Mixing animal and plant proteins: Is this a way to improve protein techno-functionalities?

Mixing animal and plant proteins: Is this a way to improve protein techno-functionalities?

Food Hydrocolloids 97 (2019) 105171 Contents lists available at ScienceDirect Food Hydrocolloids journal homepage: www.elsevier.com/locate/foodhyd ...

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Food Hydrocolloids 97 (2019) 105171

Contents lists available at ScienceDirect

Food Hydrocolloids journal homepage: www.elsevier.com/locate/foodhyd

Mixing animal and plant proteins: Is this a way to improve protein technofunctionalities?

T

Alane Cangani Alves, Guilherme M. Tavares∗ Department of Food Science, School of Food Engineering, University of Campinas, Campinas, SP, Brazil

A R T I C LE I N FO

A B S T R A C T

Keywords: Food proteins Aggregation Gelling properties Interfacial activity Techno-functional synergism

In recent years, several research groups have focused on studying the partial replacement of animal proteins with plant proteins in food application, as an alternative to reduce animal protein consumption. This approach has proven to be useful in tracking synergistic techno-functional behaviors of these mixed protein systems with innovative potential. Certain mixed protein systems have been shown to be very efficient in modulating the texture of protein gels, ability to form low-cost edible films and to produce stable emulsions and foams. Thus, this review compiles the described mechanisms behind the behavior of animal and plant proteins in mixed systems, featuring the main strategies applied to enhance their techno-functional synergism and highlighting future challenges for this scientific field.

1. Introduction Proteins are among the major components of food products. Apart from their nutritional relevance, several techno-functional properties of food proteins have been explored by food industries (Lv, Zhao, & Ning, 2017; Toldrá, Reig, Aristoy, & Mora, 2017). Food proteins provide amino acids that are used by the human body as the building blocks for protein synthesis (e.g. hormones, enzymes, antibodies, etc.) (Lv et al., 2017). In the context of food technology however, the physicochemical properties and the behavior of proteins during processing determines the quality of final products. The structural versatility of food proteins and their amphiphilic nature allow them in certain conditions to interact with several compounds in food products. These interactions occur especially through hydrogen bonds, electrostatic interactions and/or hydrophobic association. The interacting compounds include themselves and other proteins, carbohydrates, vitamins, and minerals (Quintero, Naranajo, Ciro, & Rojas, 2017). Thus, the extent of structural changes induced to these proteins during food processing and storage may modulate such interactions. These can dramatically impact on sensorial attributes of food products, such as texture and taste as well as on the technological applications of these proteins (Pizones Ruiz-Henestrosa, Martinez, Carrera Sánchez, Rodríguez Patino, & Pilosof, 2014; Quintero et al., 2017). Raw animal materials such as milk, eggs, meat, and seafood remain the most important sources of proteins recently used by food industries, followed by plant sources such as legumes and nuts. Some emerging



protein sources such as insects, seaweed and in vitro meat (based on cultured cells) still have limited use by food industries (Lv et al., 2017). The projection of a global human population of around 9.5 billion by 2050 indicates that the demand for animal protein will double during this period. However, animal protein production is associated with intense greenhouse gas emissions and a greater demand for land area, unlike plant protein production (United Nations, 2015). This scenario of increased animal protein consumption represents a time bomb, in regard to sustainability and food security that is highlighted by several reports from the United Nations (FAO, 2011; United Nations, 2015). These concerns have consolidated consumer groups like the vegetarians and triggered the emergence of new groups. The flexitarians are one new group, for example, who consciously reduce animal protein consumption without removing it entirely from their diet (Dagevos & Voordouw, 2013; De Backer & Hudders, 2015). The partial replacement of animal protein with plant protein in formulated products stands as the beginning for reduce environmental impacts associated with enormous animal protein consumption (FAO, 2011; Henchion, Hayes, Mullen, Fenelon, & Tiwari, 2017; Mession, Roustel, & Saurel, 2017a). Thus, a growing number of research groups have focused on the development of animal protein-based products or ingredients, supplemented or partially substituted with plant proteins (Chihi, Mession, Sok, & Saurel, 2016; Mession et al., 2017a; Silva, Cochereau, Schmitt, Chassenieux, & Nicolai, 2019b). However, the achievement of this task without affecting technological properties, texture and taste of the products remain a great challenge (Amagliani &

Corresponding author, Rua Monteiro Lobato, 80, Campinas, SP, 13083-862, Brazil E-mail address: [email protected] (G.M. Tavares).

https://doi.org/10.1016/j.foodhyd.2019.06.016 Received 7 December 2018; Received in revised form 11 April 2019; Accepted 17 June 2019 Available online 18 June 2019 0268-005X/ © 2019 Elsevier Ltd. All rights reserved.

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by calcium phosphate nanoclusters (Dickinson, 2003). The CMs are thermal-stable structures, self-aggregating only at temperatures above 140 °C in normal milk pH and ionic environment (Dickinson, 2003). Nevertheless, CMs are very sensitive to chelating agents, which can induce their disruption (Walstra et al., 2005). In the food industry, casein-based ingredients are widely used to improve viscosity, stabilize emulsions and foams and to enhance the nutritional properties of different products (Ranadheera et al., 2016).

Schmitt, 2017; Chihi et al., 2016; Karaca, Low, & Nickerson, 2011; Lin et al., 2017; Mession et al., 2017a). It is noteworthy that the use of plant proteins as ingredients is generally is associated with some limitations such as their poor water solubility and a very pronounced taste (Day, 2013; Silva et al., 2019b; Wouters et al., 2017). However, plant proteins also display some advantages that include a lower cost of production, low allergenicity (with some exceptions, e.g. gluten) and unique techno-functional properties (Chihi et al., 2016; Karaca et al., 2011; Lin et al., 2017; Wouters et al., 2017). Understanding the mechanism behind animal and plant protein interactions represents an opportunity to develop innovative applications. Therefore, this paper provides an overview of the current studies about animal and plant protein interactions in mixed systems. This review will also feature the main strategies applied to enhance their techno-functional synergism.

(b) Major whey proteins: β-Lactoglobulin (β-Lg) and α-lactalbumin (α-La) are the major proteins in bovine whey, representing around 50% and 20% of its total protein content, respectively (Thompson et al., 2009). β-Lg is a globular protein with 162 amino acid residues and a molecular weight of about 18.3 kDa. Its isoelectric point varies between 5.1 and 5.2, and at neutral pH it appears mostly as a non-covalent dimer (Thompson et al., 2009). This protein displays a denaturation temperature of around 75 °C, two disulfide bridges and one free thiol group (- SH) (Chihi et al., 2016; Croguennec et al., 2017; Livney, 2010; Ustunol, 2014; Yada, 2018). On the other hand, α-La displays four disulfide bridges and no free thiol group (Ustunol, 2014; Yada, 2018). It is also a globular protein with a molecular weight of 14.2 kDa, 123 amino acid residues and an isoelectric point between 4.3 and 4.7. α-La is a metalloprotein with one site of high affinity for calcium fixation. While the apo form (without calcium) of α-La denatures around 30 °C, its holo form (presence of calcium) denatures only around 60 °C (Croguennec et al., 2017; Livney, 2010; Yada, 2018). Due to the high reactivity (free thiol group) of β-Lg, especially during thermal treatments, several properties of whey protein isolate (WPI) are dictated by its behavior. During heating, the irreversible aggregation of whey proteins occurs according to the following mechanism: (i) protein unfolding and (ii) aggregation of unfolded proteins by disulfide bounds and hydrophobic interactions (Wolz, Mersch, & Kulozik, 2016).

2. Profile of the main recurrent proteins in mixed systems Proteins from animal and plant sources have been used to develop mixed protein systems. As understanding of the interactions and synergism between proteins in these systems is dependent on their structure and physicochemical properties, this section briefly reviews the main recurrent proteins used in mixed systems. Table 1 summarizes some of the physicochemical properties of the reviewed proteins. 2.1. Proteins from animal sources 2.1.1. Milk proteins Milk proteins are classified into two groups: caseins and whey proteins. In bovine milk, caseins represent 80% of the total protein content (approximately 2.7 g/100 g), while the other 20% correspond to whey proteins (approximately 0.6 g/100 g) (Walstra, Wouters, & Geurts, 2005). (a) Caseins: Four different proteins form the caseins group: αs1-, αs2-, β- and κcasein (Walstra et al., 2005). They are acidic rheomorphic proteins (isoelectric points in the range of 4.9–5.6) of molecular weight between 19 and 24. They display a high content of phosphoserine and proline residues and a poor number of sulfur-containing amino acid residues (Beliciu & Moraru, 2011; Croguennec, Tavares, & Bouhallab, 2017; Thompson et al., 2009). In milk, these caseins form a sponge-like supramolecular structure, known as casein micelle (CM), of approximately 200 nm of hydrodynamic diameter, 105 kDa and isoelectric point of 4.6 (Ranadheera, Liyanaarachchi, Chandrapala, Dissanayake, & Vasiljevic, 2016; Thompson et al., 2009). To form CMs, the different caseins are bound together by hydrophobic interactions and especially

2.1.2. Egg white proteins Ovalbumin (Ova) is the major protein in egg white, representing around 54% of its dry matter (Anton, Nau, & Lechevalier, 2009). Several other proteins are present in egg white such as ovotransferrin (12–13% of the dry matter), ovomucoid (11% of the dry matter), lysozyme (3.4–3.5% of the dry matter), ovoglobulins (2% of the dry matter) and ovomucin (1.5–3% of the dry matter) (Anton et al., 2009). The main techno-functional property of egg white used by the food industry is its ability to form and stabilize foams, which is highly associated with Ova (Ustunol, 2014). Ova is a globular phosphoglycoprotein composed of 386 amino acid residues, with a molecular weight of about 45 kDa and an isoelectric

Table 1 Physicochemical properties of the main recurrent proteins in animal and plant protein mixed systems (Thompson, Boland, & Singh, 2009; Ustunol, 2014; Yada, 2018).

Animal proteins

Plant proteins

Source

Protein

Isoelectric point

Molecular weight (Mw) (kDa)

Milk

Caseins

4.6–5.6

β-Lactoglobulin (β–Lg) α-Lactalbumin (α–La) Ovalbumin (Ova) Gelatin β-Conglycinin (7S) Glycinin (11S) Vicilin (7S) Legumin (11S) Gliadin Glutenin

5.1–5.2 4.3–4.7 4.5 5–9 4.9 4.6 4.5 4.5 6–7 6–7

Individual Caseins: 19–24 Casein Micelle ≈ 105 18.3 14.2 45 ∼300 150–200 300–380 ∼150 360–400 30–75 High Mw subunits: 80 - 120 Low Mw subunits: 30 - 51

Egg White Cattle/Fish Soybean Pea beans Wheat

2

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2.2.2. Pea proteins Legumin (11S) and Vicilin (7S) are the main proteins in pea beans, representing around 50–60% of its total protein content. Both proteins are globulins, and have the same isoelectric point of 4.5 and a denaturation temperature ranging from 82.7 to 85.5 °C (Chihi et al., 2016; McCarthy et al., 2016; Shevkani, Singh, Kaur, & Rana, 2015; Tomé, Pires, Batista, Sousa, & Raymundo, 2015). Convicilin is responsible for a minor contribution of the pea bean protein content (Chihi et al., 2016; Yada, 2018). Legumin (11S) has a hexameric structure with a total molecular weight of around 360–400 kDa, consisting of six subunits (∼60 kDa) each one formed by an acidic α-chain (∼40 kDa) linked to a basic βchain (∼20 kDa) by a disulfide bridge (Amagliani & Schmitt, 2017; Chihi et al., 2016; Klost & Drusch, 2019; McCarthy et al., 2016; Mession, Roustel, & Saurel, 2017b; Tzitzikas, Vincken, de Groot, Gruppen, & Visser, 2006; Yada, 2018). Vicilin (7S), on the other hand, is a trimetric protein of about 150 kDa, formed by subunits of around 50 kDa (Mession et al., 2017b; Tzitzikas et al., 2006). Compared to legumin (11S), vicilin (7S) is a more flexible protein, thus having better interfacial activity (Lam, Can Karaca, Tyler, & Nickerson, 2018).

point of 4.5 (Croguennec et al., 2017; Ustunol, 2014). It contains six cysteine residues, with four found as free thiol groups (- SH) and two involved in one disulfide bridge. This protein has a high content of hydrophobic amino acid residues and a denaturation temperature around 84.5 °C at pH 7.0 in egg white (Croguennec et al., 2017; Donovan & Mapes, 1976; Lechevalier, Croguennec, Anton, & Nau, 2011; Ustunol, 2014). The good foam ability of Ova is related to its tendency to form coagulated protein networks at the air-water interface, which can be improved by its controlled thermal-induced covalent aggregation (Croguennec, Renault, Beaufils, Dubois, & Pezennec, 2007; Dickinson, 2010). 2.1.3. Collagen/gelatin Gelatin is a mixture of polypeptides obtained from the partial hydrolysis of collagen. It is a fibrilar protein which can be obtained from animal skin, bone extract, offal meat and skeletal muscle (Denavi et al., 2009; Gómez-Guillén, Giménez, López-Caballero, & Montero, 2011; Yada, 2018). Usually, collagen is rich in glycine (33%), proline and hydroxyproline (23%) and alanine (11%) residues. However, it has a very small content of tyrosine, histidine and sulfur-containing amino acid residues (less than 1%) (Ustunol, 2014). Gelatin is a widely used ingredient in food industries, due to its ability to form thermo-reversible gels associated with its coil-to-helix transition prompted by cooling (below 30 °C) (Gómez-Guillén et al., 2011; Yada, 2018). Gelatin with different solubility, gel strength and thermal stability properties can be obtained by controlling the hydrolysis process of the collagen (Gómez-Guillén et al., 2011). In general, gelatin can be found as “type A gelatin” and “type B gelatin” displying isoelectric points between 6.0 and 9.0 and near to 5.0, respectively (Gómez-Guillén et al., 2011; Yada, 2018).

2.2.3. Gluten Wheat proteins are divided into three major groups: glutenins, gliadins and albumins/globulins. Glutenins and gliadins are responsible for forming gluten through their polymerization. This polymer has unique cohesive and viscoelastic properties, especially important for bakery products (Ustunol, 2014). Gliadins are monomeric proteins with a molecular weight between 30 and 75 kDa. Glutenins are polymeric proteins formed by high molecular weight subunits (80–120 kDa) and low molecular weight subunits (30–51 kDa) stabilized mainly by hydrophobic interactions and interchain disulfide bridges (Elmalimadi et al., 2017; Guo, Sun, Zhang, Wang, & Yan, 2018; Ustunol, 2014; Yada, 2018).

2.2. Proteins from plant sources

3. The interaction between animal and plant proteins

2.2.1. Soy proteins The major soybean proteins are β-Conglycinin (7S) and Glycinin (11S) which represent around 37% and 30%, respectively, of the total protein content of soybean (Ustunol, 2014). β-Conglycinin (7S) has an isoelectric point of 4.9, a molecular weight varying between 150 and 200 kDa and has a low content of tryptophan and sulfur-containing amino acid residues (Beliciu & Moraru, 2011, 2013; Denavi et al., 2009; Pizones; Ruiz-Henestrosa et al., 2014; Yada, 2018). It is a globular protein formed mainly by α (∼67 kDa), α’ (∼71 kDa) and β (∼50 kDa) subunits. These may be associated in seven different combinations to form a trimer stabilized by hydrogen bonds and hydrophobic interaction (Pizones Ruiz-Henestrosa et al., 2014; Yada, 2018). No disulfide bridges are involved in the stabilization of the trimeric structure (Beliciu & Moraru, 2011, 2013; Pizones Ruiz-Henestrosa et al., 2014). On the other hand, the globular protein glycinin (11S), is a hexamer of 300–380 kDa and has an isoelectric point of 4.6 (Beliciu & Moraru, 2011; Denavi et al., 2009; Pizones; Ruiz-Henestrosa et al., 2014; Yada, 2018). Its quaternary structure is formed by six subunits of 54–64 kDa, and stabilized by hydrophobic and electrostatic interactions. In general, each subunit displays one acidic chain of around 35 kDa and one basic chain of around 20 kDa assembled together by a single disulfide bridge (Beliciu & Moraru, 2011, 2013; Denavi et al., 2009; Pizones; RuizHenestrosa et al., 2014; Yada, 2018). Due to the compact structure of glycinin, its interfacial activity is lower than the one of β-conglycinin, which lacks disulfide bridges (Nishinari, Fang, Guo, & Phillips, 2014). The denaturation temperature of β-conglycinin and glycinin at neutral pH is generally reported between 68 to 79.4 °C and 88–96.4 °C respectively (Guo et al., 2012). β-Conglycinin heated alone tends to form soluble and non-compacted aggregates, whereas glycinin tends to form dense and insoluble aggregates (Guo et al., 2012; Nishinari et al., 2014). In mixture, increasing the proportion of β-conglycinin limits the growth of the co-aggregates (Guo et al., 2012; Nishinari et al., 2014).

Although the interaction between proteins during food processing is well documented (Amagliani & Schmitt, 2017; Foegeding & Davis, 2011), studies describing the interaction between animal and plant proteins in mixed systems are still rare. This paper reviews the recent studies related to animal and plant protein mixed systems, highlighting the impacts of the applied treatments on protein structure and technofunctional properties. The following section is divided into three major topics: (i) co-aggregation, (ii) gel and film formation and (iii) interfacial behavior (stabilization of emulsions and foams). Although the two first topics approach correlated phenomena, the co-aggregation topic will focus on given insights on the behavior at the molecular level of the mixed systems. The gel and film formation topic will mostly discuss the microstructure and macroscopic behavior of these systems. Table 2 summarizes the studies focused on techno-functional properties of animal and plant proteins in mixed systems. 3.1. Co-aggregation The aggregation of proteins is partly dictated by factors linked to the protein itself, such as: structure, molecular weight and reactivity (presence of free thiol groups for instance) (Lin et al., 2017). The reactional conditions that include protein concentration, presence of other molecules, pH and ionic strength (which have great impact on protein charge and solubility) also play an important role in protein aggregation (Lin et al., 2017). Uncontrolled protein aggregation may have undesirable consequences on food texture. Nevertheless, the modulation of the form, size, and solubility of protein aggregates allows the development of innovative applications, like texture modifier ingredients and encapsulating agents (Sobhaninia, Nasirpour, Shahedi, Golkar, & Desobry, 2018; Ustunol, 2014). Apart from specific cases, for 3

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Table 2 Compilation of the studies concerning techno-functional properties of animal and plant protein mixed systems. Properties

Animal Protein

Plant Protein

References

Co-aggregation

Whey proteins

Soy proteins

β-Lg

Glycinin (11S) Pea proteins

Roesch and Corredig (2005) Jose, Pouvreau, and Martin (2016) Anuradha and Prakash (2009) Chihi et al. (2016) Mession et al. (2017b) Roesch, Juneja, Monagle, and Corredig (2004) Roesch and Corredig (2006) Lin, Hill, and Corredig (2012) Grygorczyk, Alexander, and Corredig (2013) Comfort and Howell (2002) Roesch and Corredig (2005) Jose et al. (2016) McCann, Guyon, Fischer, and Day (2018) Beliciu and Moraru (2011) Beliciu and Moraru (2013) Silva, Balakrishnan, Schmitt, Chassenieux, and Nicolai (2018) Silva et al. (2019b) Silva et al. (2019a) Mession et al. (2017a) Silva et al. (2018) Silva et al. (2019b) Silva et al. (2019a) Chihi, Sok, and Saurel (2018) Tomé et al. (2015) Denavi et al. (2009) Cao, Fu, and He (2007) Oechsle et al. (2016) Oechsle et al. (2016) Wouters et al. (2017) Pizones Ruiz-Henestrosa et al. (2014) Tomé et al. (2015)

Gelling and film formation

Caseins Milk proteins (Casein micelles + whey proteins)

Soy proteins

Whey proteins

Caseins

Pea proteins

Foaming and emulsifying

β-Lg Cape Hake sawdust proteins Collagen/Gelatin

Soy proteins

Egg White proteins β-Lg Cape Hake sawdust proteins

Gluten Gluten Soy proteins Pea proteins

increase in the size of the formed soluble aggregates by raising the ionic strength to 300 mM (Jose et al., 2016). The effect of ionic strength on the size of the aggregates was more pronounced for mixtures containing high proportions of WPI. It is worth noting that Roesch and Corredig (2005) used SPC in their experiments while Jose et al. (2016) used SPI obtained at lab-scale from soy flour. The difference in composition between these products (higher content of carbohydrates of SPC, for instance) and their processing history could help to explain the differences reported by these authors. Concerning the thermal aggregation of mixtures of β-Lg and Glycinin (11S), an increase in the soluble protein content after heat treatment was observed after the β-Lg:Glycinin ratio was raised (Anuradha & Prakash, 2009). In this case, it is hard to dissociate the effects of protein ratio and total protein content on the results, because both simultaneously changed during experiments. These authors heattreated β-Lg:Glycinin mixtures at weight ratios varying from approximately 1:1 to 1:2, at pH 7.9 and total protein content between 0.3 and 0.5%. During the study, it was observed that thermal aggregation was induced only at temperatures above 65 °C (Anuradha & Prakash, 2009). Disulfide bridges and hydrophobic interactions also seemed to participate on the stabilization of β-Lg and Glycinin aggregates obtained during this study. The increase in the proportion of β-Lg in a mixture with pea proteins, also resulted in a reduction of the size of the soluble aggregates obtained after heat treatment, at a constant total protein concentration (2%) (Chihi et al., 2016). Chihi et al. (2016) hypothesized that thermal aggregation between these proteins in a mixture is triggered by the denaturation of β-Lg. Unfolded β-Lg forms disulfide bridge stabilized complexes with legumin (11S) subunits released during the heat treatment. These complexes then interact through non-covalent bounds with other pea globulins (legumin and vicilin) forming soluble aggregates of about 90–110 nm, which were smaller than those formed by pea globulins heat treated in absence of β-Lg (Chihi et al., 2016). In

example, electrostatic driven protein aggregation, the aggregation of proteins is usually induced by external triggers like thermal treatments, enzymatic hydrolysis and/or high-pressure treatments (Chi, Krishnan, Randolph, & Carpenter, 2003; Ustunol, 2014; Wang, Nema, & Teagarden, 2010). So far, very few studies have focused on the characterization of aggregates obtained in animal and plant protein mixed systems. In all these studies the pH was set at neutral or slightly alkaline conditions (between 7.0 and 7.9), the ionic strength was variable but ranged from 5 to 300 mM and protein aggregation was systematically induced by heat-treatment, using temperatures between 60 and 95 °C for 10–60 min. Roesch and Corredig (2005) characterized the formation of soluble and insoluble aggregates during the heating (90 °C) of mixtures of soy and whey proteins. These mixtures contained different proportions of soy protein concentrate (SPC) and WPI, at the total protein content of 1.4%. These authors demonstrated the formation of complexes between whey and soy proteins stabilized by disulfide bridges, and also by noncovalent interactions. In the mixture containing a higher proportion of soy proteins (70 SPC:30 WPI), the formation of high molecular weight soluble aggregates was observed (Roesch & Corredig, 2005). However, in the mixture with a higher proportion of whey proteins (30 SPC:70 WPI), the heat treatment induced mainly the formation of insoluble aggregates predominantly formed by β-Lg, β-Conglycinin (7S) and the basic subunits of Glycinin (11S). On the other hand, no insoluble aggregates were found by Jose et al. (2016) after the heat treatment (95 °C for 60 min) of soy protein isolate (SPI) and WPI mixtures at different ratios. These mixtures contained a total protein concentration of 1%, pH and ionic strength (7.0 and 100 mM) were under the same conditions of the former study. Under the described conditions, the authors reported aggregates of around 65 nm of hydrodynamic diameter for the SPI:WPI ratio of 10:90. The aggregates reduced slightly in size when the soy protein proportion was increased. These authors also reported an

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contrast to β-Lg, which co-aggregated with pea proteins, CMs modified the aggregation kinetics of pea proteins mainly by stabilizing them against thermal denaturation (Mession et al., 2017b). The denaturation temperature of legumin (11S) and vicilin (7S) increased 4 °C when mixed with CMs (Mession et al., 2017b). 3.2. Gelling and film formation Gels or films can be made when the protein concentration is high enough to generate a tridimensional network. This network is stabilized by disulfide bridges and/or non-covalent interactions after protein unfolding, otherwise, protein aggregates are observed. Apart from protein concentration, other reactional parameters affecting the exposure of previously buried reactive patches are relevant on network development. The presence and nature of proteins and other molecules, pH, ionic strength and temperature are examples of such parameters (Foegeding & Davis, 2011; Singh, 2016; Yada, 2018). The rheological properties of gels and films are directly related to their microstructure. Therefore, by mixing animal and plant proteins it is possible to obtain gels and/or films displaying various microstructures and by consequence displaying different rheological behavior. Comfort and Howell (2002) characterized the microstructure of heat-induced gels (90 °C) made of soy protein isolate (SPI) and WPI; alone and at different weight ratios, while maintaining the total protein content at 18%. The authors observed that depending on the protein weight ratios, the proteins from one of the sources formed a continuous network, excluding the proteins from the other one. At high soy protein concentration, these proteins formed a continuous phase segregating the whey proteins. However, a phase inversion was reported with increasing whey protein concentration, and then, whey proteins were responsible for the gel network. The critical ratio for phase inversion was approximately 85:15 (SPI:WPI), where unstable gels highly susceptible to syneresis were obtained. At this critical ratio, the gel network was formed by soy proteins, nevertheless SPI concentration was not enough to completely segregate the whey proteins, that, in their turn, negatively affected the network formation (Comfort & Howell, 2002). The observed behavior was attributed to the differences of molecular weight, superficial hydrophobicity, affinity to water and denaturation kinetics between the proteins from these two groups (Comfort & Howell, 2002). Contrasting results were reported by Roesch and Corredig (2005) which did not observe apparent phase segregation in heat-induced gels (90 °C) containing SPC and WPI at 6% total protein content. At this concentration, gelation was driven by whey proteins, since at high soy protein proportion (90:10 - SPC:WPI) gelation was not achieved. Although no phase segregation was reported, when the concentration of soy protein was higher than the concentration of whey protein (70:30 -SPC:WPI), two steps of network development were observed: whey proteins formed aggregates between themselves and/or with soy proteins during heating phase, followed by the aggregation of residual soy proteins during cooling phase (Roesch & Corredig, 2005). The gel microstructure became more inhomogeneous with the increase of the concentration of soy proteins (Fig. 1 A, B, C). By varying the total protein concentration, besides the proportions of soy and whey proteins in heat-induced gels (95 °C), it was found that whey proteins formed a primary network structure responsible for gel strength and soy proteins acted as fillers of the formed network (McCann et al., 2018). This result goes in the same direction as those found by Roesch and Corredig (2005). This hypothesis is endorsed by the fact that gels presenting total protein concentration of 6%, 12%, and 16%, and SPI:WPI ratios of (0:100), (50:50) and (70:30) respectively, had similar strengths (McCann et al., 2018). Even with the similar strength of the different gels, their microstructures were distinctly different (Fig. 1 D, E, F), which opens the possibility to develop rich protein systems displaying different mechanical properties (McCann et al., 2018). In addition to protein concentration and the ratio between different

Fig. 1. Confocal laser scanning micrographs of heat induced gels formed by different animal and plant protein mixed systems. (A to C) Heat induced gels (90 °C/1 h) of soy proteins and whey proteins at neutral pH, total protein concentration of 6% w/w and SPC:WPI ratios of 0:100 (A), 50:50 (B) and 70:30 (C) (Adapted from Roesch and Corredig (2005)). (D to F) Heat induced gels (95 °C/ < 1 h) of soy proteins and whey proteins at neutral pH, total protein concentration of 12% w/w and SPI: WPI ratios of 0:100 (D), 50:50 (E) and 100:0 (F) (Adapted from McCann et al. (2018)). (G to I) Heat induced gels (95 °C/30min) of soy proteins and whey proteins at neutral pH, 100 mM of ionic strength, total protein concentration of 10% w/w and SPI:WPI ratios of 0:100 (G), 50:50 (H) and 100:0 (I) (Adapted from Jose et al. (2016)). (J to L) Heat induced gels (90 °C/1 h) of soy proteins and casein micelles (CM) at pH 5.8, total protein concentration of 6% w/w and SPI:CM ratios of 0:100 (J), 50:50 (K) and 100:0 (L) (Adapted from Silva et al. (2019b)).

proteins, the ionic strength has also been reported as an important parameter modulating the microstructure of gels obtained from whey and soy proteins mixtures. Jose et al. (2016) studied heat induced gels (90 °C for 60 min) resulting from SPI and WPI mixed at different ratios. The gels were formed under a constant total proteins content of 10%, at pH 7.0 and ionic strength of 100 mM and 300 mM. These authors observed that for both ionic strengths, the coarseness of the gels decreased by increasing the SPI proportion (Fig. 1 G, H, I – gel at 100 mM of ionic strength). However, at the same SPI:WPI ratio, the increase in ionic strength resulted in an increase of coarseness of the gel (Jose et al., 5

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conditions the CMs were responsible in forming the gel network. The formation of CM-whey protein complexes induced by heat treatment increased the gel strength, independent from soy proteins (Roesch & Corredig, 2006). A gel network structured predominantly by CMs was also obtained when the content of soy proteins was increased to around 2.7% (Roesch et al., 2004). In this study, the content of milk protein was also reduced (around 2.4%, CM:whey protein ratio around 80:20), the heat treatment was less intense (78 °C for 30 min) and the final pH of the mixture was 5.0 (Roesch et al., 2004). However, in this case, soy proteins had a small part in the gel network and that these proteins were responsible for increasing the onset pH of gelation (Roesch et al., 2004). On the other hand, when acidification reached a higher final pH of 5.5 (using GDL), mixtures of 2.0% of soy proteins (heat treated at 100 °C for 7 min) and 1.4% of milk proteins (CM:whey proteins ratio around 80:20) gels structured mainly by soy proteins were formed (Lin et al., 2012). However, with the addition of rennet to the mixture, CMs were successfully incorporated in the gel network. Despite this, a small extension of κ-casein hydrolysis by rennet reflected a minor impact on gel rheology, with gels displaying a higher elastic modulus being obtained after a large extension of κ-casein hydrolysis (Grygorczyk et al., 2013; Lin et al., 2012). Heat-induced gels were also obtained by treatment at 90 °C for 30 min, with mixtures of pea proteins (PEA) and alkaline extracted proteins from cape hake sawdust (HPP) in different proportions and a total protein content of 20% (Tomé et al., 2015). During heating, the gel network was promptly formed by the HPP and posteriorly reinforced by PEA. Thus, by increasing the HPP proportion, stronger and more structured gels were obtained (Tomé et al., 2015). On the other hand, Mession et al. (2017a) characterized the gelation during acidification (from pH 7.1 to 4.2) of lab-extracted PEA or its isolated fractions vicilin (7S) or legumin (11S) combined with CMs. These authors produced mixed systems at 3.6% total protein content, respecting equal mass ratios between the proteins. To produce the gels, PEA or its fractions were treated at 85 °C for 60 min combined with CMs or alone. In this last case the CMs were added to the treated dispersion after cooling. Acidification was performed by adding enough GDL to reduce the pH to 4.2 after 24 h (Mession et al., 2017a). Vicilin (7S) thermal-induced aggregates obtained in the presence or absence of CMs improved gelling properties of the mixture. Pre-aggregation of vicilin (7S) prompted an early beginning of network formation (pH around 6.8) compared to the system where CMs and vicilin (7S) were heattreated together (pH around 6.4). Thermal aggregation of legumin (11S) in the presence or absence of CMs did not improve the properties of the acidic gel obtained. PEA heat treated in the presence of CMs showed behavior close to the one observed for legumin (11S), while it was closer to vicilin (7S) behavior when heat-treated in the absence of CMs (Mession et al., 2017a). In complement, the acidic gelation of heat induced β-LG-PEA co-aggregates was investigated by Chihi et al. (2018). These authors heat treated (85 °C for 60 min) mixtures of β-LG and PEA at several mass ratios, pH 7.0 and 4% of total protein content, to obtain co-aggregates. The characterization of the co-aggregates was described by Chihi et al. (2016) and discussed in the last paragraph of the “Co-aggregation” topic of these review. The obtained co-aggregates were induced to gelation by acidification (using GDL) to reach the final pH of 4.5 after 24 h. The formed gels were compared to control gels achieved from the acidification of the mixture of aggregates formed by the heat treatment of each protein source separately (β-LG or PEA) (Chihi et al., 2018). Gels from the co-aggregates were more elastic, displayed a higher water holding capacity and a more entangled microstructure compared to the control gels (Chihi et al., 2018). Regardless of the synergic effect of mixed protein systems on the gelling properties discussed above, the same was not necessarily observed for composite films. By increasing the ratio of soy proteins on composite films with bovine type B gelatin, their tensile strength, elongation to break, elastic modulus, swelling capacity, and transparency decreased (Cao et al., 2007). However small amounts of soy

2016). The differences on the microstructure of the gels obtained by Jose et al. (2016) compared to those obtained by Roesch and Corredig (2005) and McCann et al. (2018) is probably related to the less intense processing history of the soy proteins used by Jose et al. (2016) (Fig. 1 A to I). The processing history of the proteins appears as an important, but often neglected, parameter dictating the behavior of protein mixed systems. In contrast to the behavior of whey and soy protein mixed systems, heat-induced neutral gels of soy proteins mixed with CMs were primarily structured by a soy proteins network. CMs mixed with SPI at the equal mass ratio and total protein concentration between 7.5 and 12.5% exhibited local phase separation of CMs and unfolded soy proteins after heat-treatment above 80 °C (Beliciu & Moraru, 2011). Rheological properties of these mixed systems were closer to the behaviors of only SPI than to one of only CMs. At 15% of total protein content, CMs physically prevent a strong network formation even after heat treatment at 90 °C (Beliciu & Moraru, 2011), although gelation was observed after heat treatment at 95 °C, which is above of the glycinin (11S) denaturation temperature (93.6 °C) (Beliciu & Moraru, 2013). It is important to consider that Beliciu and Moraru (2011) and Beliciu and Moraru (2013) worked at pH close to neutrality (around 6.8), where CMs alone do not form gels when submitted to temperatures below to 100 °C. Taking this into consideration, Silva et al. (2019b) characterized the thermal gelation of CMs and SPI mixed systems at several protein ratios. The authors heated dispersions from 20 °C to 90 °C at 5 °C min−1, in a slightly acidic pH (5.8–6.0) and with total protein concentrations varying between 4 and 8% w/w. They observed that at pH 5.8 the critical gelation temperature of CMs suspension absent of soy proteins was approximately 47 °C and 30 °C for total protein concentration of 4 and 8% w/w respectively (Silva et al., 2019b). In mixed systems, the increase of SPI proportion led to an increase of the critical gelation temperature. For instance, at CMs:SPI ratio of 60:40 the critical gelation temperature at pH 5.8 was around 85 °C and 75 °C for a total protein concentration of 4 and 8% w/w respectively (Silva et al., 2019b). This research group also demonstrated, that the calcium binding ability of soy proteins decreases calcium availability to bind CMs during gelation, thus increasing the critical gelation temperature (Silva et al., 2018). No evidence of co-aggregation between the CMs and the soy proteins in the mixed systems was found, even after heat treatment at 90 °C during 1 h. Hence, CMs and soy proteins form individual networks in mixed systems. This results in a decrease of the rigidity of the heat induced gel (90 °C/60 min) formed by mixed systems compared to non-mixed systems at equal protein concentration (Silva et al., 2019b). A more inhomogeneous network was also reported to gels formed by mixed systems (Fig. 1 J, K, L). Similar results were found for mixed systems between CMs and pea proteins (Silva et al., 2018, 2019b). This research group successfully used these previously characterized mixed systems to produce gelled emulsions that have similar gel stiffness to those produced using mixtures of CM and whey proteins (Silva et al., 2019a). The reported results demonstrate the potential of soy and pea proteins to replace whey proteins in dairy products such as dessert creams. Fig. 2 shows a schematic compilation of the thermal gelation mechanism of soy proteins in mixed systems with whey proteins or casein micelles. Focusing on understanding gelation in more complex mixed systems, Corredig's research group studied: (i) acidic gelation using glucone-δ-lactone (GDL) of heat treated mixtures containing CMs, whey proteins and soy proteins (Roesch & Corredig, 2006; Roesch et al., 2004) and (ii) gels induced by acidification using GDL combined with rennet action (variable amount) of mixtures of heat treated soy milk and reconstituted skim milk (Grygorczyk et al., 2013; Lin et al., 2012). Acidification using GDL (final of pH 4.6) of heat treated (90 °C for 10 min) mixtures of native CMs (around 2.7%), whey proteins (0.42%) and soy proteins (0.18%) induced gel formation. The resulting gels had a similar elastic modulus of gels obtained when soy proteins were suppressed from the mixture (Roesch & Corredig, 2006). Under these 6

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Fig. 2. Schematic diagram of gelling mechanism of soy proteins (SP) in mixed systems with whey proteins (WP) or casein micelles (CMs). HT: Heating Treatment, TPC: Total Protein Content.

proteins did not dramatically affect film properties and reduced its production cost (Cao et al., 2007). Comparable results were reported for composite films of soy proteins and cod gelatin by Denavi et al. (2009). Although a reduction in translucence of films was observed by increasing the proportion of soy proteins, it promoted a higher barrier effect against water-vapor and an increase in breaking resistance. Weaker films were also obtained by partially replacing bovine collagen by soy proteins or gluten, which have been proposed as a viable alternative to modulate sensorial attributes of sausages, such as bite resistance (Oechsle et al., 2016).

structured by gluten hydrolyzed (by trypsin or pepsin) (GH) and egg white protein powder (EW), either isolated or in mixed systems at different proportions. Isolated GH showed higher foam ability than EW, whereas the foam formed by EW was more stable than the one formed by GH. Replacing around 15% of EW by GH, the mixed system showed a foaming capacity similar to or higher than for GH alone. These authors pointed out that in mixed systems, EW formed a second layer by electrostatic and hydrophobic interactions after adsorption of GH at the interface. This phenomenon increased the resistance of the foam bubbles against coalescence (Wouters et al., 2017). Synergic effects on the foam ability was also reported for β-conglycinin (7S) and β-Lg (Pizones Ruiz-Henestrosa et al., 2014). More stable and denser foam formed by small bubbles was obtained by β-conglycinin (7S) and β-Lg in mixture (50:50) compared to the isolated proteins, as shown in Fig. 3. The total protein content was fixed at 0.1% and the pH of the dispersions was 7.0. Under this condition, the interaction between these proteins in solution led to the formation of a more viscoelastic film at the air/water interface (Pizones Ruiz-Henestrosa et al., 2014). No significant effect was observed for this mixed system at pH 3.0, nevertheless, the antagonistic effect on foam ability was reported for glycinin (11S) and β-Lg at this pH (Pizones Ruiz-Henestrosa et al., 2014). PEA in mixture with alkaline extracted proteins from HPP also demonstrated synergism in the stabilization of oil-in-water emulsions (Tomé et al., 2015). Emulsions were prepared at pH 3.8 and 7.0 by mixing 65% (w/w) of vegetable oil, 32% (w/w) of water and 3% (w/w)

3.3. Foaming and emulsifying properties Due to their amphiphilic nature and ability to adsorb to polar/nonpolar interfaces forming stable films, proteins are widely used as a foaming and emulsifying agents in the food industry. To reduce the surface tension at an interface, proteins reorient their hydrophilic moieties towards the aqueous phase and the hydrophobic ones towards the oil phase in the case for emulsions or the gas phase in foams. Thus, the size and flexibility of the proteins are major parameters concerning their interfacial activity (Foegeding & Davis, 2011; Stone, Wang, Tulbek, & Nickerson, 2018; Yada, 2018). In this context, some research groups have focused on tracking synergic effects of animal and plant protein mixed systems for stabilizing emulsions and foams. Wouters et al. (2017) studied the formation and stability of foam 7

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Fig. 3. Evolution of size of air bubbles in foams stabilized by β-Lg, soy β-Conglycinin (7S) and a mixture containing equal mass proportion of both proteins. Foams were obtained by bubbling nitrogen (45 mL/s) in 25 mL of protein dispersions at pH 7.0, 20 °C and total protein content of 1 g L−1. Bubbling was stopped when foams reached the volume of 120 mL, that corresponds to t = 0. Adapted from (Pizones; Ruiz-Henestrosa et al., 2014).

Fig. 4. Schematic diagram that summarize the major parameters concerning animal and plant proteins in mixed systems and their synergic techno-functionalities.

of research groups. In view of the consequences of excessive consumption of animal proteins on sustainable development, the partial replacement with plant proteins in formulated foods and in food ingredients appears as a viable alternative. Coupled with this, such alternatives meet the demands of emerging consumer groups that consciously choose to reduce their consumption of animal proteins (e.g. flexitarians). Most of the studies covered by this review focused on the understanding of the mechanisms behind the behavior of animal and plant proteins in mixed systems, overlooking the technological applications of these mixed systems in final products. Nevertheless, this review highlights several insights that may be very useful in the development of innovative products, based on the mixtures of animal and plant

of protein respecting different proportions of PEA:HPP. Maximum firmness for the emulsions was observed at pH 7.0 at PEA:HPP proportions of (50:50) and (20:80), confirming the synergism of the mixture. Better synergic effects were found at pH 7.0 compared to pH 3.8, probably because at pH 3.8 the interaction between the different proteins was minimized by the proximity of the isoelectric point of PEA, which is 4.5 (Tomé et al., 2015). 4. Concluding remarks and unanswered questions Mixing animal and plant proteins to track synergistic effects is a relatively new approach in Food Science. The current review compiled the initial steps in this field that has been attracting a growing number 8

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proteins. These include, the possibility to (i) control the size of thermoinduced protein aggregates, (ii) increase the total protein content of gels, without considerable rheological changes, and (iii) reduce raw material costs for the production of edible films with little impact on their properties. Fig. 4 summarizes the major relevant parameters for studies concerning animal and plant protein mixed systems, as well as the major techno-functional synergic effects reviewed by this paper. There is an evident imbalance concerning the proteins used in mixed system studies. In these studies, dairy proteins are the most commonly used animal protein source while, soybean and pea proteins stand out as plant sources. In this context, there is much to be done to cover other protein sources used by food industries. It is worth noting that none of the studies treated in this review have focused on rice proteins. These proteins are growing in industrial importance due to their low allergenicity, high nutritional value, relative low costs of production and varied applications. These include, for example, production of alternative infant formulas and gluten-free products. Such discussion also points the gap in knowledge on the characterization of mixed protein systems, between traditional animal or plant proteins and proteins extracted from emerging sources, like seaweed and insects, for instance. The behavior of the animal and plant protein mixed systems is recurrently characterized during and/or after heat treatments. In general, heat treatments are used to induce structural changes in proteins leading to interactions between them at the molecular level. In this context, the application of emerging technologies, such as high-pressure and ultrasound treatments to improve techno-functional properties of mixed protein systems, remains a new perspective and an opportunity for innovation. After all, such emergent treatments have been shown to be effective in modulating the techno-functional properties of proteins from single sources. Could the same be observed for mixtures of proteins from different sources? Another equally important and unanswered question is: what is the behavior of animal and plant protein mixed systems during digestion? Understanding how the kinetics of protein digestion in isolated systems is different from mixed systems is crucial, in regards to the development of products of high biological and nutritional value. This remains a growing scientific field with several unanswered questions which represent an opportunity for the development of interesting research.

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