Plant Cell Walls as Dietary Fibre: Range, Structure, Processing and Function

J Sci Food Agric 1996,70,133-150

Plant Cell Walls as Dietary Fibre: Range, Structure, Processing and Function Gordon J McDougall*, Ian M Morrison, Derek Stewart and John R Hillman Unit for Industrial Crops, Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK (Received 16 March 1995; revised version received 6 July 1995; accepted 30 August 1995)

Abstract: The ingestion of dietary fibre has been correlated with the prevention of many health-threatening diseases and cancers. Plant cell wails are the major source of dietary fibre and this review investigates the relationship between the structure of different types of plant cell walls and their beneficial effects. The effects of processing and cooking on dietary fibre are also examined. Structure- function relationships between individual cell wall components and the beneficial effects of dietary fibre are not well defined and it may be that the physical, physiochemical and topochemical properties of plant cell walls and their components are also important.

Key words: dietary fibre, plant cell walls, health, gastrointestinal tract, structure- benefit relationships, polysaccharides, lignin, food processing.

INTRODUCTION

Of all animals, humans consume the widest range of foods. The diversity of foods consumed by humans is a function of our omnivorous nature, ingenuity, curiosity and processing skills. Cooking allows the consumption and digestion of foods that would be unpalatable in their raw state. Most humans, and especially those in the developed Western countries, are not limited in their choice of foods by their habitat or ecosystem. Unlike the natural fauna, the populations of Western countries have no need to hunt for food; they simply need to shop. The food base has broadened as a result of increased trade and the adoption of technologies for the storage and distribution of seasonal foods on a year-round basis. Changing attitudes to foods, brought about by travel and exposure through advertising and the mass media, have also had an influence on food choice. It is undoubtedly true that the diet of Western societies has become influenced by fashion.

Despite the huge choice of possible foodstuffs and the increasing awareness of the availability of these foods, many local diets are resistant to change and are based on historical, social and economic factors. For example, the diet of Scotland as a whole has been to deemed to

* To whom correspondence should be addressed.

be unhealthy (Anon 1993) and the findings of this report apply equally to much of the UK (Anon 1992). The rate of premature death of adults in Scotland and the rest of the UK is one of the highest in the world. Although other activities such as smoking are implicated, many of the causes and predisposing conditions leading to premature death, such as coronary heart disease, strokes, obesity, high blood pressure and cancers, are linked to nutrition or are exacerbated by an inapprop- riate diet especially one low in dietary fibre (Burkitt and Trowel1 1975). The ingestion of dietary fibre has been shown to have beneficial effects on coronary heart disease, obesity, diabetes, breast cancers, large bowel cancers and other bowel disorders. Therefore, the Scot- tish Health Service Advisory Council has recommended that the average daily intake of dietary fibre should be increased from 10.5 to 16.4 g. This can only be achieved by changes in lifestyles and habits. It is perhaps perti- nent to point out that the word ‘diet’ once referred to ‘mode of living’ before it took on its modern meaning (Anon 1976).

What is dietary fibre? The definition of dietary fibre has caused a great deal of confusion and, indeed, in 1990 the British Nutrition Foundation advocated that its scientific use as a generic term should be avoided. Considering the successful transfer of this pseudo- medical term into popular use, it is not surprising that

133 J Sci Food Agric 0022-5142/96/$09.00 0 1996 SCI. Printed in Great Britain

134 G J McDougall et a1

dietary fibre as a concept has survived. Most experts now define dietary fibre (DF) as that part of foodstuffs which is not digested by the secretions of the human gastrointestinal tract (GIT) (Eastwood 1992). This empirical 'catch-all' definition has evolved from older definitions such as 'unavailable carbohydrate or non- starch polysaccharides' as discussed by Heaton (1990). Despite the confusion in its definition. DF is almost entirely plant derived. Although there are other minor non-plant sources, plant cell walls (PCWs) constitute the major part of DF. Therefore, this review will con- centrate on the range, type, composition, processing, digestion and physiological effects of PCWs as DF. However, the effects of other components such as 'resistant' starch and soluble plant, microbial and algal polysaccharides, which may be added to processed food, will also be included.

THE RANGE, TYPE, SIZE AND DISTRIBUTION OF CELL WALLS IN PLANT

FOODS

PCWs are not uniform. The type, size and shape of cell walls (CWs) is closely linked to the function of the cell

primary cws and Some thick secondary cw layers inside the primary wall (Fig 1). Cells with position of the plasma membrane. Bar-2.5 pm. thickened CWs may have specialised functions is providing rigidity or transporting water in plant tissues and

Fig 1. An electron micrograph displaying primary and sec-

middle lamella; s, secondary cell wall. The arrow denotes the within a plant tissue (Esau, 1977). plant have ondary layers of plant cell walls. p, primary cell wall; m,

TABLE 1 A description of the functions and distribution of the three main cell types in

plants

Cell type' Cell wall type Distributionb Example

Parenchyma (90) Structural Storage Transport

Boundary

Collenchyma (I) Support

Sclerenchyma (9) Conducting

Non-conducting

Primary Primary Modified Primary Specialized Secondary

Thickened Primary

Lignified Secondary 'Lignified'" Secondary

U Pith U U Phloem sieve cell

End o s p e r m

U Endodermis Epidermis

L, s Celery petiole strands

U Xylem

U Sclereids Fibres

Figures in parantheses after the cell types are the estimated proportions of these cell types in the human diet.

U, universal; S, stem; R, root; L, leaves. ' These cells may or may not be lignified.

Plant cell walls as dietary3bre 135

the shape and structure of the CW has implications for its behaviour as DF. Long thin cells with a thick wall and no living contents (eg xylem, phloem, sclereids) will contribute to the physical effects of DF in a different way from a thin-walled cell full of starch grains. In addition, components of a thick wall will be less accessible to digestion than those of a thin wall. Different CWs also have different structures. Therefore, any discussion of DF must recognise the function of the plant tissue ingested, the range of cell types ingested, their function and the structure of their CWs. Figure 2 gives an overview of this holistic approach.

Three main plant cell types are recognised: parenchyma, collenchyma and sclerenchyma (Mauseth 1988). Parenchyma makes up the major part of food plants. Sclerenchyma and collenchyma make up a small proportion of the plant tissue ingested and there are few cases where these tissue types comprise the major part of the foodstuff. Table 1 gives a description of the major properties of these cell types, their function and their distribution in plants.

DF can come from three main sources: vegetables; fruits, nuts and seeds; and non-plant DF sources. Com-

Plant food organ

Tissue type

Parenchyma Sclerenchyma Collenchyma

Xylem Non-xylem C f L rf

Boundary Storage Synthetic \ 4, Transport Specialized cell types

J

J Cell wall types: primary walVmiddle lamella secondary wall

Assembly of Biopolymers into wall matrix (bonds and linkages)

Non-covalent Covalent

Hydrogen bonds Ionic bonds Sugar esterilication Phenolic cross links e.g. cellulosB e g. Ca” bridges e g. pectins a M NCPs e.g. NCPs and lignin and xylcglucan between pectins proteins and iignins

extensin noaslinking

Biopolymers

A / $ - \ Polysaccharides Glycoproteins Polyphenolics

4 4 Cellulose. NCPs. pectins Glycoproteins Suberin, cutin. lignin

4 4 Sugars Amino-acids Phenylpropanoids.

Waxes, Fatty acids

Fig 2. An holistic view of the range, type distribution and structure of cell walls in plant foods.

monly eaten vegetables offer a range of cell types with diverse CW structures. For example, the potato tuber contains a large number of thin-walled storage parenchyma (- 10 pm diameter, wall thickness, 0.1- 0.2 pm) that are filled with starch granules (see Fig 3) but it also contains strands of vascular tissue containing phloem and xylem. Some xylem sclerenchyma cells can be millimetres long and up to 20 pm in diameter with thick secondary CWs that occupy 90% of the cross- sectional area. The skin of a potato is an example of periderm. Periderm consists of epidermal cells and suberised thick-walled cork cells. Apart from the tissue types found in tubers, root vegetables (eg carrots) contain a prominent periderm and specialised tissues like the Casparian strip, which is a suberised/lignified ring of cells which effectively limits water transport through the tissues of the root. Onion bulbs consist of layers of cells each with well-developed outer and inner epidermal walls and so have an elevated content of suberin, waxes and cutin. Leafy vegetables comprise of thin-walled photosynthetic parenchyma mesophyll cells sandwiched between upper and lower epidermal layers. Phloem/xylem elements and sclereids are present particularly in the ribs and veins.

Fig 3. Scanning electron micrograph of potato tuber. Cryo- trimmed, freeze-dried potato tuber viewed by scanning electron microscope. Bar-100 pm. For method, see Williamson

and Duncan (1989).


Fig 4. Fluorescence micrograph of a cross-section of a barley grain stained with Calcofluor, bright areas are rich in

8-glucans. Bar-0.2 mm.

Fruits, nuts and seeds also offer a diversity of cell types and CWs. Fleshy fruits contain a multitude of thin-walled storage parenchyma that contain starch and sugars. The seeds are either eaten and contribute to D F (soft fruit berries, tomato, cucumber, courgettes, etc) or are removed (orchard fruits, oranges, peppers, etc). The flesh (mesocarp) of some orchard fruits may contain elongated and thick-walled sclereids and xylem/phloem elements that radiate from the central seed. The skin, when eaten, brings thickened, suberised, wax-containing and cutin-containing epidermal CWs into the diet. The segmented flesh of citrus fruits (oranges, etc) contain juice sacs full of sugars, vitamins and other nutrients. The segment cases consist of modified epidermal cells whose CWs are rich in suberin, waxes and cutin. Nuts are dry, single-seed fruits which provide mainly thin- walled storage cells containing protein, lipid and starch. Seeds consist of three main parts: the cotyledons, the embryo axis and the reserve tissues. The seeds of dicotyledonous plants have two cotyledons which consist of thin-walled storage parenchyma containing starch, lipid and/or protein. The cotyledons and embryo are surrounded by specialised cell layers, the pericarp and the testa, which can contain thickened, lignified and suberised CWs embedded with waxes, cutin, specialised poly-

saccharides or tannins. Cereal grains are the fruits (caryopses) of monocotyledenous seed plants. They differ from other seed-based structures in that they only have one cotyledon and that the testa and pericarp are fused (Fahn, 1982). These fused layers can be removed intact during processing as cereal brans. The bran of barley (see Fig 4) consists of two epidermal layers, cross cells and the testa, all of which have thick-walled cells that can contain suberin, lignin, cutin and specialised polysaccharides.

Natural non-plant sources of D F include mushrooms which are compacted fungal hyphae. Their CWs contain polymers such as chitin, mannoproteins and p(1-3, 6) linked glucans which all contribute to DF. Retextured fungal biomass, under the brandname ‘Quorn’, is mar- keted as a meat substitute. Small amounts of chitin are present in the diet of those who eat seafood or insects. Certain processed meat products may contain connec- tive tissue and smooth muscle that resist digestion in the GIT.

THE STRUCTURE OF PLANT CELL WALLS

PCWs are extremely complex structures. They are multicomponent composites held together by a plethora of intermolecular bonds (see Fig 2). The component polymers have great structural variety which provide different functional possibilities. CW polysaccharides have the greatest innate potential for structural diversity. Although plant polysaccharides are formed from only 10 common monosaccharides, each monosaccha- ride can exist in two ring (pyranose and furanose) forms, and these residues can be linked through glycosidic bonds at any one of their three, four or five available hydroxyl groups and in two (a or f l ) orientations (Fry 1988). As a result, polysaccharides can adopt a huge number of three-dimensional shapes and thereby offer a vast range of functional surfaces. PCWs can also contain lignin and suberin which provide hydrophobic surfaces. In addition, charged groups on proteins and polysaccharides can affect the ionic properties of the cw.

Complete understanding of the structure of PCWs has still to be achieved. Although the chemical structures of the individual components of CWs have been largely delineated, the relative proportions of these components are less well known. No definitive analysis of the composition of the CW of a single plant cell type has been obtained in which a balance sheet has tallied. Some components are either not estimated or estimated approximately. Therefore, all PCW compositions tend to be generalisations. In addition, the composition of PCWs and the intermolecular bonds between CW components change as a result of growth, development and differentiation of plant tissue. Furthermore, some inter-

Plant cell walls as dietary j b r e 137

molecular bonds have been inferred but not confirmed (Fry 1986).

At the simplest level, PCWs are composites of four main components. These are cellulose, non-cellulosic polysaccharides (NCPs), proteins and polyphenolic compounds. Certain generalisations can be made on the type of polymers found in cereals compared with vegetables. Xyloglucan is a major NCP of vegetables but is found at much lower concentrations in cereals where j?-linked glucans are more important (see Table 2). Although monocotyledenous plants other than cereals are eaten (eg onions), these tend to have primary CW compositions more like the dicotyledenous vegetables than cereals (Fry 1988). The structures of the main components of PCWs are illustrated in Fig 5.

Although cellulose, a p( 1-4) linked homopolymer of D-glucopyranose residues, has a deceptively simple composition, its three-dimensional structure is much more complex (see Franz and Blaschek 1990). Every D- glucose residue is twisted 180" to the next residue so that the true repeating unit is cellobiose. The long ribbon-like chains (up to 15000 residues long) form extensive hydrogen bonds and group together in crystalline microfibrils (30-100 chains in diameter) which form the structural framework of PCWs. Native celluloses differ in their crystallinity; secondary CWs contain highly crystalline cellulose but primary CWs contain more amorphous cellulose.

The NCP have been subdivided into the acidic pectic polysaccharide and the hemicelluloses, mainly composed of neutral sugars. Although superseded (Wilkie 1985), this subdivision can be useful if one notes that pectic polysaccharides are relatively easy to extract from the PCW but the hemicelluloses require more drastic conditions. The pectic polysaccharides are rich in galacturonic acid, rhamnose, arabinose and galactose residues (Brett and Waldron 1988). The main pectic component of vegetable PCWs is rhamnogalacturonan I (RG I) which is interspersed with stretches of unsubstituted a(1-4) linked galacturonic acid (homogalacturonan). Homogalacturonan forms inter-

TABLE 2 A comparison of the composition of primary cell walls of

cereals and vegetables"

Polymer YO Composition (w/w dry wt) ~

Cereals Vegetables

Cellulose 30 30 Pectin 5 35 Arabinoxylan 30 5 Mixed linkage glucan 30 ND Xyloglucan 4 25 Extensin 0.5 5

Adapted from Fry (1988).

chain bonds with Caz+ ions and adopts a highly stable, pseudo-crystalline structure that holds neighbouring chains together (Rees 1982). This interaction allows pectins to form gel-like structures in the wall. RG I chains are substituted with arabinan, galactan and ara- binogalactan sidechains and cannot interact with Ca2+ in this way. The overall structure can be envisaged as 'smooth' homogalacturonan blocks interspersed by 'hairy' RG I blocks. A complex but minor component called rhamnogalacturonan I1 (RG 11) is also present and contains 14 different sugars. Pectins cannot be extracted in a pure form without the use of alkali or polygalacturonanase and this suggests extensive cross- linking through glycosidic linkages or by phenolic cross-links through ferulic acid esterified to pectic components (Fry 1986). The extent of methyl esterification, methoxylation and acetylation differs between sources and this alters the available carboxyl groups which influences the cation exchange capacity and hydro- phocicity of these polysaccharides.

Hemicelluloses are generally extracted from PCWs using alkali following removal of pectins. These polysaccharides have p( 1-4) linked backbones of xylose, mannose or glucose residues that can form extensive hydrogen bonds with cellulose (see Dey and Harboine 1990). Xyloglucan is the major hemicellulose of primary CWs of vegetables; cereals contain much less xyloglucan and, where present, it is less substituted with xylose. Mixed linkage glucans or p(1-3, 4)-glucans are the pre- dominant hemicelluloses in cereals (see Fig 4). A further example of the complexity of PCW structure is that the fine structure of xylans is different depending on their source. Primary CWs from vegetables contain only a small amount of glucuronoxylan whereas secondary CWs contain, as a major component, a glucuronoxylan with little arabinose. Arabinoxylans from cereals can be esterified to ferulic acid at C5 of the arabinose sidechains and these phenolic groups can be coupled to form diferulate which crosslinks the parent polysaccharides (McDougall 1993).

Lignin is formed by the polymerisation of coniferyl, p-coumaryl and sinapyl alcohols (Lewis and Yamamoto 1990). These phenylpropane units are linked by an irregular three-dimensional pattern of ether and carbon-carbon bonds in which either of the carbons may be part of the aromatic ring. Lignin tends to fix the polymers in place, excludes water and makes the CW more rigid. In addition, lignin may be covalently linked to polysaccharides both directly via sugar residues and indirectly via ferulic acid esterified to polysaccharides (McDougall 1993). Suberin is a polyester of unsatu- rated, R-hydroxy C16-C4 fatty acids, a-R dicarboxylic acids and C20-C30 acids and alcohols. It also contains ferulic acids and lignin-like material. Cutin is also a polyester of C16-18 hydroxy fatty acids. It is exten- sively cross-linked, the hydroxy group of one monomer being esterified to the carboxy group of another. As

138 G J MeDougall et a1

Polymer Backbone

Cellulose [Glc P(1-4)Glc p( 1-4)] n.....

Sidechains Comments

None Forms crystalline microfibrils

CH20H

Galacturonan [GalAa( 1 -4)GalAa( 1 -4)]n.... a None

Rharnnogalacturonan GalA a(1-2)Rha a(1-4)GalA a(1-2)Rha Arabinans

Interacts with Ca methoxylated rnethylated acetylated

Rhamnogalacturonan II as minor component

‘on Mixed linkage Glucans Glc p(1-4)Glc p(1-3)Glc p(1-4)Glc None c 30% (1 -3) linkages

Xylans [Xyl p( 1 -4)Xyl p( 1 -4)ln..... Arabinose Methylated acid groups Glucuronic acid acetylated

feruloyl groups , o e :- .ray

HO OH HO OH

Xyloglucan as cellulose

Extensin

Lignin

polypeptide rich in Ser(Hyp)4 repeats

polymer of cinnarnyl alcohols

CH20H I

Xylose Acetylated Galctose Fucose as Xyl( -Gal)-( F U ~ ) ~

Arabinans Tyrosines coupled to linked to Hyp, galactose to Ser

form isodityrosine cross-links

None Cross-linked to proteins and pol ysaccharides

OH b

Glc = glucose; GalA = galacturonic acid; Rha = rhamnose; Xyl = xylose: Gal = galatose; Fuc = fucose. a - xyloglucan may be substituted with a(1-6) Xyl or a( 1-6) Xyl p( 1-2) Gal or a( 1-6) Xyl p(1-2) Gal a(1-2) Fuc units. b - where R1 = R2 = H; p-cournaryl alcohol; where R1 = H and R2 = OCH3; coniferyl alcohol;

where R1 = R2 = OCHg sinapyl alcohol.

Fig 5. Structure of the major components of the plant cell wall.

Plant cell walls as dietary jibre 139

Galacturonan {RG 1 with

arabinoglalactan structures side-chains

-

Fig 6. The diagram illustrates the intertangling of matrix polysaccharides with the insoluble cellulose/extensin phase. The wall matrix is progressively filled with polymers from left to right. In the cell wall, cellulose microfibrils may also cross over other microfibrils but this has been omitted for clarity, The diagram has been adapted with permission from Carpita and Gibeaut (1993).

some monomers have more than one hydroxyl group, the structure can be branched. The complete layered structure may also contain hydrocarbon waxes and some ferulic acid. Like lignin, suberin and cutin encrust and embed the CWs in which they are deposited making them impermeable to water. Tannins can be found intracellularly or bound to the CW. Commonly found in pulses and in grapes, these hydrophobic mol- ecules can complex with polysaccharides and protein often rendering them insoluble (Porter 1993).

It is now recognised that PCWs contain a host of structural proteins (Showalter 1993). The best described is extensin (Wilson and Fry 1986) which comprises N 5% of the primary CW of vegetables but only -0.5% in cereals (Table 2). It is a glycoprotein (- 50% protein) which has an unusual amino acid composition contain-

ing -40% hydroxyproline and large amounts of lysine and serine. Tyrosine residues are implicated in phenolic cross-linking of extensin and this may account for the remarkable insolubility of this protein in the CW (Biggs and Fry 1990). Other proteins are present in smaller amounts but these may have important roles in the architecture of the CW such as cross-linking with lignin (Keller et al 1988).

These individual components are held together by covalent, ionic, hydrogen bonds and van der Waals forces to form the CW. A review by Carpita and Gibeaut (1993) sets out models of the possible interactions between the components of the primary PCW. PCWs are envisaged as a composite of two phases, the microfibrillar phase consisting of cellulose microfibrils and possibly proteins such as extensin which forms an


insoluble framework and the matrix phase composed of NCPs which surround and embed the framework (Fig 6). Hemicellulosic NCPs hydrogen bond to cellulose and may regulate wall strength and porosity by control- ling the separation of microfibrils. Pectic polysaccharides fill the matrix through gel formation. Homogalacturonan maintains this structure through 'egg-box' interactions with Ca2+ ions. Covalent diferulate crosslinks between polysaccharides could also strengthen the structure. A detailed survey of known and possible interpolymeric bonds in the CW is given by Fry (1986). Although there is no descriptive model for the secondary PCW, it is likely that a similar two phase system will apply in which the cellulose microfibrils (present at -70% in some secondary CWs) are surrounded by a matrix composed of the other constituents (McDougall et al 1993). Of course, the secondary wall may contain lignin and linkages between CW components and lignin are known (Iiyama et al 1994).

For the study of structure-function relationships of PCW components and their physiological effects, it is crucial that the chemical structure of the PCWs can be monitored. There are standard methods for the complete analysis of polysaccharide structure (see Fry (1988) for details), but methods for the structural analysis of lignin, suberin, cutin and CW proteins are more compli- cated. The complete study of PCWs as DF requires the fate of these components to be explored. Radiochemical tracer methods could be invaluable but rapid, non- destructive spectroscopic methods already used for PCW analysis, such as Fourier transform infrared spectroscopy (Stewart and Morrison 1992) and solid state nuclear magnetic resonance techniques (Stewart and Morrison 1993), may also be successfully applied to the study of the variability of PCWs as DF.

PHYSIOLOGICAL EFFECTS OF DIETARY FIBRE

PCWs exert physiological effects as they and their components pass through the GIT. A number of review articles on this topic have been published (Kay 1982; Schneeman 1986; Anderson et al 1990; Eastwood 1992), for other articles see Furda and Brine (1990) and Southgate et a1 (1990). Figure 7 illustrates the various parts of the GIT and their functions. We have split the discussion into separate parts that deal with effects of DF in sequential sections of the GIT but discussion of some topics is applicable to different sections.

PCWs influence texture and palatability of diet

Food is normally cut up, masticated into small pieces and lubricated with saliva in the mouth prior to swal- lowing, Cursory examinations of masticated plant tissues show that raw plant tissues enter the GIT as a

Hydralmn Tasle

Liver and gallbladder Bile formation for iipld emulsification Stomach

'Holding" area Denaturation of prolein Fa1 hydrolysis

Enzymes for

Large intestine I colon Water and electrolyte absorption \\\ypj t " Fermenlation w- /v Elimination of residue

Rectum

Fig 7. Diagram of the gastrointestinal tract.

mixture of tissue pieces containing a large proportion of intact cells. The way that the tissue fragments will depend on cellular structure. For example, tissues may preferentially split along long, thin cells. Some cell breakage does take place. This releases sugar and other metabolites which influence the taste and therefore the enjoyment of the food. The intracellular contents also include free radicals and other compounds such as anti- oxidants and reducing agents that influence redox reactions. The sight and smell of food and the action of chewing stimulate receptors which signal to the central nervous system that food is being eaten. These signals result in reflex changes via the parasympathetic nervous system which prepares the GIT for food (Vander et al 1980).

PCWs promote satiety and reduce calorie intake

Many plant cells hydrate and burst in the acidic conditions of the stomach. Certain acid-labile bonds in the CW are also broken causing sloughing of CW polysaccharides and an opening of the CW structure. Bonds in wheat bran and isphagula seed husk are hydrolysed almost instantaneously on contact with the acidic (pH -2.5) stomach contents of humans (Andersen et a1 1988) releasing arabinose probably from ara- binofuranosyl residues (Fry 1988). PCWs swell in the stomach causing an increase in the viscosity of the stomach contents. Such bulking distends the stomach and has been implicated with increased feelings of satiety and may combat overeating and obesity (Leeds 1987). However, as diets rich in fibre often take longer to eat than other calorie-comparable diets, this effect may be the result of slower stomach filling. Ingestion of DF appears to be able to control hunger and results in reduced calorie intake in subsequent meals (Burley and

Plant cell walls as dietary fibre 141

Blundell 1990). Well after the meal, increased digesta bulk is present to distend the small intestine and is sensed by mechanoreceptors which feedback to reduce stomach motility and delay stomach emptying. This ileo-gastric reflex influences the perception of hunger. Soluble PCW components such as pectins, fl-D-glucans and gums give rise to the greatest increases in viscosity and are the most effective in this respect but the bulking effect of other components, including gelatinised starch, is also important.

PCWs modulate nutrient absorption in small intestine

Diets rich in PCWs delay glucose and lipid uptake into the blood stream. Soluble polysaccharides increase digesta viscosity, reduce the effectiveness of gut mixing and limit diffusion of nutrients to the intestinal mucosa for absorption and prevent access of pancreatic amy- lases and lipases to their substrates in the intestine. The CW network may act as a sieve through which soluble compounds and fluids are circulated (Eastwood 1992). This also limits access of digested material to the absorptive mucosa and digestive enzymes to their substrates. Pulses are particularly effective in limiting blood glucose levels due to the peculiar thickness of the CWs of their storage parenchyma cells that enclose starch granules. The CWs retain their integrity even after cooking and thereby limit access of the pancreatic amy- lases to the starch (Wursch et a1 1986; Tovar et al 1992). CW polysaccharides may inhibit or bind digestive enzymes while the tannins present in some plant foods can cause inhibition of trypsin, lipase and amylase (Longstaff 1989). For these reasons, diets enriched in DF are recommended to modulate glucose responses in patients with non-insulin dependent diabetes (Lean et a1 1991).

The ingestion of DF also reduces serum cholesterol levels. The mechanism whereby this occurs is not completely clear but four main hypotheses have been put forward.

(i) The increased viscosity of the digesta limits access of cholesterol to the absorptive mucosa.

(ii) Cholesterol binds to or is entrapped within PCWs and withheld from the absorptive surfaces. PCW components may also interfere with micellar formation and prevent emulsification of cholesterol. A higher proportion of cholesterol would then be excreted in the faeces.

(iii) Bile acids bind to PCW components in the small intestine and are excreted in the faeces. This interrupts the normal enterohepatic recovery of bile acids from the colon. As a result, hepatic levels of bile acids are reduced and cholesterol is metabolised to make up the deficit.

(iv) PCW components are fermented in the colon producing short-chain fatty acids (SCFAs), some

of which are transported to the liver in the portal vein. These SCFAs have been found to inhibit hepatic cholesterol synthesis in uitro. However, effective levels of SCFAs in uitro were 10-15 times higher than are recorded in uiuo (Illman et a1 1988).

Different DF sources that cause similar reductions in cholesterol levels do not act by the same mechanisms. For example, sugar beet fibre (residue after sugar extraction) causes increased cholesterol excretion in the faeces but does not increase bile acid excretion whereas oat bran and pectin increase both faecal bile acid and cholesterol excretion (Langkilde et a1 1993). A study of the effects of three different galactomannan gums that differed in their galactose/mannose ratios found that the most effective in reducing serum cholesterol also had the lowest viscosity in uitro and no apparent differences in any other areas (Evans et a1 1992). Therefore, it may be that a universal mechanism for lowering blood cholesterol levels does not operate. Hydrophobic components such as lignin, suberin and methoxylated pectins could be important in these interactions.

There is evidence that the particle size of PCWs can be reduced in the ileum before they pass through to the large intestine (Selvendran and Robertson 1990). This process appears to involve solubilisation rather than the digestion of PCW components. Certain soluble PCW polysaccharides such as RG I can act a potent immuno- modulators and stimulate the destruction of tumour cells by the hosts’ immune system (Zhao et al 1994). Waldron and Selvendran (1993) raised the possibility that similar polysaccharides, solubilised from the PCW in the small intestine, could subsequently enter the enterohepatic blood system or lymph and potentiate the anti-tumour activity of the immune system.

Fermentation of PCWs

In the large bowel, a mixed flora of anaerobic bacteria decompose PCWs by fermentation. Soluble pectins, gums, fl-D-glucans, arabinans and arabinogalactans are completely decomposed and some previously insoluble components such as ‘resistant starch’, xylans and xyloglucans are decomposed to different extents. The fermentation products include SCFAs (acetate/propionate/butyrate, in the ratio 60 : 25 : 10). This fermentation not only maintains the saccharolytic population of bacteria but releases propionate and acetate for metabolism in the liver (Schneeman 1990). Butyrate appears to be almost exclusively utilised by the colonic epithlial cells and has been found to act as a protective agent against experimental tumourogenesis of these cells (McIntyre et a1 1993).

Parenteral or enteral feeding of patients with nutrient solutions can cause atrophy of the mucosal surfaces of


the gut which appears to be the response of the epithelial cells to the lack of stimulation from bulk in the diet (Frankenfield and Beyer 1991). This atrophy can have implications for the role of this layer of cells as an effective barrier to the exterior (ie the gut contents) and to microbial invasion. To avoid this effect, soluble D F sources have been added to feeding solutions. In addition to their role as intestinal bulk, they provide SCFAs through fermentation which may act as trophic factors in maintaining mucosal integrity and proliferation (Evans and Shronts 1992). Therefore, a symbiotic relationship can be postulated between the microflora of the colonic contents and the mucosal epithelial cells. That the products of digestion feedback to influence the digestive system is a common theme in the digestive process (Vander et al 1980); amino acids influence intestinal secretion, fatty acids influence bile secretion and SCFAs affect mucosal epithelial proliferation. CW polysaccharides are broken down to oligosaccharide fragments by enzymes secreted by saccharolytic bacteria in the colon prior to fermentation. Apart from acting as inducers for the production of further saccharolytic enzymes in colonic bacteria, such oligosaccharides have potent biological signalling roles in plants (Aldington et a1 1991) and, considering the known signalling roles of carbohydrate groups in mammalians, it seems possible that they could influence GIT function or modulate some of the beneficial effects of DF.

Although most soluble polysaccharides are rapidly fermented, other components such as hemicelluloses, cross-linked pectins and cellulose survive to enter the distal colon. Studies suggest that components of wheat bran survive to the distal colon and are fermented there giving rise to significant levels of butyrate (McIntyre et a1 1993). The maintenance of fermentation to SCFAs (especially butyrate) throughout the colon may be an important factor in preventing colorectal cancer (Clausen et al 1991). Nevertheless, the overriding factor may be the adaptation to a high fibre diet as the major difference in SCFA production between rats fed a lifelong high-fibre diet and those on a lower fibre diet was the doubling of butyrate production in the former (Edwards et a1 1992). Therefore, insoluble and/or previously inaccessible polysaccharides that survive through to the distal colon may have a special role in protection against large bowel cancers.

PCWs increase faecal bulk, reduce transit time and bind and remove potentially harmful compounds

Some PCW components survive the GIT and are excreted in the faeces and these partially decomposed and intact components provide two main benefits. Firstly, they retain water and water-soluble metabolites and therefore increase faecal mass and, secondly, they decrease gastrointestinal transit time. The reduced transit times induced by high-fibre diets may be a con-

sequence of increased bulk in the colorectal area (Read 1990). Bulky bowel contents distend the colonic walls and thereby stimulate sensors which promote emptying of the colon contents to the rectal area. Finely milled wheat bran is much less effective in achieving reduced transit and increased faecal bulk than coarsely milled bran (Schneeman 1986). This effect is not due to increased decomposition by colonic bacteria (Van Dokkum et a1 1983; Van Soest 1984). Studies on the fate of wheat bran in the human GIT using scanning electron microscopy of material recovered from faeces (Dintzis et a1 1979a,b) showed that the aleurone and endosperm were completely digested but the pericarp, including the lignified cross cells, was largely intact. The smaller particle size of the pericarp caused less stimulation of gut wall sensors which led to a longer transit time. The finding that the ingestion of indigestible plastic particles (2 mm diameter) had similar effects on transit time and stool weight as wheat bran (Tomlin and Read 1988) supports this theory. The promotion of faecal mass by D F is a consequence of the presence of undigested DF, increased faecal bacterial mass and associated solutes. Soluble polysaccharides such as pectins which are completely fermented increase faecal mass to a lesser extent through their promotion of colonic bacterial growth which increases faecal bacterial mass.

A bulky faeces with a putty-like consistency can be easily voided and this may have direct benefits in alle- viating constipation, diverticulitis and other bowel conditions (Eastwood 1992). The ease and frequency of defaecation is also of psychological importance. There is no doubt that constipation can be mentally as well as medically damaging. However, D F intake is not the only variable affecting faecal output; exercise, stress, personality traits and other aspects of lifestyle may also have a large bearing on this factor. The pattern as well as the type of food intake may also be important. The Western habit of three meals a day at set times may have psychological effects in training the GIT when to expect food and in raising expectations of when defaecation would be appropriate or normal.

Burkitt (1971) linked bowel and colorectal cancer to the slow passage of small, concentrated bowel contents and there is good evidence that ingestion of high DF diets results in increased removal of carcinogens from the gut (Bingham 1990). Potential mutagens, steroids, bile acids and xenobiotics are proposed to bind or adsorb to DF components and be rapidly excreted (Bingham 1992). In uitro studies suggest that lignin may be involved in this form of binding (Schneeman 1990) presumably by hydrophobic interactions. However, the lignin used in these studies was present at much higher concentrations than could ever occur in normal food sources and was structurally different from native lignin. Therefore, the adsorption of hydrophobic compounds to lignin may not occur to this extent in uivo. It is also

Plant cell walls as dietaryfibre 143

interesting that pectins are unable to bind to bile acids in uitro (Pfeffer et a1 1993). Suberised CWs may provide the required hydrophobic surfaces as these form a higher proportion of PCWs ingested. A comprehensive study of the mechanism by which this occurs, perhaps starting with a survey of the binding of relevant model compounds to authentic PCW components under physiological conditions, is warranted. This kind of information could be invaluable in assigning the beneficial effects of DF to specific PCW structures.

The ingestion of diets enriched in DF has been positively correlated with the reduced incidence of sex- hormone-dependent cancers such as breast and prostate cancers (Aldercreutz 1991). DF-enriched diets decrease the serum levels of certain steroidal hormones and increased faecal bulking caused by DF is positively correlated with enhanced steroid excretion. Certain PCW components have been implicated in binding steroidal hormones in uitro, most notably lignin (Whitten and Schultz 1988). It is likely that the mechanisms whereby DF exerts this protective effect on sex-hormone-dependent cancers are similar to the mechanisms for DF effects on cholesterol levels and will remain as difficult to pin down. In this case, the main effect of D F may not be positive but arises because high DF diets are very often also reduced in fat, protein and/or calorie intake. However, it is intriguing that plant lignans and iso- flavones, also ingested in high DF diets, are weak oestrogens and, as such, induce the synthesis of sex hormone binding globulin which reduces serum oestro- gen levels (Aldercreutz 1988). Oral pharmaceuticals such as steroidal oestrogens, painkillers and antibiotics are often taken on a regular, if not a chronic, basis and the effects of a high D F diet on the uptake, metabolism, faecal excretion and effectiveness of these drugs must be taken into account (Lindebaum et a1 1981). For example, long-term intake may cause an adaptation of colonic microflora and enhanced metabolism of these drugs (Rowland 1991). On a global scale, the disposal of faeces containing pharmaceuticals such as steroidal hormones and their biologically active derivatives could pose serious environmental and health problems. A possible drawback of PCWs as DF is that they bind cations due to the carboxyl groups on pectins and glu- curonoxylans. The cation exchange capacity of CW components can lead to the increased faecal excretion of minerals and electrolytes (Toma and Curtis 1986). DF- rich, mineral-depleted diets may, therefore, cause nutritional problems. However, the increased mineral content of DF-rich foods such as fruits and vegetables may offset this risk.

EFFECTS OF PROCESSING AND COOKING ON PCWs AS DF

Cooking of plant tissues alters the physical and chemical properties of PCWs which, in turn, affects their per-

formance as DF. Boiling of starchy vegetables and fruits causes a loss of integrity of the tissue due to cell separation and dissolution of the middle lemellae. Cells are sloughed, some breakdown of pectins occurs through /?- elimination and starch gelatinises and swells, often causing cell breakage. This loss of tissue and cellular integrity makes mastication more effective and increases the surface area of the tissues and the CWs. In general, this makes the digesta more viscous. Therefore, post- prandial effects on blood glucose and lipid will still occur. However, the increased openness of the CW may allow more efficient release of starch and lipid.

The gelatinisation of starch upon heating increases its solubility and its susceptibility to acid and amylase digestion. Upon cooling, a certain portion of starch, in particular high amylose forms, can retrograde to a less- soluble form which is resistant to acid and amylase action (Berry 1986). This form resists digestion in the small intestine and is fermented in the colon. Baking of cereal flours also produces 0.5-1.0% ‘resistant’ starch and therefore white bread has a higher ‘fibre’ content than white flour. Starch-lipid and starch-protein complexes can also be formed during cooking and these are also more resistant to a-amylase (Holm et al 1983).

A very small proportion of cereal grains are consumed in their natural form. They are processed by milling into flours (wholemeal) or pretreated to remove the bran and milled to white flour. The flours are then cooked in some manner to provide the final product. An indication that the form of DF ingested is vitally important is shown by the finding that faecal bulking in rats caused by whole grain flours was greatest with barley and oats followed by wheat (Ranhotra et a1 1991). This is the opposite to the situation with grain brans as wheat bran is more effective in causing faecal bulking than oat or barley brans (Schneeman 1986).

Cooking can also cause the formation of cross-links between food components. Maillard products arise from the reaction of sugars and proteins (Adrian 1974), often leading to the browning of foodstuffs and providing important flavour components. The end products of these reactions can be complex polymers that are not digested in the small intestine and may, therefore, increase the DF content of the food. Indeed, certain high molecular mass Maillard products have been found to mimic some of the physiological effects of DF (Ragot et a1 1992). Other Maillard products, mainly those from meats, can have carcinogenic or tumour- promoting effects (Barnes et a1 1981). The formation of these cross-links is of great interest to the food processing industries and has been studied intensively (Friedman 1992). However, their behaviour as DF has not been so well investigated. The type of cooking (boiling, steaming, frying, roasting or grilling) will affect the type and levels of Maillard products. In general, cooking techniques that use dry heat or scorching (roasting and frying) promote the formation of Maillard


products to a greater extent. Different cooking methods will also affect the properties of PCWs as DF. Micro- wave heating was found to have a different set of effects on the soluble and insoluble fibre contents of vegetables than boiling (Nyman et a1 1994).

An increasing number of plant food by-products (eg potato skins) are being extrusion-cooked, a process important to many shaped food products. In this process, the material is reduced to a small particle size, heated to high temperatures then extruded with considerable acting shear forces to form the shaped product. The process breaks CW bonds and causes a reduction in insoluble fibre content, an increase in soluble fibre and the formation of some Maillard reaction products (Bjorck et al 1984; Camire and Flint 1991).

Other processing or preservation methods such as canning, tinning or preserving involve pre-cooking then suspending fruits/vegetables in solutions of dilute acetic acid, brine or sugar. All of these treatments increase maceration of the tissues and CW breakdown and digestion (Nyman et al 1987). The consumption of frozen vegetables is increasing. Freezing and thawing bursts plant cells and causes tissue damage increasing the accessibility of the tissue. Dry storage of cereals and pulses can cause an increase in apparent DF content due to dehydration or oxidative reactions (Selvendran et al 1987). Drying of fruits (ie grapes to raisins/sultanas and plums to prunes, etc) not only alters their textural properties but enhances their effects on gut motility and transit time.

Most ‘fresh’ fruit and vegetables eaten today have been stored for a considerable period before they are purchased. Fresh produce is stored during import and subsequent transport to retail outlets. Although varieties of fruit and vegetables have been selected that retain fresh characteristics for longer and goods are stored and transported in chilled conditions, the effects of such storage on DF content is not known. Waldron and Selvendran (1990) noted that the pectic content of asparagus was reduced during storage with a coincident increase in lignin content.

If efforts to increase DF intake are to be successful then it is imperative that accurate information on the content and structure of DF in foodstuffs is available. The accurate determination of DF hinges on the iso- lation of the PCW as a composite with minimal breakdown and contamination from non-PCW components. The method recommended by the Association of Ofi- cia1 Analytical Chemists (AOAC) mimics the digestive processes of the stomach/small intestine and estimates the residue that survives sequential digestion with a- amylase, protease and amyloglucosidase (Lee et a1 1992). While previous methods based on sequential chemical extractions underestimated DF due to extraction of PCW components (Schneeman 1986), this rapid and reproducible method slightly overestimates DF as a

result of incomplete removal of starch/protein. Variabil- ity can arise from different pretreatments of different types of foods. Some tissues have to be defatted using petroleum ether and sugar-rich fruits may have to be extracted with 85% ethanol and dried prior to analysis. Different pretreatments have been found to alter the observed D F content of polysaccharide preparations (see Stevenson et a1 1994) and it is essential that these are strictly standardised. As this method demands that the plant tissues are milled prior to analysis, it does not take into account the effects that the tissue structure and CW shape may have on the accessibility of certain wall components.

A number of artificial components added during processing may impact on the DF quotient of foods. Poly- saccharides extracted from plant. algal and microbial sources may be added to foods during processing as film-forming compounds, binding agents, filling agents, thickeners, stabilisers, bulking agents, emulsifiers, fat mimetics and foam-modifying agents (Whistler and BeMiller 1993). All of the industrially important polysaccharides act as soluble D F being undigested in the small intestine and completely fermented in the large intestine. Synthetic triglycerides with lower calorific values have been developed to replace fats in the diet. These ‘calofats’ have been chemically altered to reduce their susceptibility to lipases (Mangold, 1983 ; Kleeman et a1 1990; Smith et a1 1994) and are not digested by the secretions of the human GIT. Therefore, they can be thought of as D F components. However, it remains to be seen if they display any beneficial effects and these detergent-like compounds could have detrimental effects on the composition of gut microflora, the hydro- phobicity of the gut contents and solidity of faeces. Low-calorie sweeteners are compounds that mimic the sweetness of sucrose but are not digested by a-amylase (Khan 1993). These compounds are also not digested in the small intestine but are fermented in the large bowel. Whether these dietary components qualify as DF is open to debate, but they may serve as inducers of saccharolytic enzymes in colonic microflora.

Raw plant tissues offer different benefits. The tissue integrity of most salad vegetables and fruits is not greatly altered by mastication. As a consequence, digesta viscosity will be lower and less cellular material is accessible to digestive enzymes. Native starch is quite insoluble and large amounts will survive through to the colon. Therefore, a greater proportion of the fibre is insoluble or inaccessible for a longer period. The PCWs will cause reduced bulking effects but corresponding decreases in the accessibility of starch and lipids due to incomplete cell breakage will ensure that post-meal glucose and lipid levels do not rise steeply. The most important benefit may be that a greater proportion of vitamins and micronutrients lost or leached out during cooking are retained in raw foods. Indeed, vitamins A, C and E, common in raw plant foods, are implicated in

Plant cell walls as dietary Jibre 145

the protection against free-radical-driven mechanisms in carcinogenesis (Berger et a1 1991; Fraga et a1 1991) and the development of heart disease (Riemersma et a1 1991). In fact, some argue that the prevention of carcinogenesis by high DF diets may be partially due to the ingestion of elevated levels of these vitamins (Southgate 1990) and other naturally occurring non-nutritive che- moprotective compounds such as tannins, phenols, thio- cyanates, flavanoids and certain minerals in fruits and vegetables (Wattenburg 1993).

CONCLUSIONS, QUESTIONS AND DIRECTIONS

The integrity of the PCW is important to deliver the physiological effects of DF. The PCW enters the GIT as a composite and the components appear to have different roles in the beneficial effects of DF. Soluble and solubilised PCW components increase the viscosity of the digesta and modulate serum glucose and lipid levels. Despite the widely accepted definition of DF, these beneficial components do not survive passage through the GIT. They are often completely fermented in the colon along with other exposed components such as resistant starch. This degradation supports the population of saccharolytic bacteria and provides SCFAs for utilisation in the liver. Butyrate, which seems to be preferentially formed from CW components that survive into the distal colon, is implicated in the prevention of colorectal cancer and the maintenance of a functional epithelial muscosa through proliferative effects on colonic epithelial cells. Those components that do survive fermentation in the colon, function to bulk the faeces and maintain a short GIT transit time. Poten- tially harmful compounds may bind to these components and be rapidly excreted.

Therefore, the passage of PCWs through the GIT is characterised by a sequential stripping away of wall components. The multi-composite PCW can be likened to a ‘slow-release vehicle’ which ensures that there is bulk in the stomach and small intestine and that, after accessible components are fermented in the caecum, other components survive to provide bulk in the colon. The ingestion of DF provides bulk throughout the GIT. This may have important consequences beyond the promotion of efficient propulsion of gut contents by peri- stalsis. The gut surfaces are in constant contact with the digesta and their sensors feedback information to the central nervous system. Bulk throughout the GIT may influence the feedback from the parasympathetic nervous system and promote steady-state feelings of satiety and general well being. Lack of bulk may promote the distress signals associated with hunger, irri- table bowel syndrome or constipation.

The current definition of D F emphasises the inertness of PCW components. That DF components are defined

in such a negative manner, ie digestion by GIT secretions, is at best unfortunate and at worst reinforces older concepts of DF as ‘unavailable carbohydrate’ (as discussed by Heaton (1990)). Therefore, it is important to stress the beneficial effects of DF and the dynamic changes that PCW components undergo to bring about these effects in the gut. In fact, it is likely that none of the components of the PCW passes through the GIT structurally unchanged.

Questions on the digestion of individual PCW components still remain. There is some evidence that cellulose is degraded in the GIT. ‘Before and after’ analyses have suggested that the total percentage of PCW remaining in the faeces is less than the percentage cellulose content of the original sample (Cummings 1984; Kelleher et a1 1984; Stevens et a1 1988; Gray et al 1993). The insoluble, crystalline nature of cellulose presents the main barrier to digestion as partially degraded ‘high- porosity’ celluloses are used as food additives and are completely digested in the human colon (Whistler and BeMiller 1993). Most studies have concerned cellulose in primary CWs. The degree of PCW degradation in the rumen has been found to be closely related to the thickness of the wall (Wilson 1993). Considering the longer exposure to cellulolytic bacteria in the rumen, it seems unlikely that secondary CWs containing large amounts of crystalline cellulose would be degraded in the human GIT. However, even a slight alteration in the crystallinity of cellulose, late in the GIT, would alter its physical properties (eg water-binding capacity) and have marked effects.

It also seems unlikely that lignin is decomposed in the GIT but the cleavage of lignin-polymer linkages could open up the CW structure. The alkaline pretreat- ment of wheat bran, for example, increased the digestibility of the carbohydrate component in the rumen to 12% compared with the untreated value of 35% (Selvendran et al 1987). This treatment probably cleaves phenolic ester cross-links between CW polysaccharides and lignin (Iiyama et a1 1994).

The polyester structures of cutin and suberin may be subject to degradation. However, cuticle components and suberin were not reported to be affected in the human GIT (Martin and Juniper 1970) and no further information has accrued since. If de-esterification of cutin or suberin did occur, it would alter the hydropho- bicity and thereby the accessibility and digestibility of the surrounding tissues.

Little is known about the fate or role of CW proteins as DF. Although extensin only comprises, at most, 5% of vegetable CWs, its contribution to the architecture of the CW may be significant as it forms part of the extremely insoluble framework of the wall. It is also polyanionic having a PI > 9. Therefore, it could contribute to the ion exchange capacity of DF (perhaps binding bile acids) and the overall insoluble DF content. The insolubility of extensin may ensure that it


passes through the stomach and small intestine unde- graded by proteolysis but partial deglycosylation or limited proteolysis could open up the entire primary wall structure of many vegetable CWs.

Many studies have been carried out on the fate of purified, isolated wall components in the GIT and although these have helped to define the physiological possibilities of these components as DF, they do not necessarily relate to the situation in the intact wall where the accessibility of the component in question may be limited. The use of specifically radio-labelled substrates allows the production of CWs labelled in specific residues (Buchanan et a1 1994a,b, 1995). The metabolic fate of the labelled component in the gut can then be monitored within the CW structure. This approach gives quantitative estimates of digestion and qualitative data on the fate of the metabolised label. For example, Buchanan et al(1994b) have found that PCWs containing pectins specifically labelled with 14C galacturonic acid were rapidly metabolised in rats. Within 18 h of feeding, 90-95% of the radioactive label had been metabolised and a significant amount had been incorporated into proteins and fats. The 5-10% of label remaining in the faeces may represent the proportion of radioactivity incorporated into excreted bacteria. Similar approaches could be extended to lignin, suberin, cutin and extensin.

Eating diets enriched in DF to defend against or treat health disorders without recourse to pharmacological, medical or surgical intervention could be defined as a form of ‘personal bio-remediation’. This is certainly the concept of ‘personal insurance’ against certain health risks that the manufacturers of high bran and high oat bran cereal products are using in their advertising cam- paigns and, of course, DF-enriched diets are recommended by the British Government (Anon 1992, 1993). To extend this concept of ‘functional foods’ to its logical conclusion, it may be possible to target the intake of certain PCWs or components as providers of one of the beneficial effects of DF to protect against specific diseases. However, the current understanding of structure- function relationships between PCW components and the beneficial physiological effects of DF are not suffi- ciently defined for this degree of specificity. There are broad areas of understanding. The control of post- prandial blood sugar levels appears to be best modu- lated by viscous ‘soluble’ polysaccharides whereas faecal bulking requires ‘insoluble’ CW components like lignin and cellulose. It may be that structure-function relationships of the specificity found in other areas of biology may not exist for the beneficial effects of DF and that the physiochemical properties or the solubility or accessibility of components in particular PCWs are more important (Eastwood and Morris 1992). On the other hand, the study of structure-function relationships has only really been possible for a short period of time and should be encouraged. A multidisciplinary

approach involving experts in PCW structure and composition with physicians, epidemiologists, dieticians, nutritionists, clinicians and cancer researchers could map out the possible inter-relationships between PCW structure and DF effects. The instigation of such a multidisciplinary team has been proposed to evaluate the general evidence regarding human health and diet and report on the implications of the provision of healthy food on agricultural policy in the European Union (Golden and James 1994).

It should be possible to alter the properties of PCWs as DF by modern and traditional breeding methods. Current crop varieties have been selected for yield and qualities such as disease resistance, succulence, colour and sweetness without great regard for effects on DF content. Indeed, in many cases, breeders have selected against elevated, in particular insoluble, D F content. All crops probably have ancestral varieties that have valuable traits for D F content. Considering the beneficial medicinal effects of DF intake, breeding programs for new varieties should rank D F content as a valuable trait. Consider, also, the marketing possibilities and the added value of the health benefits of high-fibre foods. Breeding programmes to identify genotypes with high DF content could use percentage dry matter as an initial screening method then once promising varieties had been identified, more complex investigations into total, soluble and insoluble DF content could begin. Such an approach has been used to increase signifi- cantly the dry matter content of forage swedes (Gowers and Gemmell 1988; Bradshaw and Griffiths 1990).

Plant tissue and cell culture may bring other opportunities. The somaclonal variation inherent in cultured plant cells may provide useful variants unavailable to the normal breeding process (Craig and Millam 1995). Suspension-cultured plant cells produced in bulk in fermentors could provide near homogenous cell populations (with homogenous cell walls) for the study of PCW-DF structure-function relationships. Attempts to alter the CW content by breeding may cause pleio- tropic efferts on other valuable traits. Since polysaccharide and starch synthesis operate from limited pools of sugar precursors, alterations in one may affect the other. For example, ‘waxy’ isolines of barley that contain 96% amylopectin compared with 25% in the wild type also have elevated levels of CW 8-glucans (Xue et a1 1991).

Another route to plants with altered DF content and properties may be provided by the modification of the composition of PCWs by manipulation of the genes for synthetic enzymes in wall biogenesis. Enzymes that syn- thesise polysaccharides are being purified to provide genetic targets for the manipulation of the polysaccharide composition of the CW (Rodgers and Bolwell 1992). Lignin content and structure has already been altered by genetic manipulation of important target enzymes in the biosynthetic pathway of lignin in

’

Plant cell walls as dietaryjbre 147

a number of plant types (Elkind et a1 1990; Bugos et al 1991; Halpin et a1 1994). Genes for extensin and other CW proteins have been identified (Showalter 1993) and could possibly be manipulated. However, the reduction of the content of certain CW components may induce compensatory changes in the CW composition to maintain a functional CW. For example, plant cells cultured in the presence of dichlorobenzonitrile, an inhibitor of cellulose synthesis, compensated for their lack of cellulose by producing increased levels of homog- alacturonans in dicotyledonous tobacco and tomato or by increased phenolic cross-linking of NCPs in mono- cotyledonous barley (Shedlezky et a1 1992).

It may be possible to alter the properties of the PCW in a more subtle manner without causing gross changes to the proportion of components. Ferulic acid is esterified to polysaccharides and appears to be involved in cross-links both between polysaccharides and between polysaccharides and lignin (Iiyama et a1 1994). If the enzyme that attaches the feruloyl groups to the polysaccharide could be identified then genetic manipulation of its expression could produce PCWs with altered phenolic cross-linking. This would markedly alter the solubility of PCWs and alter their performance as DF. In a similar vein, if the levels of the CW proteins postulated to be linked to lignin in the CW (Keller et a1 1988; Domingo et a1 1994) were genetically manipulated, this could influence total CW solubility and digestibility.

ACKNOWLEDGEMENTS

The authors thank the Scottish Office Agriculture and Fisheries Department for financial support; Gregor Menzies for his graphic expertise and many members of staff at SCRI for their help in producing this review.

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Plant Cell Walls as Dietary Fibre: Range, Structure, Processing and Function