Biomimetic plant foods: Structural design and functionality

Abstract Background The rising number of people living with chronic conditions, such as diabetes and cardiovascular disease, along with the widespread demand for healthier foods have posed significant challenges to the food industry. Plant-based foods, beyond simple nutrition, can provide health-benefiting functionalities within the complex environment of the human gastrointestinal (GI) tract. Biomimetics is defined as taking inspirations from nature to solve problems. Biomimetic plant foods (BPFs) can offer solutions for the future with the design of nature-inspired food structures for improved health and well-being. Scope and approach This review provides an insight into the assembly of plant food structures and their disassembly in the human GI tract. Their role in controlling the digestive fate of nutrients is elucidated. Recent developments and future perspectives on designing BPFs are also presented and discussed. Key findings and conclusions Plant foods in nature possess hierarchically self-assembled structures. During processing and GI digestion, these structures are disassembled to enable liberation and assimilation of nutrients and bioactive molecules contained within the food matrix. The assembly and disassembly are linked to a hierarchy of structure in plants within which different levels (molecule, polymer, cell wall, cell, tissue, organ) and their interactions can modulate nutrient bioaccessibility and digestion. Inspired by nature, BPFs can be engineered to deliver in-body functionality. The emerging trend of biomimetics will potentially pave the way for the future of food.

[1]  Mariam B. Sticklen,et al.  Plant genetic engineering for biofuel production: towards affordable cellulosic ethanol , 2008, Nature Reviews Genetics.

[2]  B. Hamaker,et al.  Preload of slowly digestible carbohydrate microspheres decreases gastric emptying rate of subsequent meal in humans. , 2017, Nutrition research.

[3]  M. Wahlqvist.  Food structure is critical for optimal health. , 2016, Food & function.

[4]  P. Kuchel,et al.  Digestion of starch: In vivo and in vitro kinetic models used to characterise oligosaccharide or glucose release , 2010 .

[5]  Keith W Waldron,et al.  Role of cell walls in the bioaccessibility of lipids in almond seeds. , 2004, The American journal of clinical nutrition.

[6]  K. Duodu,et al.  Influence of Cooking Conditions on the Protein Matrix of Sorghum and Maize Endosperm Flours , 2008 .

[7]  S. Alavi,et al.  Sorghum proteins: the concentration, isolation, modification, and food applications of kafirins. , 2010, Journal of food science.

[8]  N. Ferté,et al.  Oil-bodies as substrates for lipolytic enzymes. , 2001, Biochimica et biophysica acta.

[9]  A. Clemente,et al.  Factors affecting the in vitro protein digestibility of chickpea albumins , 2000 .

[10]  A. Enejder,et al.  Effects of thermal processing on the in vitro bioaccessibility and microstructure of β-carotene in orange-fleshed sweet potato. , 2010, Journal of agricultural and food chemistry.

[11]  J. Tzen,et al.  Constitution of stable artificial oil bodies with triacylglycerol, phospholipid, and caleosin. , 2004, Journal of agricultural and food chemistry.

[12]  L. Thompson,et al.  Factors affecting starch digestibility and the glycemic response with special reference to legumes. , 1983, The American journal of clinical nutrition.

[13]  E. Vanstreels,et al.  Mechanical characteristics of artificial cell walls , 2010 .

[14]  Yulong Yin,et al.  The physicochemical properties and in vitro digestibility of selected cereals, tubers and legumes grown in China , 2006 .

[15]  Robert G. Gilbert,et al.  Effect of particle size on kinetics of starch digestion in milled barley and sorghum grains by porcine alpha-amylase , 2009 .

[16]  Harjinder Singh,et al.  Behavior of almond oil bodies during in vitro gastric and intestinal digestion. , 2012, Food & function.

[17]  B. Bouchet,et al.  Digestion of carbohydrate from white beans (Phaseolus vulgaris L.) in healthy humans. , 1998, The Journal of nutrition.

[18]  B. Hamaker,et al.  Resistance of Sorghum .alpha.-, .beta.-, and .gamma.-Kafirins to Pepsin Digestion , 1995 .

[19]  Jin Gu,et al.  Impact of hemicelluloses and pectin on sphere-like bacterial cellulose assembly , 2012 .

[20]  G. Bornhorst,et al.  Gastric digestion in vivo and in vitro: how the structural aspects of food influence the digestion process. , 2014, Annual review of food science and technology.

[21]  Bharat Bhushan,et al.  Biomimetics: lessons from nature–an overview , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[22]  S. Shojaosadati,et al.  Bacterial nanocellulose-pectin bionanocomposites as prebiotics against drying and gastrointestinal condition. , 2016, International journal of biological macromolecules.

[23]  Michael J Gidley,et al.  Heterogeneity in the chemistry, structure and function of plant cell walls. , 2010, Nature chemical biology.

[24]  K. Duodu,et al.  Effects of endosperm texture and cooking conditions on the in vitro starch digestibility of sorghum and maize flours , 2005 .

[25]  S. Gaisford,et al.  A study of starch gelatinisation behaviour in hydrothermally-processed plant food tissues and implications for in vitro digestibility. , 2015, Food & function.

[26]  J. Aguilera,et al.  Food microstructure affects the bioavailability of several nutrients. , 2007, Journal of food science.

[27]  J. Tovar,et al.  Cell walls limit in vitro protein digestibility in processed legume seeds , 1995 .

[28]  J. Tzen.  Integral Proteins in Plant Oil Bodies , 2012 .

[29]  M. Gidley,et al.  Effect of carrot (Daucus carota) microstructure on carotene bioaccessibility in the upper gastrointestinal tract. 2. In vivo digestions. , 2010, Journal of agricultural and food chemistry.

[30]  M. Jarvis,et al.  Intercellular adhesion and cell separation in plants , 2003 .

[31]  D. Barreca,et al.  The effects of processing and mastication on almond lipid bioaccessibility using novel methods of in vitro digestion modelling and micro-structural analysis. , 2014, The British journal of nutrition.

[32]  B. Hamaker,et al.  Starch-Entrapped Biopolymer Microspheres as a Novel Approach to Vary Blood Glucose Profiles , 2009, Journal of the American College of Nutrition.

[33]  M. Gidley,et al.  Composition and structure of tuber cell walls affect in vitro digestibility of potato (Solanum tuberosum L.). , 2016, Food & function.

[34]  I. Fisk,et al.  In vitro assessment of the bioaccessibility of tocopherol and fatty acids from sunflower seed oil bodies. , 2009, Journal of agricultural and food chemistry.

[35]  H. Adlercreutz,et al.  Physical, microscopic and chemical characterisation of industrial rye and wheat brans from the Nordic countries , 2009, Food & nutrition research.

[36]  P. Butterworth,et al.  The role of plant cell wall encapsulation and porosity in regulating lipolysis during the digestion of almond seeds. , 2016, Food & function.

[37]  D. Mcclements,et al.  Controlling Lipid Bioavailability through Physicochemical and Structural Approaches , 2008, Critical reviews in food science and nutrition.

[38]  A. C. Smith,et al.  Pectin distribution at the surface of potato parenchyma cells in relation to cell-cell adhesion. , 2001, Journal of agricultural and food chemistry.

[39]  Suman Mishra,et al.  Effects of simulated digestion in vitro on cell wall polysaccharides from kiwifruit (Actinidia spp.) , 2012 .

[40]  M. Bonn,et al.  The role of intact oleosin for stabilization and function of oleosomes. , 2013, The journal of physical chemistry. B.

[41]  José Miguel Aguilera,et al.  Microstructural principles of food processing and engineering , 1999 .

[42]  D J Cosgrove,et al.  Assembly and enlargement of the primary cell wall in plants. , 1997, Annual review of cell and developmental biology.

[43]  Peter Fratzl,et al.  Biomimetic materials research: what can we really learn from nature's structural materials? , 2007, Journal of The Royal Society Interface.

[44]  Y. Ogawa,et al.  Impact of structural characteristics on starch digestibility of cooked rice. , 2016, Food chemistry.

[45]  L. Gibson.  The hierarchical structure and mechanics of plant materials , 2012, Journal of The Royal Society Interface.

[46]  Genyi Zhang,et al.  Slow digestion property of microencapsulated normal corn starch , 2014 .

[47]  Harjinder Singh,et al.  The physical and chemical structure of lipids in relation to digestion and absorption , 2012 .

[48]  E. Capuano.  The behavior of dietary fiber in the gastrointestinal tract determines its physiological effect , 2017, Critical reviews in food science and nutrition.

[49]  L. Kaur,et al.  Starch digestibility in food matrix: a review , 2010 .

[50]  B. Hamaker,et al.  Biophysical features of cereal endosperm that decrease starch digestibility. , 2017, Carbohydrate polymers.

[51]  M. Gidley,et al.  Complexity and health functionality of plant cell wall fibers from fruits and vegetables , 2017, Critical reviews in food science and nutrition.

[52]  P. Ellis,et al.  Manipulation of lipid bioaccessibility of almonds influences postprandial lipemia in healthy human subjects , 2008, The American journal of clinical nutrition.

[53]  P. Butterworth,et al.  Impact of cell wall encapsulation of almonds on in vitro duodenal lipolysis , 2015, Food chemistry.

[54]  Y. Brummer,et al.  Structural and functional characteristics of dietary fibre in beans, lentils, peas and chickpeas , 2015 .

[55]  A. Darke,et al.  In vitro assembly of cellulose/xyloglucan networks: ultrastructural and molecular aspects , 1995 .

[56]  A. Keshavarzian,et al.  Starch-entrapped microsphere fibers improve bowel habit but do not exhibit prebiotic capacity in those with unsatisfactory bowel habits: a phase I, randomized, double-blind, controlled human trial. , 2017, Nutrition research.

[57]  S. Tosh.  Review of human studies investigating the post-prandial blood-glucose lowering ability of oat and barley food products , 2013, European Journal of Clinical Nutrition.

[58]  R. Mezzenga,et al.  Food structure and functionality: a soft matter perspective. , 2008, Soft matter.

[59]  A. Logan,et al.  Stabilization of fish oil-in-water emulsions with oleosin extracted from canola meal. , 2013, Journal of food science.

[60]  M. Jarvis,et al.  The textural analysis of cooked potato. 2. Swelling pressure of starch during gelatinisation , 1992, Potato Research.

[61]  J. Tzen,et al.  Size and Stability of Reconstituted Sesame Oil Bodies , 2003, Biotechnology progress.

[62]  M. Gidley,et al.  Digestion of isolated legume cells in a stomach-duodenum model: three mechanisms limit starch and protein hydrolysis. , 2017, Food & function.

[63]  Jaspreet Singh,et al.  The role of cotyledon cell structure during in vitro digestion of starch in navy beans , 2012 .

[64]  G. Macfarlane,et al.  Bacteria, colonic fermentation, and gastrointestinal health. , 2012, Journal of AOAC International.

[65]  P. Belton,et al.  Factors affecting sorghum protein digestibility , 2003 .

[66]  M. Golding,et al.  The influence of emulsion structure and stability on lipid digestion , 2010 .

[67]  L. Etienne-Mesmin,et al.  Relevance and challenges in modeling human gastric and small intestinal digestion. , 2012, Trends in biotechnology.

[68]  I. Delgadillo,et al.  Effect of Grain Structure and Cooking on Sorghum and Maize in vitro Protein Digestibility , 2002 .

[69]  E. Weber,et al.  Protein bodies, storage organelles in plant seeds , 1980 .

[70]  Genyi Zhang,et al.  Nutritional property of starch in a whole-grain-like structural form , 2018 .

[71]  S. Teuber.  Hypothesis: The Protein Body Effect and Other Aspects of Food Matrix Effects , 2002, Annals of the New York Academy of Sciences.

[72]  A. Masclee,et al.  Effect of fat saturation on satiety, hormone release, and food intake. , 2009, The American journal of clinical nutrition.

[73]  Zhiping Shen,et al.  Mimicking natural oil bodies for stabilising oil-in-water food emulsions , 2014 .

[74]  M. Gidley,et al.  Inhibition of α-amylase activity by cellulose: Kinetic analysis and nutritional implications. , 2015, Carbohydrate polymers.

[75]  R. Singh,et al.  Modes of Disintegration of Solid Foods in Simulated Gastric Environment , 2009, Food biophysics.

[76]  B. Larkins,et al.  Structure of maize protein bodies and immunocytochemical localization of zeins , 1988, Protoplasma.

[77]  M. Langton,et al.  Starch Microstructure and Starch Hydrolysis in Barley and Oat Tempe During In Vitro Digestion , 2012 .

[78]  R. Singh,et al.  Gastric emptying rate and chyme characteristics for cooked brown and white rice meals in vivo. , 2013, Journal of the science of food and agriculture.

[79]  M. Gidley,et al.  Intactness of cell wall structure controls the in vitro digestion of starch in legumes. , 2016, Food & function.

[80]  M. Gidley,et al.  Characterisation of soluble and insoluble cell wall fractions from rye, wheat and hull-less barley endosperm flours , 2014 .

[81]  R. Singh,et al.  Digestion of Raw and Roasted Almonds in Simulated Gastric Environment , 2009, Food Biophysics.

[82]  P. Ellis,et al.  A review of the impact of processing on nutrient bioaccessibility and digestion of almonds , 2016, International journal of food science & technology.

[83]  M. Ashby,et al.  Cellular Materials in Nature and Medicine , 2010 .

[84]  C. Edwards,et al.  Re-evaluation of the mechanisms of dietary fibre and implications for macronutrient bioaccessibility, digestion and postprandial metabolism , 2016, The British journal of nutrition.

[85]  M. Jarvis.  Plant cell walls: Supramolecular assemblies , 2011 .

[86]  D. Delmer,et al.  Pea Xyloglucan and Cellulose: VI. Xyloglucan-Cellulose Interactions in Vitro and in Vivo. , 1987, Plant physiology.

[87]  M. Gidley,et al.  Relationships between protein content, starch molecular structure and grain size in barley. , 2017, Carbohydrate polymers.

[88]  V. Fogliano,et al.  A closer look to cell structural barriers affecting starch digestibility in beans. , 2018, Carbohydrate polymers.

[89]  A. C. Smith,et al.  Plant Cell Walls and Food Quality. , 2003, Comprehensive reviews in food science and food safety.

[90]  A. Fardet.  A shift toward a new holistic paradigm will help to preserve and better process grain products' food structure for improving their health effects. , 2015, Food & function.

[91]  M. Gidley,et al.  Effect of carrot (Daucus carota) microstructure on carotene bioaccessibilty in the upper gastrointestinal tract. 1. In vitro simulations of carrot digestion. , 2010, Journal of agricultural and food chemistry.