked gluten)
Condensed tannins (from Some grape seed tannins bound partially digested gliadin (Dias et al., 2015)
grape seed) fractions—larger MW tannins bound more protein and larger
protein bound more tannins
Condensed tannins (from Tannins bound specific gliadin fractions—mainly the ones with the (Dias,
grape seed) highest proline content Perez-Gregorio,
Mateus, & De
Freitas, 2016)
Condensed tannins Tannins increased gluten elasticity, without decreasing extensibility (Girard et al., 2016)
(extracted from sorghum Larger MW tannins greater strengthening effect (sorghum > grape
and grape seed) seed)
Condensed tannins Larger MW tannins had greater binding affinity for gluten proteins (Girard et al., 2018)
(extracted from sorghum (sorghum > grape seed)
and grape seed) At room temperature, tannins interacted with largest gluten protein
fraction available, e.g., glutenin > gliadin, HMW-GS > LMW-GS
Condensed tannins (from Oligomeric condensed tannins decreased gluten-free –SH and surface (Liu et al., 2018)
grape seed) hydrophobicity
Changed protein structure: increased alpha-helix and beta-turns,
decreased beta-sheets
Condensed tannins (from Large MW condensed tannins increased gluten film strength and (Girard et al., 2019)
sorghum) and tannic acid wheat flour batter viscosity more so than tannic acid
Condensed tannins predominantly complexed gliadins between 60
to 80 ◦ C, indicating tannins likely interacting with gliadins as they
denature and expose hydrophobic amino acid residues
Tannic acid Cross-linked gluten, thus stiffened gluten film and increased strength (Hager et al., 2012)
Tannic acid Increased dough strength, though it broke S–S bonds (Wang et al., 2015;
Zhang et al.,
2010)
Tannic acid Increased mix time, gluten particle size, created more compact gluten (Wang et al., 2015)
structure, decreased surface hydrophobicity, and increased
alpha-helix + beta turns but decreased beta sheets
Tannic acid Gliadins in solution turned hazy with addition of tannic acid indicating (Siebert et al., 1996)
tannic acid–gliadin interactions

arabinoxylans. The presence of free radicals promotes these

F I G U R E 5 Schematic of redox reaction between cysteine
residues in gluten proteins and oxidizing or reducing agents
phenolic acid (Challacombe, Abdel-Aal, Seetharaman, &
Duizer, 2012), is mostly esterified to arabinose side chains of
ferulic acid moieties to cross-link with each other (Izydor-
czyk, Biliaderis, & Bushuk, 1990) or the amino acid tyrosine
(Piber & Koehler, 2005), in what is called oxidative gelation.
This is an especially important effect in soft wheat products
such as cakes, where the viscosity and stability of the batter
have a large impact on the product quality. For example, the
oxidative gelation of both arabinoxylans and proteins in soft
wheat flour reduced cookie spread during baking (Bettge &
Morris, 2007). Conversely, gluten strength is the predominant
factor in quality of hard wheat products. Overall, oxidative
gelation between ferulic acid and tyrosine likely plays a very
minor role in enhancing gluten strength because only 0.5%
of the ferulate and less than 0.02% of the tyrosine present in
flour were found to cross-link (Piber & Koehler, 2005).
16
Like phenolic acids, monomeric flavonoids are strong
antioxidants that will decrease gluten strength by breaking
disulfide bonds. Flavones are the primary wheat flavonoids;
the C-2 and C-3 double bond and oxygen attached to C-4 via
double bond (e.g., apigenin; see Figure 2) make flavones espe-
cially potent antioxidants (Rice-Evans, Miller, & Paganga,
1996). We were unable to find any studies that specifically
looked at the effect of endogenous wheat flavonoids (except
for anthocyanins in specialty wheat varieties; see Section
4.1.2.2) on gluten strength or dough rheology. But even
whole grain wheat contains a relatively minor amount of
flavones (less than 400 μg/g dm) (Hernandez et al., 2011),
and most of this is removed with the bran portion during
milling. So, refined flour is not likely to be greatly affected
by endogenous flavonoids. However, this is likely one of the
components of bran that contribute to its detrimental effect
on gluten structure in whole grain applications (Khalid et al.,
2017). To what extent endogenous flavones affect gluten
rheology has yet to be explored.
4.1.2 Effects of supplemental monomeric
polyphenols on gluten functionality
Effects of supplemental phenolic acids on gluten functionality
Whether they come from cereal bran, nonwheat whole grains,
or fruit purees or pieces, extractable phenolic acids added
to wheat-based products generally degrade gluten strength.
However, the structure and quantity of the phenolic acids
determine how significantly they affect gluten rheology. In
general, the carboxylate group of hydroxycinnamic acids
increases their antioxidant capacity relative to hydroxy-
benzoic acids because the electrons of the structure are
delocalized from the aromatic nuclei (Rice-Evans et al.,
1996). So, hydroxycinnamic acids have greater reducing
power in redox reactions.
As a clear example of the reducing strength of hydrox-
ycinnamic versus hydroxybenzoic acids, Han and Koh
(2011b) tested purified caffeic, ferulic, gallic, and syringic
acids added to wheat flour dough at 4.44 μmol/L/g flour for
their effects on gluten macropolymer structure and dough
rheology. The hydroxycinnamic acids (caffeic and ferulic
acids) increased sodium dodecyl sulfate extractability of
gluten implying a reduction in macropolymer size, whereas
lower antioxidant activity of hydroxybenzoic acids (gallic
and syringic acids) did not (Han & Koh, 2011b). The authors
suggest this is because the hydroxycinnamic acids reduced
protein intermolecular cross-links, thus making them more
soluble. Although all the added phenolic acids decreased
dough mixing strength (mix time and mix tolerance) and ten-
sile strength (decreased resistance to extension and increased
extensibility), the hydroxycinnamic acids had a far greater
effect (Han & Koh, 2011b). In fact, of the phenolic acids,
caffeic acid decreased gluten strength the most (Han & Koh,
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
2011b). The authors attributed this effect to its antioxidant
potential because caffeic acid has an extra –OH group as
compared to ferulic acid. Only the hydroxycinnamic acids
significantly reduced bread loaf volume (Han & Koh, 2011b).
The evidence demonstrates that structure plays a large role
in the ability of phenolic acids to affect gluten rheology,
consequently wheat-based product quality.
Although phenolic acid’s structures affect their antioxidant
potential, both extractable and bound phenolic acids can
reduce protein cross-links, thus weaken gluten. Snelders et al.
(2014) assessed the effects of free ferulic acid and arabinoxy-
lans with free or bound ferulic acid on gluten extractability
and dough rheology. The motivation was to improve fiber
content of products using arabinoxylans and assessing the
relative effect of arabinoxylans versus ferulic acid on gluten
rheology. Free ferulic acid (2 to 18 g/kg flour) was shown to
reduce dough resistance to extension and increase extensibil-
ity in a dose-dependent manner (Snelders et al., 2014). The
arabinoxylans with bound or free ferulic acid at equivalent
levels similarly affected the dough rheology (Snelders et al.,
2014). In fact, the extractability of high-MW gluten proteins
(i.e., those most dependent upon disulfide linkages) in sodium
dodecyl sulfate increased by 22% with free ferulic acid (18
g/kg flour) and by 32% with approximately equivalent levels
of arabinoxylan-bound ferulic acid (Snelders et al., 2014).
This is the evidence of depolymerization of proteins via the
ferulic acid antioxidant effect, regardless of extractability
status of the phenolic acid. Therefore, total phenolic acid
content of an ingredient should be considered for its impact
on gluten functionality, not just extractable phenolic acids.
Although the phenolic acid antioxidant effect on glutens
can lead to dough that is sticky and weak, the volume and
texture of products resulting from this dough do not neces-
sarily suffer (Han & Koh, 2011b; Snelders et al., 2014). For
example, free ferulic acid added to a bread formulation at 825
mg/kg reduced final product volume a modest 5%, though it
did increase dough softening, a measure of gluten breakdown
(Nicks et al., 2013). However, at 5,000 mg/kg, bread volume
was reduced by 21% (Nicks et al., 2013). Similarly, Koh and
Ng (2009) found that 250 mg/kg free ferulic acid reduced
dough strength and subsequent bread volume by 4%.
Though the effect of phenolic acids on gluten has been
studied for over a century, the exact mechanism is still not
fully elucidated. We know that phenolic acids can reduce
dough mixing strength, increase dough breakdown, create
sticky doughs, and reduce macropolymer size (Han & Koh,
2011b; Snelders et al., 2014). Some of this could be through
phenolic acids interacting with thiyl radicals resulting from
disulfide scission during mixing (MacRitchie, 1975), for
example, forming adducts between cysteine and phenolic
acids (Jackson & Hoseney, 1986; Sidhu, Nordin, & Hoseney,
1980). This prohibits disulfide bond reformation, and thus
limits gluten macropolymer size (Koh & Ng, 2009). Loss
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
of sulfhydryls or phenolic acids during mixing suggests that
phenolic acid–protein interactions occur (Han & Koh, 2011a).
Phenolic acids could also dimerize after reactions with
thiyl radicals, though dimeric forms have only been found
to increase with mixing in oxidative environments (Labat,
Morel, & Rouau, 2000b). Oxidants, which occur naturally
within and are added to flour (e.g., glucose oxidase), catalyze
the phenolic acid reduction of disulfide bonds. Further, the
phenolic acids might alter other protein interactions. For
example, hydrogen bonding can occur between phenolic
acid hydroxyl groups and protein carbonyls, or hydrophobic
interactions can form between phenolic acid aromatic rings
and hydrophobic amino acid residues (Snelders et al., 2014).
Either of these would interrupt noncovalent interactions that
stabilize the gluten structure. The most likely mechanistic
explanation for phenolic acid effects on gluten is a combi-
nation thereof: minor deviations in disulfide cross-links and
noncovalent interactions can cause large changes in gluten
rheology (Belton et al., 1995; Han & Koh, 2011b).
Effects of supplemental monomeric flavonoids on gluten
functionality
Monomeric flavonoids have been tested as additives to
doughs and breads, primarily as bioactive additives, for
example, onion skins rich in quercetin (Gawlik-Dziki et al.,
2013; Swieca, Gawlik-Dziki, Dziki, Baraniak, & Czyz, 2013)
and green tea catechins (Wang & Zhou, 2004). Generally,
this is to leverage the health benefits associated with phenolic
compounds such as cardioprotective and anti-inflammatory
effects. Flavonoids vary in structure and antioxidant activity,
but broadly, those with greater degree of hydroxylation on
the B and C rings or a double bond between C-2 and C-3
have higher antioxidant capacity (Balasundram, Sundram, &
Samman, 2006; Rice-Evans et al., 1996). Thus, flavonoids
are likely to reduce gluten strength by reducing disulfide
bonds, which may reduce final product quality.
Flavan-3-ols were reported to weaken gluten. Catechin
(94% pure extract, 0.8 to 2.5 mg/g flour) decreased mixing
strength and dough resistance to extension, while increasing
extensibility (Girard et al., 2016). For example, 2.5 mg cat-
echin/g flour decreased force to extend a weak gluten dough
by 29% and increased extensibility 1.5× (Girard et al., 2016).
This was likely due to the antioxidant effect of catechin,
which reduces disulfide cross-links. In support of this, green
tea powder (12.9% catechins) added to bread formulation at
10 to 40 mg/g flour produced a dose-dependent decrease in
bread volume, and increase on bread hardness (Ning, Hou,
Sun, Wan, & Dubat, 2017).
Likewise, flavonols have also been shown to reduce gluten
strength. Quercetin (98% pure extract, 0.5 to 2.0 mg/g flour)
reduced resistance to extension and increased extensibility of
a wheat flour dough (Lin & Zhou, 2018). At 1.0 mg/g flour,
quercetin reduced dough extensibility by 18% compared to
17
a control with no quercetin. Furthermore, quercetin added to
baked and steamed bread formulations at 0.5 to 2.0 and 12
to 36 mg/g flour, respectively, resulted in final products with
reduced volume and harder texture in a dose-dependent man-
ner (Lin, Gwyneth Tan, Leong, & Zhou, 2018; Lin & Zhou,
2018). Baked bread with 2.0 mg quercetin/g flour had a vol-
ume reduction of 10% compared to the control, whereas the
hardness increased by 24% and the chewiness by 23% (Lin &
Zhou, 2018). Similarly, steamed bread with 36 mg quercetin/g
flour exhibited reduced volume (12%) and increased hardness
(33%) and chewiness (21%) (Lin et al., 2018). The authors
found that steamed bread with lower addition of quercetin (0.5
to 8.0 mg/g flour) did not significantly differ in final volume
or texture from the control. This suggests that low usage levels
may not detrimentally affect product quality, likely because
there is a threshold of how much antioxidant is needed to
reduce disulfide cross-links to an extent that they impact
properties such as volume and texture. But these dosages will
vary by phenol based on their antioxidant potential.
Another class of monomeric flavonoids that are attractive
as food additives is anthocyanins because they are functional
as natural colorants. Pigmented varieties of grains often
contain significant amounts of anthocyanins (Table 2), and
these commodities (e.g., purple wheat, black rice, blue
maize, etc.) or their components (bran and extracts) can
be used to add color and health attributes to wheat-based
foods. Sorghum contains a special class of anthocyanins,
3-deoxyanthocyanins, which have better color stability than
typical anthocyanins. Fruits with red to blue colors (e.g.,
cherries, berries, and grapes) are also rich in anthocyanins
and are commonly used as sources of these compounds.
Like other monomeric flavonoids, anthocyanins are
strong antioxidants (Rice-Evans et al., 1996) and thus are
detrimental to gluten strength. For example, anthocyanin-rich
black rice extract powder (approximately 20% anthocyanins)
added to bread formulations (10 to 40 mg/g flour) reduced
dough tensile strength and resultant bread volume, plus
increased bread crumb hardness (Sui et al., 2016a). Similarly,
blackcurrant polyphenol extract, which is approximately 27%
polyphenols and especially high in anthocyanins, decreased
gluten macropolymer size (Sivam et al., 2012) and therefore
gluten strength. Though neither study directly tested free
sulfhydryl groups, the anthocyanins likely reduced disulfide
cross-links and increased free sulfhydryl groups.
In summary, monomeric polyphenols largely reduce gluten
polymer size and strength, which could be leveraged as
natural reducing agents to improve extensibility in products
such as hot-pressed flatbreads (e.g., tortillas). In hot-pressed
tortillas, excess elasticity will cause the dough to shrink
after being pressed, resulting in undesirably small diameters.
Reducing agents are also commonly used to reduce mix time,
improve dough handling, and soften final product texture.
Monomeric polyphenols are natural, plant-based ingredients
18
that could replace currently used reducing agents such as
bisulfites and L-cysteine.
Conversely, monomeric polyphenols reduce quality of
products that rely on gluten strength such as pan breads and
bagels. However, potential health benefits of polyphenols
could greatly benefit a large majority of humans. Cardiovas-
cular disease is the most common cause of death worldwide
(Global Burden of Disease Study 2013 Mortality and Causes
of Death Collaborators, 2015), and chronic inflammation
is a factor in a host of maladies including cardiovascular
disease (Franceschi & Campisi, 2014; Pawelec, Goldeck, &
Derhovanessian, 2014). To use polyphenols in wheat-based
foods and maintain desired product quality, their negative
impact on gluten must be mitigated. For instance, monomeric
polyphenols could be used with extra-strong gluten where
a reducing agent would serve to mellow the gluten and
allow for easier handling. Polyphenols could also be used
in products where gluten strength is not integral to product
quality, such as cookies and cakes.
4.2 Effects of polymeric polyphenols on
gluten functionality
Broadly, condensed and hydrolysable tannins are known to
strongly interact with proteins; tannins have been used for
ages to “tan” hides. Tannins complex with collagen primarily
through hydrogen bonding and hydrophobic interactions,
thus increasing the proteins’ hydrothermal stability and
reducing shrinkage (melting). These protein–tannin interac-
tions convert inflexible hides into supple leather (Covington,
1997). There have been extensive studies on tannins (both
hydrolysable and condensed) and their interaction with
proteins (Deaville et al., 2007; Hagerman et al., 1998;
Poncet-Legrand et al., 2007).
Tannins and proteins interact via two main mechanisms:
(a) extensive hydrogen bonding between hydroxyl groups of
tannins and amide groups of proteins due to the abundance of
hydroxyl groups in close proximity on the tannin molecule,
and (b) hydrophobic interactions between tannin aromatic
rings with hydrophobic regions and hydrophobic amino acid
residues (Hagerman, 2012). By contrast, monomeric polyphe-
nols have few hydroxyl groups and lack large hydrophobic
domains, and thus have a limited ability to cross-link protein
polymers. Generally, both protein and tannin size and struc-
ture play a role in their binding affinity. Tannins that have
larger structure, more conformation flexibility, and greater
numbers of hydroxyl groups interact more strongly with
proteins (Hagerman et al., 1998; Harbertson et al., 2014).
Proteins with larger, more open structure conformation, and
those that are proline rich, have a greater tendency to interact
with tannins (Hagerman & Butler, 1980a, 1980b). Gluten pro-
teins have approximately 14 mol% proline (Ewart, 1967) and
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
generally open structure (Belton, 1999), thus can extensively
interact with tannins (Girard et al., 2018; Zhang et al., 2010).
4.2.1 Effects of endogenous wheat polymeric
polyphenols on gluten functionality
Although red wheat varieties contain condensed tannins
(Mccallum & Walker, 1990; Miyamoto & Everson, 1958),
these are difficult to extract and have not been well char-
acterized. Thus, literature on the effect of endogenous
tannins on gluten is unavailable. Nevertheless, it is likely that
endogenous wheat tannins do not greatly interact with gluten
in refined wheat flour, as they are bound to cell wall material
in the bran (Mccallum & Walker, 1990). Because they are
tightly bound to cell wall components thus their binding sites
are not available to interact with proteins, these condensed
tannins are also unlikely to affect gluten rheology in whole
wheat applications beyond the antioxidant effect discussed
in Section 4.1. Further, the tannin concentration in wheat is
very low (Mccallum & Walker, 1990) and overshadowed by
monomeric phenolics (Khalid et al., 2017; Li et al., 2008).
4.2.2 Effects of supplemental polymeric
polyphenols on gluten functionality
Mechanisms of tannin–gluten interactions
The relatively young, but growing, body of work on tannin–
gluten interactions shows that condensed and hydrolysable
tannins interact strongly with gluten proteins (Dunn et al.,
2015; Girard et al., 2016; Siebert, Troukhanova, & Lynn,
1996; Zhang et al., 2010). Although they are powerful
antioxidants and break disulfide bonds (Wang et al., 2015),
the tannins actually increase gluten strength through non-
covalent protein cross-linking (Dunn et al., 2015; Girard
et al., 2016). In support of this, size exclusion HPLC showed
that the MW distribution of gluten proteins solubilized
with sodium dodecyl sulfate was shifted to greater MW
with tannic acid addition (Wang et al., 2015). Hydrogen
bonding and hydrophobic interactions are both a part of
tannin–gluten interactions (Girard et al., 2018; Wang et al.,
2015). However, the cooperative effects of these interactions
(i.e., which noncovalent interaction predominates) and how
effectively tannin and gluten interact differ based on tannin
type (condensed vs. hydrolysable), tannin MW, and gluten
conformation (Girard et al., 2018; Girard et al., 2019; Hager,
Vallons, & Arendt, 2012; Wang et al., 2015).
Effects of condensed versus hydrolysable tannins on tannin–
gluten interactions. Condensed tannins have been shown to
have a greater binding affinity than hydrolysable tannins for
proteins (Hagerman et al., 1998), including gluten (Girard
et al., 2019). Hagerman et al. (1998) found that to precipitate
1 mole of BSA protein, 40 moles of pentagalloylglucose
were required versus only 20 moles of epicatechin16 (4→8)
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
catechin. Although the elongated, flexible structure of highly
polymerized condensed tannins offers many opportunities
for noncovalent interactions with proteins, the comparatively
dense, globular conformation of hydrolysable tannins seems
to limit interactions (Girard et al., 2019; Hagerman et al.,
1998).
Because of their differences in binding affinity, condensed
tannins are more effective at increasing gluten polymer
strength than hydrolysable tannins. For example, at equiva-
lent usage levels (10 mg tannin/g gluten), sorghum-condensed
tannins significantly increased gluten film tensile strength
by 2.3×, whereas tannic acid did not increase film strength
(Girard et al., 2019). Work from another lab showed that a
similar improvement in gluten film tensile strength (2.0×)
was achieved when tannic acid was used at a 10× higher
concentration (Hager et al., 2012). In both cases, the results
imply that tannins cross-linked gluten proteins and strength-
ened the gluten matrix, thus increasing film tensile strength
compared to the control. However, because of the more linear
structure of condensed tannins, it is far more efficient at
cross-linking gluten proteins than hydrolysable tannins.
The higher protein-binding affinity of condensed tannins
also leads to increased viscosity of wheat flour batter matrices
versus hydrolysable tannins. For instance, when a slurry
(3 g wheat flour, 8.5% protein; 25 g water) was heated to
95 ◦ C and starch pasting peak viscosity recorded with a
Rapid Viscoanlyzer (RVA), condensed and hydrolysable
tannins (25 mg/g flour) increased the peak viscosity by 53%
and 19%, respectively, compared to the control (Girard et al.,
2019). It is likely that tannin–gluten interactions increased
viscosity, because subsequent RVA tests with wheat starch
and tannin showed no change in peak viscosity (Girard et al.,
2019). Similarly, condensed tannins did not increase the peak
pasting viscosity of normal corn starch (Amoako & Awika,
2016), though tannins are known to noncovalently interact
with starch, especially amylose (Amoako & Awika, 2016,
2019; Barros, Awika, & Rooney, 2014). Three-way inter-
actions among tannins, proteins, and polysaccharides have
also been shown to form ternary complexes among salivary
proteins, condensed tannins, and pectins (Soares, Mateus,
& de Freitas, 2012). Due to the magnitude of the increase
in peak viscosity found with wheat flour and condensed
tannins, of which tannin–gluten interactions seem unlikely
to be the sole driver (Girard et al., 2019), it is possible that
tannin–gluten–starch interactions could be occurring, too,
and increasing viscosity. Beyond significantly increasing
system viscosity, tannin–gluten–starch complexes could alter
starch retrogradation (thus staling rate) and macronutrient
digestibility. But, this is largely unexplored.
The tannin–gluten interaction mechanisms appear to be
different at higher temperatures. For example, in the same
RVA tests (Girard et al., 2019), the viscosity of the 25 mg
condensed tannin per gram of wheat flour solution nearly
19
doubled starting at 60 ◦ C and peaking at 72 ◦ C. Further, no
change in viscosity was seen between these temperatures
when condensed tannins were tested on pure wheat starch
(Girard et al., 2019). However, when isolated glutenins and
gliadins were added to wheat starch (10% protein, 90%
starch), a 2.8× viscosity increase at 60 to 72 ◦ C with the
condensed tannin treatment was seen with the gliadin but not
glutenin fraction (Girard et al., 2019). This suggests that the
gliadins cross-link with condensed tannins as the solution
heats, leading to larger polymers that increase the system
viscosity. Likely, as the gliadin proteins denature, they expose
hydrophobic amino acid residues that interact with tannins.
Hydrolysable tannins had no effect on solution viscosity
between 50 and 90 ◦ C (Girard et al., 2019). The implication
is that condensed tannins, but not hydrolysable tannins, are
able to interact with the exposed hydrophobic residues of
gliadins during heating of a batter. In fact, for hydrolysable
tannins to complex with heated gliadin, it must be used in
very high levels. For example, 200 and 500 mg tannic acid
per gram of gliadin increased haze formation in a phosphate
buffer (pH 4.2) with solubilized gliadin by 0.5 to 3.0× when
heated to 100 ◦ C (Siebert et al., 1996). This indicates that
hydrolysable tannins can also interact with gliadin through
hydrophobic interactions, though they are far less efficient
than condensed tannins.
Effects of condensed tannin MW on tannin–gluten interac-
tions. Within condensed tannins, the larger MW tannins
have a greater binding affinity for gluten (Girard et al., 2018).
For example, solubilized glutenins were precipitated with
condensed tannins (grape seed, mDP approximately 8.3;
sorghum, mDP approximately 19.5) using nephelometry to
calculate tannin–protein binding affinity (Girard et al., 2018).
Grape seed tannins required a minimum molar concentration
of 10.7 to 12.7 to precipitate 1 mole of glutenin protein
fraction, whereas sorghum tannins required significantly less:
3.6 to 3.9 moles to precipitate 1 mole of glutenin protein
fraction (Girard et al., 2018). Thus the larger sorghum tannins
were approximately 3× more efficient gluten cross-linkers
than the smaller grape seed tannins.
The increase in protein precipitation efficiency with higher
MW tannins was similarly seen with BSA (Harbertson et al.,
2014; Zeller et al., 2015). Zeller et al. (2015) separated
condensed tannins from two sources (white clover and big
trefoil) into two fractions (mDP approximately 9 and 18)
totaling four separate tannin fractions. To precipitate 50% of
the BSA, the larger mDP fractions required 0.433 to 0.447
mg tannin/g protein, versus 0.698 to 0.731 mg tannin/g
protein for the smaller mDP fractions (Zeller et al., 2015).
The condensed tannin source and structural differences were
irrelevant; only the mDP affected binding kinetics. The more
polymerized tannins have a greater number of hydroxyl
groups and hydrophobic regions available for interaction with
20
proteins. Thus, highly polymerized tannins are more efficient
at cross-linking proteins into larger complexes. These larger
protein complexes can significantly alter protein rheology.
Highly polymerized tannins can improve dough handling
properties by increasing gluten matrix density through tannin
cross-linking. For example, sorghum-condensed tannins
at 2.5 mg/g flour increased wheat flour dough mixing
time by 64% and peak angle by 15%, indicating that the
condensed tannins strengthened the gluten proteins and
reduced breakdown from overmixing. By comparison, the
relatively smaller grape seed-condensed tannins increased
mix time by 40%, but decreased peak angle by 5% (Girard
et al., 2016). The implication is that the highly polymerized
sorghum-condensed tannins were able to greatly improve the
dough mixing strength and tolerance. The mostly oligomeric
grape seed tannins modestly strengthened the dough, yet
made it more susceptible to overmixing. This suggests
that the higher MW tannins cross-link gluten enough to
overcome the destabilizing and depolymerizing antioxidant
effect, whereas the lower MW grape seed tannins cannot
fully overcome the inherent antioxidant effect of tannins on
gluten.
Effects of gluten conformation on tannin–gluten interactions.
Although the tannin type and size are clearly important, the
protein conformation also greatly affects tannin–protein inter-
actions. Recent work has shown that, at room temperature
(e.g., during dough mixing), condensed tannins preferentially
interact primarily with glutenin fractions in wheat flour
through hydrophobic interaction and hydrogen bonding (see
Figure 6 for proposed interaction sites) (Girard et al., 2018).
For example, sorghum-condensed tannins (mDP approxi-
mately 19.5; 7.5 to 30 mg/g protein) were added to solubilized
gliadin and glutenin proteins; the proteins that remained sol-
uble (i.e., those not precipitated by protein) were assessed by
reversed phase HPLC (RP-HPLC) (Girard et al., 2018). Both
solubilized gliadin and glutenin protein concentrations were
decreased in a dose-dependent manner (Girard et al., 2018).
At 30 mg/g protein, the tannins decreased glutenin fraction
solubility by about 31%, whereas the gliadins decreased by
12% to 20% (Girard et al., 2018). Thus, the tannins com-
plexed the glutenins, which have a fairly elongated and open
conformation, to a greater extent than the gliadins, which
are comparatively more globular. Because of the much more
extended structure of glutenins, tannins have better access to
glutenin amino acid residues for noncovalent interactions.
Further, within the glutenins, HMW-GS solubility
decreased about 75%, whereas LMW-GS decreased only 6%
to 12% (Girard et al., 2018). The HMW-GS are much larger
(65 to 90+ kDa; Delcour & Hoseney, 2010) than the LMW-
GS (30 to 60 kDa; Delcour & Hoseney, 2010), and they have a
more elongated structure in comparison. These factors likely
allowed for more extensive noncovalent interactions because
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
the tannins had better access to amino acid side chains. To
further investigate which glutenin subunits were complexed
with tannins, the HMW-GS–tannin complexes were resol-
ubilized with sodium dodecyl sulfate and triethanolamine,
and then analyzed with lab-on-a-chip electrophoresis (Girard
et al., 2018). This produced additional evidence that showed
that the larger x-type HMW-GS (82 to 88 kDa; Shewry,
Halford, & Lafiandra, 2003) were precipitated to a greater
extent than y-type (67 to 73 kDa; Shewry et al., 2003) (Girard
et al., 2018). Thus, protein size and conformation are key in
determining their interaction with tannins.
Effects of tannin–gluten interactions on gluten functionality
Tannic acid cross-linking was shown to improve gluten
strength in doughs and breads. Zhang et al. (2010) found
that 0.01 to 0.03 mg/g commercially available tannic acid
increased dough mixing stability, extensibility, and force to
extend in a dose-dependent manner. At 0.03 mg/g, dough sta-
bility was increased to about 12.5 min, compared to about 6.5
min for the control as measured by a farinograph (Zhang et al.,
2010). The ability of the tannin to increase dough strength
also lead to breads with improved volume; bread volume was
reported as 620 mL when 0.03 mg/g tannin was added versus
524 mL for the control (Zhang et al., 2010). Similarly, Wang
et al. (2015) showed a dose-dependent effect of tannic acid on
improving gluten strength (1.0 to 3.0 mg tannic acid/g flour).
Tannic acid greatly increased mixing strength and tolerance
to overmixing, and increased mean particle size of gluten
from 30 μm in the control to 111 μm with 3.0 mg tannic acid/g
flour (Wang et al., 2015). The particle size increase indicates
that tannic acid cross-linked gluten proteins leading to large
polymers. This suggests that the tannins increased the gluten
matrix size and improved its integrity (Wang et al., 2015).
Similar tannin–gluten effects were seen when condensed
tannins were added to wheat flour. Sorghum-condensed
tannins (0 to 2.5 mg/g) significantly increased insoluble
polymeric protein in wheat flour, indicating the tannins
cross-linked gluten and increased its hydrodynamic volume
(Girard et al., 2016). This effect strengthened the gluten
matrix, which was especially prominent in a weak gluten
flour more so than in a strong gluten flour. For example, the
mixing profile of the control strong gluten flour showed it
took 4.2 min to fully develop (peak) and had a wide peak
angle (112◦ ), indicative of good mixing tolerance (Girard
et al., 2016). By comparison, the control weak gluten flour
took 2.0 min to peak and had a peak angle of 99◦ , evidencing
its weaker gluten network and lower mixing tolerance (Girard
et al., 2016). However, sorghum-condensed tannins added
to the weak gluten flour at 2.5 mg/g flour increased the
resistance of a weak flour dough to mixing such that it
resembled a strong gluten flour mixing profile: 3.5 min to
peak, 116◦ peak angle (Girard et al., 2016). Further, the creep
and recovery profile of the weak tannin–gluten dough showed
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
F I G U R E 6 Proposed proanthocyanidin–gluten interactions and complex formation
sorghum-condensed tannins decreased retarded compliance
(a measure of dough deformation) by nearly 50% compared to
the control, and increased the relative recovery from deforma-
tion by 1.8×, nearly to the level of strong gluten dough (Girard
et al., 2016). This implies the tannin–gluten cross-links cre-
ated a much more elastic dough than the control. Thus,
strength of gluten can be greatly increased by tannin cross-
linking.
Tannin–gluten interactions can also improve batter prop-
erties. For instance, in a 40% pastry flour, 60% water (w/w)
batter, sorghum-condensed tannins and tannic acid (5 mg
tannin/g gluten) increased batter viscosity by 98% and 33%,
respectively, compared to the control (Girard et al., 2019).
Further, both tannins stabilized the batters; liquid separation
was reduced by 79% up to 1 hr. Together, this suggests
21
that that tannin–gluten, especially condensed tannin–gluten,
interactions stabilize batters, likely by cross-linking gluten
and increasing its hydrodynamic volume. This is an important
attribute in batter-type products that are chemically leavened;
they rely on the viscosity of the product to prevent air cells
from coalescing and retain gas as it expands.
By cross-linking gluten proteins in doughs, films, and
batters, tannins were shown to create stronger doughs and
films and more viscous batters (Girard et al., 2016; Girard
et al., 2019; Liu, Shi, Song, Wu, & Zhang, 2018; Wang
et al., 2015; Zhang et al., 2010). Between gluten proteins,
tannins are most likely to interact with glutenins, especially
large HMW-GS, leading to extra-large polymers. This greatly
strengthens the gluten structure and could improve strength of
wheat flour doughs, thus machinability. The ability of tannins
22
to further cross-link gliadin proteins when heated (Section
4.2.2.1.1) could stabilize structure of products that rely
upon stable system viscosity to prevent air cell coalescence
and capture expanding gas during baking, such as quick
breads and cakes. Gliadins do not typically benefit the gluten
matrix strength, but if tannins can cross-link gliadin with the
glutenin macropolymer, it is likely to lead to dense, fibrous
structure in extruded products such as texturized gluten.
5 POTENTI AL AP P L ICAT IO N S O F
POLY PHENOL-GLUTEN
I N T E R AC T I O N S
To capitalize on their health benefits, polyphenols could
be added to wheat-based foods that are consumed world-
wide in a multitude of forms. In addition, as consumers
increasingly look for “natural” and clean-label products,
polyphenols derived from botanical sources may play a role
as redox reagents to modify the gluten network. Further,
these polyphenols are often sourced through waste streams
(e.g., grape pomace, cereal bran, and etc.), so they are an
economical ingredient.
5.1 Applications of monomeric
polyphenols–gluten interactions
5.1.1 Uses of monomeric polyphenols as
processing aids
Although monomeric flavonoids and phenolic acids reduce
gluten strength as previously discussed, this property could
be useful in some wheat-based product applications. The
antioxidant effect of monomeric phenolics could be used
to reduce dough mixing time and improve flexibility of the
gluten network; currently, reducing agents such as bisulfites
are used for these purposes. For instance, L-cysteine is
commonly added during tortilla production to increase dough
extensibility and decrease elasticity, allowing for desirable
expanded tortilla diameters during the hot-press (Bejosano
& Alviola, 2015). Monomeric phenolics are a label-friendly
ingredient that would provide similar function. Monomeric
phenolics could also be used to inhibit gluten matrix forma-
tion in products where an extensive gluten network is not
desired, for example, in cakes, cookies, or pressed or rolled
products such as pie crust.
5.1.2 Uses of monomeric polyphenols in
gluten films
The antioxidant effect of phenolics could also be used to
modify gluten-based films, for example, to plasticize gluten
and improve film flexibility. The film-forming nature of
gluten is important within bakery products to capture gas
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
and leaven. Hager et al. (2012) showed that gallic acid at
50 and 100 g/kg gluten increased gluten film elongation by
16% and 45%, respectively, and decreased (21% and 51%,
respectively) force required to extend film. At these high
usage levels, gallic acid apparently plasticized gluten films,
probably by reducing intermolecular protein interactions and
instead forming protein–gallic acid hydrogen bonds (Soares
& Soldi, 2010). These interactions prevent disulfide bonds
from reforming, and thus reduce protein macromolecule size.
Lower usage levels (10 to 20 g gallic acid/kg gluten) did not
greatly alter film extensibility (Hager et al., 2012). Because
of this, adding phenolic acids at low levels could be useful
if the goal is to increase polyphenol intake (e.g., for health
benefits), without altering gluten film tensile properties.
Conversely, low usage levels of monomeric polyphenols
may be able to improve gluten film integrity. For example,
catechin at 10 g/kg gluten produced gluten films with very
smooth surfaces and no cracks visible via SEM, unlike the
control films (Girard et al., 2019). Catechin slightly, though
not significantly, increased gluten film extensibility and force
required to extend film (Girard et al., 2019). This implies that
the antioxidant action of catechin may have given the gluten
proteins greater mobility and structural flexibility, allowing
them to cure into a more cohesive protein film. Similarly, the
reducing agent sodium sulfite (13 g/kg gluten) was shown
to decrease gluten film extensibility and increase its tensile
strength (Gennadios, Weller, & Testin, 1993). Reducing
agents such as this are used to aid in protein unravelling
and dispersion by cleaving disulfide bonds for protein films,
as well as in extrusion-based texturizing of proteins. Thus,
monomeric polyphenolics are a viable ingredient to replace
chemical-reducing agents such as sodium bisulfite.
5.1.3 Uses of monomeric polyphenols in
wheat-based foods for safety and health
Flavonoids have also shown promise as glycation inhibitors.
Glycation inhibitors prevent reducing sugars from reacting
with amino acids, which in turn prevents release of advanced
glycation end-products (AGE) (Matsuda, Wang, Managi, &
Yoshikawa, 2003). AGE can cause or exacerbate chronic
diseases, especially diabetic complications, when they
accumulate in vivo (Singh, Barden, Mori, & Beilin, 2001).
AGE can accumulate in the body through dietary ingestion
of AGE (Stirban et al., 2008) or through in vivo metabolism
(Schmidt et al., 1994). Dietary AGE and their precursors
occur in heat-treated food products that undergo Maillard
browning like most bakery items (Uribarri et al., 2010).
Flavonoids can reduce dietary AGE. For example,
epigallocatechin-3-gallate (3.3 to 9.9 g/kg flour) reduced
acrylamide (a common AGE precursor) formation in bread
crust by 30% to 37% as compared to the control (52 μg/kg
food) (Fu et al., 2018). Similarly, grape seed extract (rich
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
in catechins and low-MW tannins) was added to bread at a
concentration of 0.86 to 2.86 g/kg flour; within the crust,
grape seed extracts reduced the AGE carboxymethyllysine
by up to 50% from the control of 35 mg/kg food (Peng et al.,
2010). Quercetin at 2.0 g/kg flour also reduced dietary AGE
in bread crust (62% less than control) and crumb (55%) (Lin
& Zhou, 2018), as well as in steamed bread (crumb, 59%;
crust, 52%) (Lin et al., 2018). Because the flavonoids are
inhibiting the Maillard reaction, the resultant products may
have a lighter color (Fu et al., 2018). But, the inherent color
of the polyphenol source often has a bigger impact on product
color. For instance, dark purple/red grape seed extract gave
bread a darker color than the control (Peng et al., 2010).
Thus, the reduction in color intensity by reducing Maillard
reaction could be offset by natural pigments.
Besides reducing dietary AGE, flavonoids have the poten-
tial to reduce in vivo reactions that create AGE. Quercetin
added to baked bread at 0.5 to 2.0 g/kg flour reduced AGE
formation in a BSA–glucose in vitro fermentation system
up to 60% (Lin & Zhou, 2018). Similarly, the same levels of
quercetin reduced AGE formation induced by methylglyoxyl
in BSA by over 50% (Lin & Zhou, 2018). This suggests that
quercetin inhibits both total protein glycation as in the BSA–
glucose system, and inhibits one of the main precursors of
AGE, methylglyoxal. The researchers (Lin et al., 2018) used
the same method with a steamed bread matrix (i.e., a bread
cooked with steam, thus far lower Maillard reaction occurs
than when baked) and found that at 2.0 g/kg flour, quercetin
decreased in vitro protein glycation by 40% (Lin et al.,
2018). However, higher usage levels (up to 36 g quercetin/kg
flour) did not further reduce glycation and had unacceptable
detrimental effects on the steamed bread quality (Lin et al.,
2018). Because quercetin has a high radical scavenging
activity, it is able to trap reactive dicarbonyl compounds (e.g.,
methylglyoxal) and prevent protein glycation (Li, Zheng,
Sang, & Lv, 2014). Adding flavonoids to foods as glycation
inhibitors, both in baked products and in vivo, is a recent line
of inquiry with promising results.
5.2 Applications of tannin–gluten
interactions to improve food quality
5.2.1 Uses of tannins to improve gluten
functionality in wheat-based foods
By strengthening the gluten matrix, tannins could improve
the functionality of weak gluten flours in bread-type prod-
ucts. Tannin–gluten interactions could also improve protein
network density in wheat dough so that it is able to support
nonendosperm inclusions such as fiber, bran, or other ingre-
dients that could benefit health. By improving the protein
network, this clean-label ingredient could be used to produce
light, airy wholesome wheat-based foods with improved
organoleptic quality.
23
The ability of tannins to cross-link gluten proteins both
at room temperature (e.g., during mixing) and when heated
(e.g., during baking) could stabilize structure of products
that rely upon system viscosity, such as quick breads and
cakes. Similar to improving the network density in doughs,
the cross-linking of tannins and proteins could allow for
enhanced volume of baked batter-based foods. This could
also enable higher inclusion of nonendosperm ingredients,
such as bran and fiber, without the use of other additives.
Beyond baked products, tannin–gluten interactions could
improve foods such as steamed bread and noodles. Elastic,
cohesive, and nonsticky are desirable eating qualities for
northern style Chinese steamed bread (Huang, Quail, Moss,
& Best, 1995). Tannins could improve the eating quality of
steamed bread, even with inclusions, by increasing gluten
elasticity and protein network density. Within noodles,
tannins potential to create ternary complexes of tannin–
gluten–starch could allow for cohesive noodles fortified with
protein or fiber.
Though tannins are known for producing an astringent
oral sensation, tannin–gluten interactions may limit this
sensory attribute. Astringency is at least partly caused by
tannins interacting with and precipitating salivary proteins
(Rossetti, Bongaerts, Wantling, Stokes, and Williamson,
2009), but this mouth-drying sensation can be reduced by
tannin–protein interactions (Jauregi, Olatujoye, Cabezudo,
Frazier, & Gordon, 2016; Yan, Hu, and Yao, 2009). For
example, milk reduces the astringent effect of tea, through
interactions of tea flavan-3-ols and dairy proteins (Yan, Hu,
and Yao, 2009). Tannins already complexed with gluten
proteins would likely be unavailable for interactions with
salivary proteins, thus unlikely to induce astringency.
5.2.2 Uses of tannins to improve gluten
functionality in plant-based meat alternatives
The fact that tannins preferentially interact with glutenin
protein fractions at room temperature (Girard et al., 2018) and
gliadin fractions at elevated temperatures (Girard et al., 2019)
suggests that processing conditions could be manipulated
to alter the impact of tannins on gluten network for desired
outcomes. For instance, extrusion is likely to cross-link
tannins with glutenins during the initial mixing stages, and
gliadins as the heat and pressure increases. This could lead
to a strong, dense protein matrix that could reduce protein
solubility, increase protein texture, and even create new,
durable materials.
The tannin interactions could be leveraged in extruded
gluten for meat extenders and analogues, that is, textured
vegetable protein. To texturize gluten, the proteins are dena-
tured and plasticized with heat and mechanical pressure in
a single or twin screw extruder. Then, as the gluten proteins
are extruded through a die, they realign and reassociate in
24
new structures, which can closely imitate meat proteins. The
antioxidant capacity of tannins could aid in unravelling and
denaturing proteins during extrusion, such as other reducing
agents (e.g., bisulfites) used as processing aids. However,
the protein cross-linking nature of tannins will likely greatly
strengthen the extruded gluten proteins. Perhaps so much so
that gluten can be textured to mimic intact meat such as steak
or pork chops. This is a wholly unexplored use for tannin–
gluten interactions. Using the same principles, tannin–gluten
interactions could be used to modify or create novel animal
feeds such as pet food and fish pellets. Hydrolyzed gluten is
sometimes used in meat and other animal product mimetics;
tannins will likely reduce protein solubility by cross-linking
hydrolyzed gluten.
5.3 Applications of tannin–gluten
interactions to modify macronutrient
digestibility
Excess calorie consumption, a well-known major risk factor
for noncommunicable diseases, is a huge global health con-
cern. Altering caloric density of foods is a great intervention
target. For instance, bread is a staple food, widely consumed
in many cultures. Ability of tannins to complex gluten
could potentially be used to reduce caloric impact of such
food.
Relatively high levels of dietary tannins can reduce protein
digestibility by denaturing proteases, inhibiting intestinal
amino acid transporters, and complexing proteins, and thus
resisting protease enzyme hydrolysis (Goncalves, Soares,
Mateus, & de Freitas, 2007; King, Fian, Ejeta, Asem, &
Adeola, 2000; Taylor, Bean, Ioerger, & Taylor, 2007). For
example, sorghums with low (less than 13 mg tannin/g flour)
and high amount of tannin (60 to 67 mg tannin/g flour) were
fed to rats over 14 days (Moraes et al., 2012). The protein
digestibility of the low-tannin sorghum group was greater
than 86% (compared to 94% digestibility with the casein
control, not significantly different at P < 0.05), whereas
the high-tannin sorghum had a much lower digestibility of
58% to 63% (Moraes et al., 2012). Similarly, high levels of
sorghum-condensed tannins (20.2 mg/g diet dm) exhibited a
10% reduction in protein digestibility, which led to decreased
rabbit growth of 10% when fed over 4 weeks, but low tannin
levels (7.9 mg/g diet dm) did not reduce protein digestibility
or rabbit growth (Al-Mamary, Al-Habori, Al-Aghbari, &
Al-Obeidi, 2001). Another study of rabbits fed a diet of
chestnut tannins (mostly hydrolysable, 0 to 10 mg/g dm)
for 50 days showed that tannins did not reduce rabbit live
weight or hot carcass weight (Liu et al., 2009). Thus, at
the levels where tannins have shown a positive effect in
gluten rheology (mostly <3.0 mg tannin/g flour), protein
digestibility is not inhibited. It is thus not likely that tannins
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
would reduce excess calorie consumption by reducing protein
digestibility.
However, even at low tannin usage levels starch digestibil-
ity can be affected by tannin–protein interactions (Austin,
Turner, McDonough, & Rooney, 2012; Dunn et al., 2015).
Reduction in starch digestibility has been shown with
wet-cooked porridges, where tannin–protein interactions are
likely to occur. For instance, starch digestion properties of
sorghum porridge with 15% tannin sorghum bran substitution
(3.6 to 11.3 mg/g porridge dm) were analyzed (Austin et al.,
2012). Tannin treatments decreased in vitro starch digestibil-
ity by 7% to 16% and estimated glycemic index by 5% to 11%
while increasing resistant starch by 3 to 10× compared to
the control sorghum porridge (Austin et al., 2012). Though
the authors did not study protein–tannin interactions, they
suggested that this complexation may have been one of the
factors that reduced starch digestion by slowing digestive
enzyme access to starch. In wheat flour tortillas, sorghum
bran substitution at 25% supplying 1.87 mg condensed tannin
per gram of flour reduced in vitro rapidly digestible starch
by 8% and increased slowly digestible starch by 73% as
compared to the control (Dunn et al., 2015). The starch
digestibility of tortillas with nontannin brans (wheat, white
and black sorghum) was not significantly different from the
control (Dunn et al., 2015). It is likely that tannin–gluten
interactions slowed amylase enzyme degradation by creating
a viscous matrix surrounding starch, which inhibited enzyme
access.
Decreasing rapidly digestible starch and increasing slowly
digestible starch could help to modulate postprandial blood
glucose levels (Lee, Bello-Pérez, Lin, Kim, & Hamaker,
2013). Slowed rate of starch digestion may reduce subsequent
calorie consumption through increased satiety between meals
(Holt & Miller, 1995; Willis, Eldridge, Beiseigel, Thomas,
& Slavin, 2009). With the prevalence of lifestyle-related
diseases increasing, in vivo research should focus on tannins
ability to complex with macronutrients and slow glycemic
response.
5.4 Applications of tannin–gluten
interactions to reduce inflammatory response
to gluten proteins
The ability of tannins to bind gluten proteins has also been an
area of interest to reduce the immune response in individu-
als with celiac disease or wheat allergies to gluten proteins,
especially gliadins. Condensed tannins have been shown
to complex with partially digested gliadin subfractions
(Dias, Perez-Gregorio, Mateus, & De Freitas, 2015). This
proof of concept work showed that tannins could com-
plex some gliadin proteins, though it did not show if
this affects immune response to the offending proteins.
However, cranberry extract (approximately 34% extractable
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
phenolic content, 100 μg/mL), which can contain up to
38 mg/g A- and B-type condensed tannins (Table 3), inhib-
ited wheat allergy patients’ immunoglobulin E (IgE) anti-
body recognition of gliadin proteins at 10 and 20 μg in
dot blot analysis (Perot et al., 2017). This indicates that
tannins could limit the immune response to gliadins by
cross-linking the allergenic protein. Further, the cranberry
extract (3 mg extract/mg gliadin) reduced 𝛽-hexosaminidase
release in a rat basophil leukemia model sensitized with
mouse IgE by 41%, confirming that the protein–phenol inter-
actions did reduce the allergenic response (Perot et al.,
2017).
Similarly, hydrolysable tannins and condensed tannins
within a pomace extract have been used to bind to and reduce
allergenicity of peanut proteins (Chung & Reed, 2012;
Plundrich, Bansode, Foegeding, Williams, & Lila, 2017).
For instance, complexes of hydrolysable tannins (0.125 to
0.4 mg tannic acid/mg peanut butter protein extract) and
peanut proteins did not release proteins in in vitro simulated
digestion buffers (pH 2 and 8) (Chung & Reed, 2012).
ELISA data showed 0.2 and 0.4 mg tannic acid/mg peanut
butter protein extract led to 75% and 100% reductions in IgE
binding, respectively (Chung & Reed, 2012).
By complexing with proteins, these polyphenols are
likely changing protein conformation or masking the epi-
topes causing adverse reactions, thus rendering the proteins
hypoallergenic (Plundrich et al., 2014). Van Buiten, Yen-
nawar, Pacheco, Hatzakis, and Elias (2019) showed that
epigallocatechin-3-gallate interacted with one of the proteins
responsible for celiac disease pathogenesis, 𝛼 2 -gliadin, via
noncovalent interactions, which increased relative helicity.
This change in conformation was likely responsible for the
reduction in inflammatory response found in a previous
study from the same lab (Van Buiten, Lambert, & Elias,
2018). Green tea extract (413 mg epigallocatechin-3-gallate
mg−1 ) at a 1:1 ratio with partially digested gliadins down-
regulated production of inflammatory biomarkers (IL-6
and IL-8) in Caco-2 cells from 1 to 24 hr (Van Buiten
et al., 2018). This indicates that tannin–gliadin interactions
may reduce intestinal inflammation associated with celiac
disease. These studies are promising, but more research is
needed to establish the tannin–gliadin fraction interaction
mechanisms, how these complexes alter immune responses,
and efficient, practical methods to use the tannin–gliadin
interactions.
5.5 Applications of tannin–gluten
interactions to create novel materials
5.5.1 Uses of tannin–gluten interactions in
biopolymers
Biopolymers are ecofriendly alternatives to plastics because
they rely on renewable resources and are biodegradable.
25
However, compared to plastic films, biopolymer films have
limitations. Generally, biopolymer films are weaker and
less extensible, with higher permeability to gases and water
(Hernandez-Izquierdo & Krochta, 2008; Lagrain, Goderis,
Brijs, & Delcour, 2010). Because of this, biopolymers have
yet to be widely adopted.
An advantage of gluten-based protein biofilms over other
proteins is that gluten has lower water vapor permeability
(Gennadios et al., 1993), which can prevent moisture migra-
tion. Gluten proteins also have low water solubility, which
prevents film dissolution and helps it to maintain structure
(Girard et al., 2019; Gontard, Guilbert, & Cuq, 1992; Hager
et al., 2012). The viscoelasticity of gluten proteins is unique
and can provide good structural integrity for biofilms. How-
ever, native gluten proteins have poor emulsifying properties
and low water solubility, which can make them difficult
to disperse in solution-cast methods and cause protein
clumping.
Gluten films can be created by wet processing (solution-
casting) or dry processing (e.g., compression molding
or extrusion). In either method, gluten functions to
create a highly cross-linked polymer network. This net-
work is often so cross-linked and strong that plasticizers
(e.g., glycerol) are necessary to reduce film brittleness
(Park, Bunn, Weller, Vergano, & Testin, 1994; Soares
& Soldi, 2010). Tannin–gluten interactions could be
exploited to improve the limiting characteristics of gluten
films and produce functional biopolymers for various
applications.
For instance, increasing protein network density with
tannin cross-links can improve a films resistance to break-
age under tension, that is, increase gluten film tensile
strength (Girard et al., 2019; Hager et al., 2012). Sorghum-
condensed tannins (10 mg/g gluten) increased solution-cast
gluten film tensile strength from 1.2 to 1.6 MPa (Girard
et al., 2019). Similarly, commercial tannic acid added
to solution-cast gluten films at 50 to 300 mg/g gluten
increased tensile strength to 1.36 to 3.22 MPa, in a dose-
dependent manner, from a control of 1.08 MPa (Hager et al.,
2012). Thus, tannin–gluten cross-linking can improve film
strength, which is one of the limiting factors to adoption of
biopolymers.
Further, though it improved gluten film strength, con-
densed tannins at 10 mg/g gluten did not significantly reduce
extensibility (Girard et al., 2019). Typically, an increase
in tensile strength comes at the expense of extensibility,
indicating film stiffening. For example, in Hager et al.’s
(2012) work, control gluten film elongated 2.05× its original
length, whereas gluten films with tannic acid concentrations
of 50 to 100 mg/g only elongated 84% to 88% (Hager et al.,
2012). At very high levels (up to 300 mg/g), the film was
stiff and essentially broke before extending (Hager et al.,
2012). Thus, high usage levels of tannins can increase film
26
strength but can also create stiff, unyielding structures.
Conversely, low levels of tannins can still significantly
strengthen the structure, but may less extensively cross-link
proteins, thereby retaining film flexibility. The combination
of strength and flexibility is paramount in biopolymers for
edible films and even biomedical applications.
By cross-linking protein structures via hydrogen bonding,
tannins may reduce exposed polar amino acid residues, and
thus decrease water vapor permeability. In fact, tannic acid at
up to 100 mg/g decreased water vapor permeability of gluten
films (Hager et al., 2012). Tannin–gluten interactions may
also reduce gas permeability by increasing the protein net-
work density. In solution-cast kafirin (the prolamin fraction of
sorghum) films, both tannic acid and condensed tannins (50
to 200 mg/g kafirin) decreased oxygen permeability by 38%
to 54% in a dose-dependent manner (Emmambux, Stading,
& Taylor, 2004). The fact that tannins and gluten interact
by similar mechanisms as tannins and kafirin suggests
tannin–gluten interactions could reduce gas permeability
in gluten films, though oxygen or other gas permeability
has not been studied in tannin–gluten films. Gluten films
strengthened with tannin cross-links could be used for edible
packaging or separation of layers (e.g., between the sauce
and crust of a ready-to-bake pizza) within a food product
to prevent moisture migration. Further work is needed to
understand how tannin–gluten interactions affect water vapor
and gas permeability, so highly functional films can be
created.
5.5.2 Tannin–gluten interactions in biofilms
to selectively distribute micronutrients
The tannin-gluten based biofilms could selectively distribute
micronutrients or bioactive compounds to targeted areas of
the digestive tract. Kafirin–tannin matrices were found to be
stable to pepsin in vitro digestion (pH 2) for up to 2 hr, which
could enable targeted delivery of micronutrients throughout
the digestive tract (Taylor, Taylor, Belton, & Minnaar, 2009).
Similarly, tannin–gluten complexes may survive digestion
within the stomach and reach the small intestine or even
the colon. For example, gluten-condensed tannin (10 mg/g
gluten, relatively low amount) films were mostly insoluble
at pH 2 and 7 (Girard et al., 2019). They were only partially
digested (17% less than control) by protease hydrolysis
using pepsin in a pH 2 buffer at 37 ◦ C (Girard et al., 2019).
Alternatively, perhaps a premeal encapsulated tannin (e.g.,
a gluten gummy with tannin) could be consumed to deliver
tannins to the small intestine to slow starch digestion by
complexing with and inhibiting digestive enzymes. Inhibiting
starch digestion in the small intestine could also increase
amount of starch available for fermentation in the colon. The
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
increase in starch fermentation in the colon could generally
leads to a more diverse colon microbiota.
5.5.3 Nonfood uses for tannin–gluten films
Tannin–gluten cross-linking could further be leveraged
outside of food use including second skin type products in
medicine (Taylor, Anyango, & Taylor, 2013), self-healing
hydrogels (Liu, McClements, Li, Xiong, & Sun, 2019), or
bio-adhesives for wood (Lei et al., 2010). Gluten nanofibers
can be produced with electrospinning, and could be used in
biomedical applications such as tissue scaffolding (Woerde-
man et al., 2005). By cross-linking gluten proteins, tannins
could plausibly improve the fiber strength and stability. In
fact, this has been shown with electrospun zein fibers. Barba-
timão tannins increased glass transition and melting temper-
atures of zein biofilms, thus improving their thermal stability
(de Oliveira Mori et al., 2014). Tannins have also been shown
to strengthen self-healing hydrogels, which could be used in
food, agriculture, or medical applications (Liu et al., 2019).
Beyond materials, tannin cross-linking improved adhesive
properties of gluten on beech wood, yielding adhesives
with 90% to 95% natural material, which satisfied standard
wood specifications (Lei et al., 2010). Tannin–gluten inter-
actions could also be used to create dense materials, such as
compostable disposable plates and cutlery. Thermo-molded
gluten materials can produce tensile strength approaching
that of low-density polyethylene, high-density polyethylene,
and propylene (Jerez, Partal, Martínez, Gallegos, & Guerrero,
2007; Woerdeman et al., 2004). Increasing molecular entan-
glements with tannin may be able to further strengthen the
structure.
Tannin–gluten interactions can be reinforced with ions,
such as ferric iron (Fe3+ ) (Liu et al., 2019). Gluten hydrogels
were created by mixing gluten in water (0.5 g/mL), then
adding second solution of iron (Fe3+ , 0.020 to 0.067 mg/g
gluten) and condensed tannins (unspecified origin and mean
DP, 0.033 to 0.600 mg/g gluten) (Liu et al., 2019). This
created a double-network matrix that recovered quickly from
repeated stress (shear deformation-compression cycles) (Liu
et al., 2019). Liu et al. (2019) showed that increasing the
ratio of iron to tannins from 1:2 up to 1:4 greatly increased
the elastic character of the double-network hydrogels
compared a control gluten hydrogel and a gluten hydrogel
with condensed tannin alone. This suggests that ferric
iron strengthened tannin–protein interactions. The authors
proposed this was likely due to each ion binding to two or
more tannin molecules (Liu et al., 2019), thus cross-linking
them and further increasing the matrix density. Tannins show
promise in improving gluten film structure and integrity,
and this effect can be additionally strengthened by ions like
Fe3+ .
EFFECT OF POLYPHENOLS ON GLUTEN FUNCTION…
6 CONC LU S I O N S A N D F U T U R E
PROSPECTS
Polyphenols offer myriad potential health benefits. Because
wheat-based foods are broadly consumed, they are a good
target for polyphenol fortification to promote human health.
Generally, polyphenols are strong antioxidants that reduce
gluten protein disulfide bonds, inhibiting protein–protein
interactions, thus reducing gluten strength. This could be
useful in applications where reducing agents are used to
reduce dough shrinkage, such as flatbreads. However, the
antioxidant effect is detrimental in products where a robust
gluten network is needed, such as loaf breads and bagels.
Unlike monomeric polyphenols, the polymeric polyphe-
nols (tannins) are capable of overcoming the antioxidant
gluten-weakening effect of polyphenols by noncovalently
cross-linking proteins through extensive hydrogen bonding
and hydrophobic interactions. This leads to much stronger
and more resilient gluten protein polymer complexes com-
pared to native gluten. The tannin–gluten interactions offer
opportunities for new and expanded wheat protein functional-
ity. As both tannin and gluten MW distribution are important
factors in these interaction, selection of raw materials (wheat
protein composition or subfractions, and tannin profile)
could be optimized to alter gluten functionality for desired
applications. Because tannin interaction with gluten proteins
is not entirely random, it can be manipulated to produce
desired rheological behavior. Tannins interact preferentially
with the largest gluten protein fraction available; thus the
larger glutenin fractions are more likely to be affected by
tannins. However, as proteins denature (e.g., with increasing
temperature), amino acid residues are exposed that favor
tannin interaction with smaller, globular proteins. In this way,
the relatively globular gliadins complex with tannins more
efficiently at elevated temperatures. This can greatly help
increase system viscosity during thermal processing, thus
improving final product texture.
Leveraging these interactions, tannins could be used in
wheat-based foods and materials to improve gluten strength
in food matrices, to enhance quality of textured gluten pro-
teins, to modify starch digestibility, or to create novel bio-
materials such as edible films or second skin type products.
To employ tannin–gluten interactions for novel functionali-
ties, further studies should assess:
1. Precise mechanisms by which tannins interact with differ-
ent gluten protein fractions to be able to select specific tan-
nins, protein profile, and processing conditions for desired
rheological outcomes.
2. Restructuring gluten via tannin cross-links for expanded
use in plant-based meat mimetics. This is an untapped
potential for utilizing tannin–gluten interactions. Tannins
primarily cross-link glutenins at room temperature, but at
27
elevated temperatures, tannins interact with gliadins as the
proteins denature and expose amino acid residues. Thus,
tannins can incorporate gliadins into the gluten macrop-
olymer. This could vastly alter protein textures, especially
in extruded products.
3. Effect of tannin–gluten interactions in food matrices on
macronutrient digestion and on colonic microbiota and
their metabolites: Tannins show promise in slowing or
inhibiting starch digestion, but additional work is needed
to leverage tannin–protein interactions to modulate caloric
density of foods. Further, the ability of tannins to slow
starch digestion may increase substrate for microbial fer-
mentation of carbohydrates through the colon. The abil-
ity of colonic microbiota to catabolize or release tannins
from tannin–protein complexes has not been studied. Con-
versely, tannin–protein complexes could alter microbiota
colonies throughout the digestive tract, especially in the
colon.
4. Tannin–gluten–polysaccharide interactions likely occur,
based on the dramatic increase in starch pasting peak
viscosity with tannins in wheat flour, but not tannins in
gluten or starch alone. However, how these complexes
affect product texture and subsequent starch retrogradation
is unknown.
5. Using tannins to reduce allergenicity or inflammatory
responses to gluten proteins is a promising line of research.
Understanding tannin–gluten interaction mechanisms is
key to creating practical and efficient methods to employ
this interaction.
6. Tannin–gluten matrixes have potential in new material
applications including edible films, biomedical products,
adhesives, and heavy-duty plastic replacement. Future
research should focus on materials science and physical
properties of tannin–gluten complexes.
AU T H O R CO N T R I B U T I O N S
A. Girard developed the manuscript concept, performed lit-
erature reviews and analyses, and wrote the manuscript. J.
Awika edited manuscript drafts and provided critical feed-
back. Both authors read and approved the final version for
submission.
CONFLICTS O F INTEREST
The authors declare no conflicts of interest.
O RC I D
Audrey L. Girard https://orcid.org/0000-0002-0257-3887
28
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How to cite this article: Girard AL, Awika JM. Effects
of edible plant polyphenols on gluten protein function-
ality and potential applications of polyphenol–gluten
interactions. Compr Rev Food Sci Food Saf. 2020;
1–36. https://doi.org/10.1111/1541-4337.12572