Structure and functions of feruloylated polysaccharides

Plant Science 127 (1997) 111 – 127

Review

Structure and functions of feruloylated polysaccharides Tadashi Ishii Forestry and Forest Products Research Institute, P.O. Box 16, Tsukuba Norin Kenkyu Danchi-nai, Ibaraki, 305, Japan Received 5 February 1997; received in revised form 21 April 1997; accepted 20 May 1997

Abstract Cell wall polysaccharides contain a small amount of ester-linked hydroxycinnamic acid derivatives, such as p-coumaric and ferulic acids. These hydroxycinnamic acids can be coupled oxidatively to form the acid dimers. Dimer formation in the growing plant cell wall would cause the cross-linkage of cell wall polysaccharides and lead to an increase in wall rigidity. Feruloyl polysaccharide esters would also participate with lignin monomers in oxidative coupling pathways to generate a ferulate-polysaccharide-lignin complexes during cell wall development. Feruloyl oligosaccharides derived from feruloyl polysaccharides have been shown to inhibit cell elongation growth induced by auxin or gibberellins. Feruloyl polysaccharides are critical entities in directing wall cross-linking and in limiting biodegradability by microorganisms. © 1997 Elsevier Science Ireland Ltd. Keywords: Cell wall; Cross-linking; Feruloyl polysaccharides

1. Introduction Plant cell walls contain polymer-bound hydroxycinnamic acid derivatives, ferulic and p-coumaric acids [1]. These hydroxycinnamic acids undergo in vivo oxidative coupling reactions to form dehydrodimers of the acids [2] and also become polymerized into the lignin macromolecule [3]. Such coupling reactions, probably catalyzed by wall bound peroxidases, decrease wall extensibility and may ultimately be involved in the control of cell growth [2,3].

Biodegradation of cell wall polysaccharides in forage fiber is of economical importance to the animal industry. The extent of wall digestibility by ruminent microorganisms may well be dependent upon the cross-linked nature of wall polysaccharides [1]. Alkaline treatment of the wall dramatically increases the ruminal microbial digestibility of graminaceous forages, enhancing the nutritional value of the forage fiber [4]. Cleavage of alkaline-labile linkages has a major role in the increased digestibility of grasses. Hydroxycinnamic acid ester cross-linkages among wall com-

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T. Ishii / Plant Science 127 (1997) 111–127

112 Table 1 Major polymers of plant cell walls Component

Cellulose (b-1,4-glucan) Hemicellulose

Pectins

Glycoproteins

Phenolics

Solubility in water

Xylogucan Xylans Mixed linked glucans Glucomannan

Approximate composition of mature walls (%)

Grasses

Grasses

Dicots

25 – 35

45 – 50

Dicots

Insoluble

30

30

Soluble Soluble Soluble

5 30 30

 25 à 5 — Ì Ã — Å

Soluble

—

Homogalacturonan Rhamnogalacturonan I Rhamnogalacturonan II Arabinogalactanprotein

Soluble Soluble

Soluble

Variable

Â Ã Ì 5 à ŠVariable

Extensin Lignin Phenolic acid

Soluble Insoluble Partly soluble

0.5 — 0.5 – 1.5 —

B5 — 0.3a —

Soluble

Â Ã Ì Ã Å

Anothers (Silica) a

Approximate composition of growing walls (%)

15 15

5

40 – 50

0.1

7 – 10 0.5 – 1.5 5 – 15

Â Ã Ì Ã Å Â Ã Ì Ã Å

25

0.1

20

Chenopodiaceae family contains cinnamic acid derivatives. The epidermal cell walls of all dicots contain phenolic residues [67].

ponents are present in both the primary and the secondary walls [5]. Therefore, hydroxycinnamic acid-polysaccharide complexes are important in the structure and function of walls during plant development as well as degradation of the walls for natural energy. Excellent reviews are available that describe cross-linkages of wall polymers in the growing cell wall [2], covalent cross-linkages in the cell wall including lignified tissues [5], and synthetic models for lignin-hydroxycinnamic acid-polysaccharide complexes [3]. In this review, the structure of feruloyl polysaccharides and their possible physiological functions are summarized.

2. Cell wall composition The growing plant cell is surrounded by a thin primary wall which is comprised predominantly of cellulose (the skeletal framework of the wall), hemicellulose (generally rigid, rod-shaped polysac-

charides that hydrogen-bind to cellulose, i.e. xylans and xyloglucan, etc.), and pectins (often acidic polysaccharides that form a loosely bound gel matrix in the wall) [6–8]. In dicotyledons, these three classes are about equally abundant, whereas graminaceous monocots (grasses) possess much less pectin (Table 1). All growing cell walls also contain some glycoproteins, lipid, structural and non-structural phenolics, and some contain cutin. Some types of phenolic compounds result in the cross-linkage of cell wall polysaccharides. At the conclusion of cell expansion, cell wall composition and mechanical properties change. Fiber cells, xylem tracheary elements, and sclerenchyma have large amounts of secondary wall and usually lack protoplasts at maturity. The walls of these cells consist of a thin primary wall, a thicker, multilaminate secondary wall, and sometimes a tertiary wall. The secondary wall is enriched in cellulose, and hemicellulose and pectic polysaccharides are quantitatively different from those of the primary cell wall [7]. Many, but not

T. Ishii / Plant Science 127 (1997) 111–127

all secondary walls are lignified, reaching levels of 20 – 30 and 7–15% lignin in matured walls of dicots and grasses, respectively.

3. Linkage of phenolic acids to cell wall polysaccharides A portion of hydroxycinnamic acids are readily released by mild alkaline treatment of wall materials, showing that these acids are ester-linked to wall polymers. These esterified compounds have been detected by spectrophotometry, gas-liquid chromatography (GLC), and high-performance liquid chromatography (HPLC) [9]. p-Coumaric, ferulic, and sinapic acids and dehydrodimers, such as diferulic acids are identified in the extracts of saponified cell walls [1] (Figs. 1 and 5(2)). The location of hydroxycinnamic acids has been visualized by autofluorescence of plant tissues excited with ultraviolet light [10]. Fluorescence microscopy of Italian ryegrass (Lolium multiflorum) sections showed that feruloyl esters fluoresced blue at pH 5.8 and changed in color to green at pH 10.0 [11,12]. Harris and Hartley [11] reported that ferulic acid is located in various tissues and organs in Italian ryegrass. The linkage of ferulic acid to wall polysaccharides has been studied by determining the structure of water-soluble fractions released from walls by mild acid hydrolysis [13] or by treatment with a mixture of polysaccharide hydrolyzing enzymes without any esterase activities, such as Driselase [14,15]. A feruloyl arabinobiose, (F-Ara)-(1 “ 5)-

Fig. 1. Cinnamic acid derivatives released from graminaceous monocot cell walls by treatment with NaOH.

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(Ara), and a feruloyl galactobiose, (F-Gal)-(1 “ 4)-Gal, were for the first time isolated from the Driselase digest of suspension cultured spinach (Spinacia oleracea) cell walls by Fry [14,15] and later from the Driselase digest of spinach-leaf walls and sugar beet (Beta 6ulgaris) pulp [16,17]. These were characterized to be O-(2-O-trans-feruloyl-a- L -arabi nofuranosyl)-(1 “ 5)- L -arabinose (Fig. 2(1)), O-a-L-arabinofuranosyl-(1“ 3)O-(2-O-trans-feruloyl-a- L -arabinofuranosyl)(1“ 5)-L-arabinose (Fig. 2(3)), and O-(6-Otrans-feruloyl-b- D -galactopyranosyl)-(1 “ 4)- D galactose (Fig. 2(2)). A series of feruloyl arabino-oligosaccharides were isolated from sugar beet (B. 6ulgaris) by mild acid-hydrolysis [13]. These feruloyl oligosaccharides probably would be derived from feruloylated arabinan and (1 “4)linked D-galactosyl oligosaccharides side chains of pectic polysaccharides [2]. A feruloyl arabinoxylan trisaccharide, (F-Ara)-(1“3)-Xyl-(1“ 4)-Xyl, (Fig. 2(5)), was isolated from the enzymic digest of sugar beet (B. 6ulgaris) [15]. The walls of graminaceous monocots typically contain larger amounts of hydroxycinnamic acids than dicotyledons. A feruloyl arabinoxylan disaccharide, (F-Ara)-(1“ 3)-Xyl, (Fig. 2(4)) was isolated from the enzymic digest of wheat (Triticum aesti6um) bran [18]. A feruloyl arabinoxylan trisaccharide, (F-Ara)-(1“ 3)-Xyl-(1“ 4)-Xyl, (Fig. 2(5)) has been isolated from the enzymic digests of sugar cane bagasse (Saccharum officinarum) [19], maize (Zea mays) shoot [20], barley (Hordeum 6ulgare) straw [21], barley aleurone [22], and bamboo (Phyllostahys edulis) shoot [23]. A feruloyl arabinoxylan tetrasaccharide, Xyl-(1 “ 4)-(F-Ara)-(1“ 3)-Xyl-(1“4)-Xyl, (Fig. 2(8)) was also isolated from bamboo shoot [23] and sugar cane bagasse [24]. A small amount of p-coumaroyl arabinoxylan trisaccharide, {(pCA-Ara)(1“ 3)-Xyl-(1“ 4)}-Xyl, (Fig. 2(7)) and tetrasaccharide, (Xyl-(1“4)-{(pCA-Ara)-(1“3)-Xyl](1“4)}-Xyl, (Fig. 2(10)) were isolated from cell walls of barley straw [22] and bamboo shoot [25–27]. An 5-O-(trans-feruloyl)-L-arabinose, FAra, (Fig. 2(11)) [28–30], an O-b-D-xylopyranosyl-(1 “ 2)-5-O-(trans-feruloyl)- L -arabinose, Xyl-(1“ 2)-(F-Ara), (Fig. 2(12)) [30,31], an O-b-

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Fig. 2. Structure of feruloylated and p-coumaroylated oligosaccharides generated from cell walls.

D-xylopyranosyl-(1 “ 3)-b- D -xylopyranosyl-(1 “

2)-5-O-(trans-feruloyl)-L-arabinose, Xyl-(1 “3)Xyl-(1 “ 2)-(F-Ara), (Fig. 2(13)) [32], an O-Lgalactopyranosyl-(1“ 4)-O-D-xylopyranosyl-(1“

2)-5-O-(trans-feruloyl)-L-arabinose, Gal-(1“ 4)Xyl-(1“ 2)-(F-Ara), (Fig. 2(14)) [30], and an {[5O-(trans-feruloyl)] [O-b-D-xylopyranosyl-(1“2)] -O- L -arabinofuranosyl-(1 “ 3)}-b- D -xylopyrano-

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115

Fig. 2. (contd.)

syl-(1 “4)-D-xylose, {[F(1 “5)][Xyl-(1 “ 2)]-Ara(1“ 3)}-Xyl-(1“4)-Xyl, (Fig. 2(15)) [33] were isolated from graminaceous monocots by mild acid hydrolysis. An O-L-galactopyranosyl-(1 “ 4)-O-Dxylopyranosyl-(1 “2)-L-arabinose was previously isolated from side chain of highly branched maize xylan [34]. These feruloylated and p-coumaroy-

lated arabinoxylan oligosaccharides are believed to be derived from arabinoxylan. Acetylation sometimes occurs at O-2 of the feruloylated arabinofuranosyl residue in the arabinoxylan. Arabinoxylan oligosaccharides acetylated at O-2 and feruloylated at O-5 were isolated from cell walls of bamboo shoot, (F, Ac-Ara)-

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Fig. 2. (contd.)

(1 “ 3)-Xyl-(1“4)-Xyl, (Fig. 2(6)) [35] and sugar cane bagasse, Xyl-(1 “4)-{(F,Ac-Ara)-(1 “ 3)}Xyl-(1“ 4)-Xyl, (Fig. 2(9)) [36]. The xylosyl residue of monocot xyloglucan was also feruloylated. An O-(4-O-trans-feruloyl-a-Dxylopyranosyl)-(1“6)-D-glucopyranose, (F-Xyl)(1“ 6)-Glc), (Fig. 2(16)) was isolated from the Driselase digest of bamboo shoot walls [25,26]. O-(a-D-Xylopyranosyl)-(1 “ 6)-D-glucose (iso-

primeverose) is known to be a component of the xyloglucan macromolecule [37]. The structures of feruloyl and p-coumaroyl oligosaccharides isolated from acidic or enzymic hydrolyzates of wall polysaccharides are summarized in Table 2. Feruloylation occurs in monocots on xyloglucan and arabinoxylans. Arabinoxylans are also acylated by less amounts of p-coumarate. In dicots a feruloyl group is

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117

Fig. 2. (contd.)

attached to the arabinan and (1 “4)-linked galactosyl oligosaccharides side chains of pectic polysaccharides and also to the arabinofuranosyl residues of arabinoxylan. Monocots contain lower amounts of pectins than dicots, usually less than 5% (w/w) in the cell wall [7]. At present there has been no report that feruloylation occurs on arabinan and (1“4)-linked galactosyl oligosaccharides of pectic polysaccharides in monocots.

4. Covalent cross-linkage of feruloylated polysaccharides The formation of covalent cross-linkages between wall polysaccharides involving ferulic acid derivatives was first demonstrated in 1971 by Geissmann and Neukom [38]. These authors showed that a water-soluble arabinoxylan from wheat flour could form a gel on addition of

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Table 2 Structures of feruloylated and p-coumaroylated oligosaccharides generated by chemical or enzymic treatment of plant cell walls Structure

Nomenclature

Origin

Reference

O-(2-O-trans-Feruloyl) -a-L-arabinofuranosyl-(1“ 5)-L-arabinose

(F-Ara)-(1“ 5)Ara

Spinach (Spinacia oleracea) Sugar beet pulp (Beta 6ulgaris) Spinach (S. oleracea) Sugar beet pulp (B. 6ulgaris) Spinach (S. oleracea) Sugar beet pulp (B. 6ulgaris)

[14 – 16] [15,17]

O-(6-O-trans-Feruloyl) F-Gal-(1“4)Gal -b-D-galactopyranosyl-(1 “4)-D-galactose O-a-L-Arabinofuranosyl-(1 “3) Ara-(1“ 3)-(F-Ara)-(1 “5)Ara -O-(2-O-trans-feruloyl-a-L-arabinofuranosyl) -(1“ 5)-L-arabinose O-[5-O-(trans-Feruloyl)-a-L-araF-Ara-(1“ 3)-Xyl binofuranosyl]-(1 “3)-D-xylose O-[5-O-(trans-feruloyl)-a-Larabinofuranosyl]-(1 “ 3) -xylopyranosyl-(1 “4)-D-xylose

(F-Ara)-(1“3)-Xyl-(1 “ 4)-Xyl

O-b-D-Xylopyranosyl-(1 “ 4)-O-[5-OXyl-(1“ 4)-{(F-Ara)(trans-feruloyl)-a-L-arabinofuranosyl-(1“3)] (1“ 3)-Xyl-(1“4)}-Xyl -O-b-D-xylopyranosyl-(1 “4)-D-xylose

[14 – 16] [15,17] [16] [15,17]

Wheat bran (Triticum aesti6um)

[18]

Sugar cane bagasse (Saccharum officinarium) Maize shoot (Z. mays) Barley aleurone (Hordeum 6ulgare) Barley straw (H. 6ulgare) Bamboo shoot (Phyllostacys edulis) Maize bran (Z. mays) Bamboo shoot (P. edulis) Sugar cane bagasse (S. officinarium)

[19] [20] [21] [22] [23] [28] [23] [24]

Barley straw (H. 6ulgare)

[22]

Bamboo shoot (P. edulis)

[25,26]

Xyl-(1“ 4)-pCA-Ara)-(1 “3) -Xy-(1 “4)-Xyl

Bamboo shoot (P. edulis)

[27]

O-[2-O-Acetyl-5-O-(trans-feruloyl)-aL-arabinofuranosyl-(1 “3)]-Ob-D-xylopyranosyl-(1 “4)-D-xylose

(F,Ac-Ara)-(1“ 3)-Xy(1“4)-Xyl

Bamboo shoot (P. edulis)

[35]

O-b-D-xylopyranosyl-(1 “4)-O[2-O-acetyl-5-O-(trans-feruloyl)-aL-arabinofuranosyl-(1 “3)]-Ob-D-xylopyranosyl-(1 “4)-b-D-xylose

Xyl-(1“ 4)-(F,Ac-Ara)(1“ 3)-Xyl-(1“ 4)-Xyl

Sugar cane bagasse (S. officinarium)

[36]

5-O-(trans-feruloyl)-L-arabinose

F-Ara

O-b-D-Xylopyranosyl-(1 “ 2)-O{5-O-(trans-feruloyl)-L-arabinose} O-b-D-Xylopyranosyl-(1 “ 3)b-D-xylopyranosyl-(1 “2)-O{5-O-(trans-feruloyl)-L-arabinose}

Xyl-(1“2)-(F-Ara) Xyl-(1“3)-Xyl-(1 “ 2)-(F-Ara)

Wheat bran (T. aesti6um) Maize bran (Z. mays) Festuca (F. arundinacea) Sugar beet (B. 6ulgaris) Maize bran (Z. mays) Festuca (F. arundinacea) Festuca (F. arundinacea)

[28] [29,30] [31] [17] [30] [31] [32]

{[5-O-(trans-feruloyl][O-b-

[F(1“5)][Xyl-(1 “2)]Ara-(1“ 3)-Xyl-(1“ 4)-Xyl

Coastal Bermuda grass (Cynodom dactylon)

[33]

O-[5-O-(p-Coumaroyl)-a-L-arbinofuranosyl-(1 “ 3)]-O-b-D-xylopyranosyl-(1“4)-D-xylose

(pCA-Ara)-(1“ 3)-Xyl(1“4)-Xyl

O-b-D-Xylopyranosyl-(1 “ 4)-O-[5O-(p-coumaroyl)-a-L-arabinofuranosyl(1“3)]-O-b-D-xylopyranosyl-(1 “4) -D-xylose

D-xylopyranosyl-(1 “ 2)-O-

a-L-arabino-furanosyl-(1“ 3)}O-b-D-xylopyranosyl-(1 “4)-D-xylose

T. Ishii / Plant Science 127 (1997) 111–127

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Table 2 (continued) Structure

Nomenclature

Origin

Reference

O-L-Galactopyranosyl-(1“ 4)O-D-xylopyranosyl-(1 “ 2) -[5-O-(trans-feruloyl)-L-arabinose] O-4-O-(trans-Feruloyl)-aD-xylopynanosyl-(1 “ 6)-D-glucose

Gal-(1“ 4)-Xyl-(1“2)-(F-Ara)

Maize bran (Z. mays)

[30]

(F-Xyl)-(1“6)-Glc

Bamboo shoot (P. edulis)

[25,26]

peroxidase and H2O2. They also demonstrated that the feruloyl residues on arabinoxylan oxidatively coupled to form dehydrodiferulates, and it was subsequently suggested that this reaction is a possible polysaccharide cross-linking mechanism in growing cells [2]. The dehydrodimer coupled at 5-5 of the aromatic rings, commonly being referred to as ’diferulic acid’ (Fig. 5(2)), was identified in Italian ryegrass [12] and rice (Oryza sati6a) endosperm [39]. The existence of the diferuloyl diester cross-link was proved in 1991 by Ishii [40], who isolated and characterized a diferuloyl arabinoxylan hexasaccharide (Fig. 3) from an enzymic hydrolyzate of bamboo shoot arabinoxylan. This fact suggests that dehydrodiferuloyl cross-linking of arabinoxylan occurs naturally in the walls of bamboo shoot (Fig. 4). In addition to arabinoxylan, xyloglucan also has feruloyl residues. These results indicate that feruloylated arabinoxylan and xyloglucan could form crosslinks with other feruloylated polysaccharides through dehydrodiferuloyl bridges. It would be possible that a cellulose-xyloglucan or cellulosearabinoxylan network cross-links other wall polysaccharides such as pectins by formation of dehydrodiferuloyl cross-links. Sugar beet and

Fig. 3. Structure of a diferuloyl arabinoxylan hexasaccharide.

spinach have feruloylated arabinan and (1“ 4)linked galactosyl oligosaccharides. Guillon and Thibault [41] (Ref. on gel formation therein) reported that pectic polysaccharides of sugar beet having ester-linked feruloyl residues on arabinan and (1“ 4)-linked galactosyl oligosaccharide also formed gels by oxidative cross-linking with peroxidase or ammonium peroxysulfate treatment. The formation of dehydrodiferuloyl bridges could terminate the expansion of cell growth in grasses. Kamisaka et al. [42] showed that the

Fig. 4. Structure of proposed covalent diferulate cross-link between polysaccharides.

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Fig. 5. Structure of photo-dimer (1) and dehydrodimers (2–8) of ferulic acid released by alkaline treatment of grass cell walls.

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121

Fig. 6. Structure of mesomeric radicals of reruloyl ester.

increase in content of ferulic and dehydrodiferulic acids in oat (A6ena sati6a) coleoptiles after sowing, is closely related to the decrease in wall extensibility and to the increase in minimum stress relaxation time and relaxation rate of walls. These authors also showed that irradiation with white light decreased wall extensibility of rice coleoptile and that this was correlated with an increase in the contents of ferulic and dehydrodiferulic acids ester-linked to arabinoxylan [43]. Feruloyl and diferuloyl esters between cell wall polysaccharides have been implicated in the aggregation of cultured rice cells. Kato et al. [44] showed that the content of ferulic and dehydrodiferulic acids in the walls of suspension cultured rice depended on the composition of culture medium. When the cells were grown in amino acid (AA) medium, the content of ester-linked hydroxycinnamic acids in the walls became lower than that in Gamborg’s B5 medium, and the cells grown in AA medium produced more extracellular feruloylated polysaccharides and smaller cell clumps. Treatment of the cell aggregates grown in AA medium with carboxyesterase decreased the size of the aggregates by 1/2 to 1/10. Fry [45] reported that cell expansion of suspension cultured spinach was strongly promoted by gibberellic acids. He proposed that the promotion of growth by gibberellic acids was inhibited by phenolic substrates and peroxidase, which catalyzed oxidative coupling of feruloyl residues of pectins in spinach cell cultures. Photodimerization of esterified hydroxycinnamic acids (Fig. 5(1)) was reported to occur in walls of many grasses [46]. Formation of a series of head-to-tail and head-to-

head homo- and hetero-cyclobutan type dimers of ester-linked p-coumaric and ferulic acids has been demonstrated. Photodimerized hydroxycinnamic acid esters are reported in both unlignified and lignified walls, but not in primary cell walls [46]. Fry [47] reported that 14C-labelled cinnamate was very rapidly taken up by cultured spinach cells and that the incorporated 14C-labelled products had properties of oxidatively coupled phenolics with highly Driselase-resistant wall components. Carpita [48] showed that significant amount of aromatic material was incorporated into walls of maize coleoptiles after the elongation stopped. Considerable amounts of ferulic acid and small amount of diferulic acid were released by saponification, but there was still a significant amount of aromatic compounds in the unsaponifiable residues. These could be involved in crosslinking the wall. Until recently the 5-5-coupled dehydrodimer of ferulic acid was reportedly the only one produced from peroxidase/H2O2-mediated oxidative coupling of ferulic acid moieties synthetically esterified to guaran polysaccharide [38]. Ralph et al. [49] synthesized seven 13C-labeled dehydrodimers of ferulic acid expected from radical coupling of ferulate (Fig. 6). These workers were able to confirm the presence of these dehydrodimers of ferulic acid in the extracts of saponified walls of a range of grasses (Fig. 5(2–8)) by neulear magnetic resonance (NMR) spectroscopy [49], GLC, GLC coupled with mass spectrometry (MS) [50], and HPLC [51]. These newly identified dehydrodimers would be most likely ester-linked to wall polysaccharides. Purification and identification of these

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dehydrodimers of ferulic acid carrying oligosaccharides derived from wall polymers remains challenging work. Feruloyl esters on polysaccharides can become opportunistically involved in lignin cross-linking by trapping lignin quinone methide intermediates [52,53] and/or can be directly involved in the freeradical polymerization process [3,49,54,55]. In the former process, a benzylaryl ether (simple aetherified structure) would form. Scalbert et al. [52] proposed that ferulic acid would form covalent feruloyl ester-ether bridges between polysaccharides and lignins on the basis of model experiments. Iiyama et al. [56] used low and high temperature alkaline treatment to quantify the extent of esterification and a-aryl esterification, respectively, of walls of mature and maturing wheat internodes. All the ferulic acids etherified to wall polymers were also esterified to polysaccharides. p-Coumaroyl residues are not involved in similar bridges [57]. Diferulic acid in the form of diester bridges between polysaccharides chains would also be etherified to lignin [5,58]. Peroxidase-catalyzed co-polymerization of feruloyl polysaccharides with lignin monomers results in a variety of structures. Helm et al. synthesized 13 C-labelled feruloylated and p-coumaroylated methyl glycosides [59] and feruloylated arabinosyl-xyloses (F-Ara-Xyl) [60]. They showed by 2-dimensional (2D) NMR spectroscopy that the feruloyl arabinosyl residues are incorporated into a synthetic lignin dehydrogenation polymer (DHP) of coniferyl alcohol by a peroxidase-catalyzed co-polymerization [3,49,50]. The incorporation of feruloyl esters into DHP resulted in all the expected radical coupling structures, some of which would not release ferulic acid by solvolytic schemes currently used for quantitation of ferulic acid in plant material. The authors also suggested that most of the ferulate was incorporated into the lignin via oxidative coupling mechanisms [49]. They claimed that the content of total ferulates in grass walls was extremely underestimated. a-Aryl ether linkages were not predominant linkages of ferulic acid to lignin, which was expected from the quinone methide intermediate mechanism [50]. Ralph et al. [53,54] also provided evidence that feruloyl polysaccharides act as initiation or nucle-

ation sites for lignification in grasses. Application of 13C NMR spectroscopy to uniformly 13C-labelled ryegrass enabled the detection of polysaccharide-ferulate-lignin coupling in plants. Diagnostic NMR spectra showed that ferulate is oxidatively coupled with lignin monomers in vivo producing ferulate-mediated polysaccharide-lignin cross-linkages. Cross-linking of arabinoxylans by ferulate dehydrodimers and incorporation of feruloylated arabinoxylans into lignin have also been shown in oat cell walls [54]. p-Hydroxylcinnamyl alcohols were also polymerized into maize walls to produce DHP-cell wall complexes [61]. Jacquet et al. [62] isolated ether-linked ferulic acidconiferyl alcohol dimer from saponified products of wheat and oat straw. These ferulate esters would be points of growth for the lignin polymers, via ether bonds that anchor lignin to wall polysaccharides.

5. Biological activity of feruloylated oligosaccharides Several oligosaccharides derived from plant cell walls and microrganisms (oligosaccharins) are biologically active [63] (Refs therein). Oligogalacturonides, which are found in enzymatic hydrolyzates of pectic polysaccharides are known as signal molecules between plants and microorganisms, and as regulators of growth and development in plants. Xyloglucan oligosaccharides and oligogalacturonides show inhibitory effects on auxin and gibberellin stimulated growth of pea. It has been reported that phenolic compounds are also involved in signal transduction between plants and microorganisms [64]. Feruloyl oligosaccharides derived from feruloyl polysaccharides also have biological activity. Actually, 10 − 4 M (F-Ara)-(1“ 3)-Xyl-(1“ 4)-Xyl and Xyl(1“4)-{(F-Ara)-(1“ 3)-Xyl-(1“ 4)}-Xyl inhibited auxin stimulated cell growth of rice [65]. The product of removal of ferulate from (F-Ara)-(1“ 3)-Xyl-(1“ 4)-Xyl (i.e. Ara-(1“3)-Xyl-(1“ 4)Xyl) had no activity. However, ferulic acid also had similar activity, but the response was smaller than for (F-Ara)-(1“ 3)-Xyl-(1“ 4)-Xyl on a mo-

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lar basis. These observations indicated that the feruloyl substituent of (F-Ara)-(1 “4)-Xyl-(1 “ 4)-Xyl was essential for the inhibitory effect, but the glycosyl portion Ara-(1“3)-Xyl-(1 “ 4)-Xyl of (F-Ara)-(1“ 3)-Xyl-(1 “4)-Xyl was also important for full inhibitory activity. Biological activity of feruloylated oligosacchrides was investigated using a modified micro-drop bioassay [66]. When dwarf rice was treated with gibberellin biosynthesis inhibitor, gibberellin-induced cell elongation was inhibited by (F-Ara)-(1“3)-Xyl(1 “ 4)-Xyl and Xyl-(1 “ 4)-{(F-Ara)-(1 “ 3)-Xyl(1“ 4)}-Xyl. The mechanisms of the inhibitory effects of feruloyl oligosaccharides remain unsolved. Antioxidative activity of feruloyl arabinoxylan fragments including F-Ara and (F-Ara)-(1“ 3)-Xyl-(1 “4)-Xyl was reported [29].

6. Biosynthesis and biodegradation of hydroxycinnamic acid esters There is not complete agreement on to the site of feruloylation of wall polysaccharides or the nature of the feruloyl donor. Fry and Miller [67] administered [3H] arabinose into spinach cultured cells and traced its incorporation into (F-Ara)Ara units of the major wall polysaccharides. The authors showed that arabinosylation and feruloylation occurred co-synthetically and intracellularly. On the other hand, in maturing barley coleoptiles Yamamoto et al. [68] suggested that polysaccharide-bound ferulate increased continuously for at least 1 day after total polysaccharide accumulation had ceased. Isolated barley coleoptile walls incubated with [2-14C] feruloyl-CoA showed a linear incorporation of the radioactivity into the walls for up to 3 h and this was 4-times higher than the rate of incorporation of [2-14C] ferulic acid itself, suggesting that feruloylation site is located within the matrix of barley coleoptiles walls. Meyer et al. [69] showed that [2-14C] feruloylCoA is a donor for feruloylation. A microsomal preparation from suspension cultured parsely (Petroselinum crispum) cells was able to transfer ferulic acid from feruloyl-CoA to uncharacterized endogeneous wall polysaccharides. An alternative

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feruloyl donor may be the glycosidic ester of ferulic acid, (1-O-feruloyl-b-D-Glc). Mock and Strack [70] demonstrated that 1-O-sinapoyl-b-DGlc is formed by UDP-Glc: hydroxycinamate Dglucosyltransferase (EC 2.4.1.120). The feruloylation and p-coumaroylation of cell wall polysaccharides occurs on highly specific hydroxy groups of polysaccharides. When these hydroxycinnamic acids undergo oxidative phenolic coupling reactions in walls, the coupling reactions themselves would be also remarkably specific. To permit a coupling reaction, feruloyl groups on the same or a different polysaccharide chain must be juxtaposed. Matrix polysaccharides could be imagined in gelatinous form and they would have enough mobility to place feruloyl residues in close proximity. But at present there is no definite proof for this theory [5]. Peroxidases are candidates for the catalysis of the dehydrogenative dimerization of feruloyl residues in the cell wall. The peroxidases not only generate the free radical intermediates of ester-linked feruloyl residues, but may also generate the hydrogen peroxide needed to achieve this from various hydrogen donors. Several mechanisms have been proposed for hydrogen donor generation [71]. Ogawa et al. [72] showed that one of the physiological functions of the cytosolic CuZn-superoxide dismutase was supplying hydrogen peroxide for lignification. Some anaerobic rumen fungi produce high levels of both p-coumaroyl and feruloyl esterases [73]. One p-coumaroyl [74] and two feruloyl [75] esterases have been purified to homogeneity from an anaerobic fungus Neocallimastix MC-2. Culture supernatants of Streptomyces oli6ochromogenes [76], Schizophyllum commune [77], and S. 6iridosporus [78] also have feruloyl esterase activity. Feruloyl esterases have been purified to homogeneity and the enzymes partly characterized from S. oli6ochromogenes [79,80], Pseudomonas fluorescens [81], Penicillium pinophilum [82], and several from Aspergillus niger [83–87]. The feruloyl esterases could be classified by their characteristic substrate specificities. Each enzyme recognizes specific substitutions on the aromatic ring. For example, one form of feruloyl esterase from A. niger was specific for ferulic, p-coumaric, and caffeic acids, while another form was specific

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for ferulic and sinapinic acids [85]. Ralet et al. [86] demonstrated that different kinds of ferulic acid esterases existed with different specificities for the feruloylated oligosaccharides. Although certain hydroxycinnamic acids are undigestible or even toxic to many soil and ruminant bacteria [88], some microorganisms can utilize hydroxycinnamic acids as carbon sources [89].

7. Future studies Over the past several years it has become clear that hydroxycinnamic acids are a key component in the wall and a regulatory factor for wall development. The strategy for future studies probably requires following subjects. 1. Structural characterization of the polysaccharides cross-linked with hydroxycinnamic acid derivatives is a key step for understanding the formation of ferulate-polysaccharides complexes in the wall. Identification of a dehydrodiferuloyl arabinoxylan hexasaccharide is the only one experimental evidence that dehydrodiferuloyl crosslinkage of arabinoxylan actually occurs in walls. However, it is uncertain whether the identified 5-5 dehydrodiferuloyl cross-linkage of polysaccharides occurs between inter- or within intrapolysaccharides. Recent results show that a 5-5 coupled dehydrodiferuloyl dimer is only one of several oxidative coupling dehydrodimers of ferulic acid. Other dehydrodiferuloyl dimers esterlinked to polysaccharides appear to be present in walls. Different polysaccharides cross-linked through dehydrodiferuloyl residues would be more effective to mechanically strengthen wall polymers. The extent of their occurrence would provide essential information on the 3-dimensional organization of wall components. 2. Understanding the biosynthesis of feruloyl polysaccharides and the regulation of cross-linking are also important to clarify the mechanisms of wall elongation and cell development. Identification of key components and their regulation for incorporation into cell wall matrices will open the door to genetic manipulation of plants either by traditional germplasm development or molecular genetics.

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