Molecular Plant Advance Access originally published online on August 24, 2009
Molecular Plant 2009 2(5):861-872; doi:10.1093/mp/ssp067
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Feruloylation in Grasses: Current and Future Perspectives
Department of Biology, 208 Mueller Laboratory, Pennsylvania University, University Park, PA 16802, USA
1 To whom correspondence should be addressed. E-mail mmb26{at}psu.edu, tel. 814-867 0223.
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Abstract |
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 TOP Abstract INTRODUCTIONFERULIC ACID: ITS ASSOCIATION...THE BIOCHEMISTRY OF...DISCUSSIONFUNDING |
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In the cell walls of forage grasses, ferulic acid is esterified to arabinoxylans and participates with lignin monomers in oxidative coupling pathways to generate ferulate–polysaccharide–lignin complexes that cross-link the cell wall. The accumulation of ferulates and the cross-linking of arabinoxylans via diferulate esters are hypothesized to function in various processes in plants. The specific roles of arabinoxylan feruloylation as well as the nature, cellular localization, and substrate for arabinoxylans feruloylation of cell walls are reviewed. The various approaches that have been used for assessing the specific roles of feruloylation are described and assessed. I argue that, until recently, the specific role of feruloylation in these various processes has been established largely by indirect experiments and, although these studies reached similar conclusions about the potential importance of wall feruloylation, they suffer from a common problem: namely they depend on correlations between two processes and do not stem from a detailed understanding of the mechanisms of feruloylation. I also argue that the nature of arabinoxylan feruloylation remains uncertain.
Key Words: Cell wall • feruloylation • ferulic acid • cross-link • dehydrodiferulate • grasses
Received for publication June 8, 2009. Accepted for publication July 21, 2009.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONFERULIC ACID: ITS ASSOCIATION...THE BIOCHEMISTRY OF...DISCUSSIONFUNDING |
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The presence of polysaccharide-bound hydroxycinammic acids (HCAs) (p-coumaric, sinapic and ferulic acid) in the cell walls of different plant species has long been known (Bunzel et al., 2003b; Brett et al., 1999; Chen et al., 1998). Of these, ferulic acid (FA) (4-hydroxy-3-methoxy-cinnamic acid) and
-coumaric acid (4-hydroxy-cinnamic cid) are common constituents in the cell walls of several plant families (Jung and Himmelsbach, 1989). Ferulic acid represents up to 3% of the dry weight of graminaceous cell walls (Kroon and Williamson, 1999; Saulnier et al., 1999), about 0.9% by weight of rice endosperm cell walls (Shibuya, 1984), 3.1% in maize bran (Saulnier et al., 1995), and dominates the monomeric fraction of ester-linked HCAs of Chinese water chestnut (Parr et al., 1996). Ferulic acid [first isolated in 1866 from Ferula foetid (Fazary and Ju, 2007)], is derived from phenylpropanoid metabolism (Ou and Kwok, 2004), is found in both primary and secondary grass cell walls (Harris and Hartley, 1976), and is most abundant in the epidermis, xylem vessels, bundle sheaths, and sclerenchyma (Faulds and Williamson, 1999; Lambert et al., 1999).
Ferulic acid residues are mainly introduced into the cell wall polysaccharides of grasses via an ester linkage between the carboxylic acid group of ferulic acid and the primary alcohol on the C5 carbon of the arabinose side chain of arabinoxylans (AXs) (Hartley and Ford, 1989; Ralph and Helm, 1993) but can also be covalently linked to lignin monomers via an ether linkage (Scalbert et al., 1985; Kondo et al., 1990) and can be released by alkaline hydrolysis at room temperature or by acid hydrolysis (see Lam et al., 1994).
It is suspected that hydroxycinnamic acids are very important components not only for the biology of the cell wall, but also for its structure because they can be coupled by peroxidase-mediated oxidative coupling to form a variety of dehydrodiferulate dimers, cross-linking polysaccharide chains (Hatfield et al.,1999a; Ralph et al., 1994; Brett and Waldron, 1996). In addition, feruloylation of AX is also considered important because it may act as a nucleating site for the formation of lignin and for the linkage of lignin to the xylan/cellulose network via lignin–ferulate–xylan complexes (Iiyama et al., 1994; Jacquet et al., 1995; Bartolome et al., 1997). Bonding between these two abundant polymers in the lignified walls of grasses contributes, as many studies have shown, to the low digestibility of most grass species even by ruminants and, in part, to the recalcitrance of grass tissues to direct degradation by simple mixtures of cellulases and xylanases (Eraso and Hartley, 1990; Grabber et al., 1998; Iiyama and Lam, 2001; Lam et al., 2003). The creation of these cross-links has also been postulated to have a number of other important roles, such as in controlling cell wall extensibility (Fry, 1979) and protecting against pathogen invasion (Ikegawa et al., 1996).
Since its discovery, FA has also been reported to exhibit a wide range of important biological and therapeutic properties. These include anti-inflammatory, anti-bacterial, anti-diabetic, anti-carcinogenic, anti-aging, and neuro-protective effects, which can be attributed to its antioxidant capacity because of its phenolic nucleus and extended side chain conjugation (Ou and Kwok, 2004).
It can be argued that grasses are the most important plants to human society. They constitute a major food source either through direct human consumption of grain—the cereal crops such as wheat (Triticum aestivum), rice (Oryza sativa), oats (Avena sativa), and maize (Zea mays)—or indirectly through animal grain and forage-fed diets. Grasses therefore constitute the main source of energy for the world's livestock, currently playing an important role in animal production and providing the basis of the animal industry. In recent years, realization of the impeding shortage in petroleum has led to a growing interest in domestic, renewable alternatives for gasoline and diesel fuels. Grasses species are emerging as potential feedstock for the production of ethanol (Hamelinck et al., 2005; McLaren, 2005).
An understanding of the nature and roles of arabinoxylan feruloylation, such as its cellular localization and the substrate for arabinoxylan, feruloylation, is fundamental to breeding new material with reduced feruloylation and so promote the production of more digestible grasses for biofuels from currently recalcitrant grass cell walls.
This review covers the attempts carried out to date aimed at uncovering the secrets of FA esterification and is divided into two sections. The first section gives an overview of ferulic acid in plant cell walls, its association with lignin/polysaccharides, and the proposed roles of ferulate cross-linking in determining grass cell wall properties, while the second section focuses on the proposed cellular locations of arabinboxylan feruloylation and candidate substrates. The various approaches used so far for assessing the specific roles of feruloylation and to establish its nature, and the information and conclusions drawn from them will be assessed. As this review illustrates, the different aspects of feruloylation, its consequences for cell wall properties, as well as its nature, are still quite unclear and new avenues need to be exploited in order to uncover the secrets of feruloylation of AX in grasses.
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FERULIC ACID: ITS ASSOCIATION WITH HEMICELLULOSE AND LIGNIN |
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TOPAbstractINTRODUCTIONFERULIC ACID: ITS ASSOCIATION...THE BIOCHEMISTRY OF...DISCUSSIONFUNDING |
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Arabinoxylan in Grasses
Cell walls are complex multifunctional structures that serve several important roles in the life of plants. They are composed of cellulose microfibrils embedded in a matrix of hemicelluloses, pectins, proteins, and phenolic substances (Carpita and Gibeaut, 1993; Carpita and McCann, 2000). The cell walls of grasses are distinctive in composition, with xylans usurping the roles of some of the other more common matrix polysaccharides (Carpita and Gibeaut, 1993; Carpita, 1996). Unlike cellulose, which is present in all plants as a non-branching polymer of β-1,4-linked glucose units, xylan is more complex in that it is composed of a backbone of 1,4-linked β-D-xylopyranose units forming a xylan backbone and of side chains connected to the backbone. The xylans of primary walls typically have arabinose and glucuronic acid side chains, referred to as arabinoxylans (AX) or glucuronoarabinoxylans (GAX). The arabinoxylans in grasses serve a major structural role by binding to cellulose microfibrils and becoming oxidatively cross-linked with each other and with lignin by hydroxycinnamic acid residues attached to arabinoxylan (Scalbert et al., 1985).
Growing cells contain highly substituted AXs in contrast with less branched xylans in fully elongated cells (Carpita, 1984a, 1984b). The level of arabinosyl substitution decreases considerably as cells stop elongating and, at the same time, the percentage of ferulated arabinosyl units increases (Carpita, 1984b, 1986). The gradual removal of arabinosyl residues during growth has been suggested to be mediated by the action of arabinoxylan and arabinofuranohydrolases (Lee et al., 2001). These feruloyl residues may make a significant contribution to the stability of the plant cell wall and increase its resistance to hydrolysis.
Although AXs are important components of grass cell walls, little is known about the details of their biosynthesis. It is generally accepted, however, that the synthesis of matrix polysaccharides (such as AX) in plants takes place within the Golgi apparatus and that following synthesis, they are carried in Golgi-derived vesicles, which fuse with the plasma membrane, whereupon their contents assemble with pre-existing polysaccharides in the wall (Ray et al., 1969; Fincher and Stone, 1981). It has been suggested that various type I glycosyl transferases (GT) might be involved in the synthesis of the xylan backbone as discussed by Fincher (2009) but none has yet been shown to functionally encode GTs involved in the synthesis of AX. However, xylosytransferase and arabinosyltransferase activities have been detected in membrane preparations from grasses (Porchia and Scheller, 2000; Kuroyama and Tsumuraya, 2001; Urahara et al., 2004; Zeng et al., 2008) but have yet to be purified to the extent to which their amino acid sequences can be obtained. York and O'Neil (2008) discuss specific aspects of several models for xylan biosynthesis and suggest that such modeling might be a useful tool to be used to design experiments to study xylan synthesis. They also summarize evidence for a large number of enzymes and genes required to build the AX backbone.
Feruloylation in Monocots
In monocots, FA is attached to cell wall polymers by either ester bonds through its carboxylic acid group with the C5-hydroxyl of 
-L-arabinosyl side chains of xylans (Figure 1) (Hartley and Ford, 1989; Ralph and Helm, 1993; Wende and Fry, 1997) or via ether bonds to lignin, with its hydroxyl group covalently linked to lignin monomers (Kondo et al., 1990; Scalbert et al., 1985). Evidence that AX is feruloylated comes from the isolation and identification of phenol–carbohydrate conjugates. These include FAX (3-O-(5-O trans feruloyl--L-arabinofuranosyl)-D-xylose) (Smith and Hartley, 1983) and FAXX (4-O-(3-O-(5-O-feruloyl--L-arabinofuranosyl)-β-D-xylanopyranosyl)-D-xylose) (Mueller-Harvey and Hartley, 1986) that are produced via the enzymatic hydrolysis of the xylan backbone. Polysaccharide-bound FA occurs widely in graminaceous plants, such as barley grain (Bartolome et al., 1997), wheat bran (Faulds and Williamson, 1995, 1990) barley straw (Mueller-Harvey and Hartley, 1986), rye (Andreasen et al., 2000), Lolium (Hartley and Jones, 1976), rice (Bunzel et al., 2002), maize bran (Faulds et al., 1995; Allerdings et al., 2006), Phalaris (Lam et al., 1992a,b), bamboo (Ishii, 1991), Avena (Kamisaka et al., 1990), and oat (Tan et al., 1992); among other monocots, they have also been identified in the bromeliaceae (pineapple) (Smith and Harris, 2001).
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Feruloylation in Dicots
In contrast to monocots, ferulic acid in dicots is associated with pectic polysaccharides via ester linkages to the C-2 hydroxyl group of arabinofuranose or the C-6 hydroxyl group of galactopyranose residues. Such linkages have been found in spinach (Fry, 1982) and sugar beet (Colquhoun et al., 1994; Ralet et al., 1994). It has been estimated that 45–50% of FA is linked to O-6 of galactose residues and 50–55% to O-2 arabinose residues in sugar beet pulp (Ralet et al., 1994). Spinach culture cell walls have approximately 10 feruloyl groups per 1000 pectic sugar residues (Fry, 1982). Ferulic acid has also been reported in Arabdopsis (Nair et al., 2004; Rohde et al., 2004; Derikvand et al., 2008), parsley (Kauss et al., 1993), and alfafa (Chen et al., 2006) cell walls.
Ferulate Cross-Linking and the Ferulate–Polysaccharide–Lignin Complex
Ferulic acid esterified to cell wall polysaccharides has the ability to form dimers cross-linking AX (see Figure 2). Two different mechanisms have been proposed for the formation of ferulate cross-linking of hemicelluloses to lignin: (1) oxidative phenol coupling mediated by hydrogen peroxide and peroxidases (Wallace and Fry, 1995; Fry, 2000) and (2) dimerization and photoisomerism by UV light (Ford and Hartley, 1990). It has been reported that peroxidase activity has a negative correlation with the rate of cell expansion (Fry, 1979; MacAdam and Grabber, 2002).
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The first FA dimer discovered was the 5-5'-dehydrodimer, isolated after alkaline hydrolysis of the cell wall polysaccharides (Harris and Hartley, 1976). Since then, a number of dehydrodimers have been identified and characterized in different grass species. The major forms are: 5-5'-DiFA: (E,E)- 4-4'-dehydroxy-5-5’ dimethoxy-3'-bicinnamic acid; 8-0-4'-DiFA: (Z)-β-4-hydroxy-3-methoxy-cinnamic acid; 8-5'-DiFA: (E-E)-4-4'-dihydroxy-3,5'-dimethoxy-β,3'-bicinnamic acid; 8-5'-C (benzofuran form): trans-5-((E)-2-carboxyvinyl))-2-(4-hydroxy-3-methoxyphenyl)-7-methoxy-2,3-dihydrobenzofuran-3-carboxylic acid, and 8-8'- DiFA (4,4'-dihydroxy-3,3'-dimethoxy-β,β‘- bicinnamic acid) (see Ralph et al., 1994 or Waldron et al., 1996 for structures).
Ferulate and diferulates have been found in a variety of plant species but it has only been with the improved analytical techniques over the last 15 years that their accurate identification and quantification have become possible. Some of the species in which the levels of esterified ferulate dimers have been quantified include: tall fescue (MacAdam and Grabber, 2002; Buanafina et al., 2008), Italian ryegrass (Buanafina et al., 2006); barley grain (Bartolome et al., 1997), maize (Grabber et al., 1998), bamboo (Ishii, 1991), and water chestnut (Parr et al., 1996). Ferulate and diferulate contents have been estimated to be 25 g kg–1 in maize stems (Saulnier and Thibault, 1999), and 4.5 g kg–1 in Chinese water chestnut (Parr et al., 1996), and Figure 3 shows the levels of ferulate monomers and dimers in mature leaves of three different grass species.
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More recently, some specific ferulate dehydrodimers (Bunzel et al., 2003a; Funk et al., 2005) and tetramers have been isolated and identified in a variety of plant tissues (Rouau et al., 2003; Bunzel et al., 2008). The predominance of trimers and larger polymer (oligoferulates) coupling products over ferulate dimers have been reported in studies using maize culture cells fed with [14C]cinnamate (Fry et al., 2000). The authors also suggested that these oligoferulates are the major contributors to the cell wall cross-linking in maize cell cultures.
The concentration of alkali-labile ferulates initially increases during primary wall formation and then peaks and declines during secondary wall formation and lignification (Morrison et al., 1998; Scobbie et al., 1993). This reduction in measurable ferulates during later stages of cell wall formation has been used to support the contention that ferulate deposition is limited to primary cell walls (Jung and Deetz, 1993). However, recent studies have shown that at least 50–70% of alkali-labile ferulate deposition occurs during secondary wall formation and lignification (Jung, 2003; MacAdam and Grabber, 2002).
Less work has been carried out quantifying the dimer content of different cell types or in different tissues, or if these different ferulate dimers have different physiological roles. Differences in terms of varying patterns of cell wall ferulate and dehydrodiferulate ester content in different sugar beet seedling tissues have been reported by Wende et al. (2000). Their data suggest corresponding variations in biosynthetic processes.
Immunocytochemical studies with maize stems also indicate that ferulates are deposited in lignified walls of secondarily thickened xylem, sclerenchyma, phloem fibers, and parenchyma tissues (Migne et al., 1998). In mature sorghum, ester and ether-linked ferulate concentrations were greater in sclerenchyma and vascular tissues than in pith parenchyma and epidermal cells (Hatfield et al., 1999b).
Very recently, Burr and Fry (2009) provided further evidence for esterified oligoferulates being more prevalent than ferulate dimers in cross-linking arabinoxylans in non-lignified maize (Zea mays) cell cultures radiolabeled with L-[1-3 H]arabinose or (E)-[U-14C]cinnamate or with exogenous feruloyl-[3H]arabinoxylans. They also proposed that ether-like bonds are formed between ferulates and polysaccharides via quinone-methide intermediates and claimed these bonds are formed during and after cross-linking. Results from Grabber et al. (1995) suggest that the spatial orientation of these feruloylated polysaccharides maximized cross-linking, and that the level of cross-linking is limited by the availability of hydrogen peroxide, which is essential for extracellular dimer formation, strongly suggesting that the formation of diferulate cross-links is a highly organized and regulated process.
In theory, there are three possible places where ferulates attached to polysaccharides can undergo oxidative coupling, cross-linking polysaccharides to which they are attached: (1) intracellularly, before polysaccharides are secreted to the wall; (2) in muro following secretion; and (3) in muro after wall-binding. Studies of the kinetics of radio-labeling of diferulates following the feeding of [14C]cinnamate to maize cell-suspension cultures (Fry et al., 2000) supports the hypothesis that ferulic acid dimer formation begins in the intra-protoplasmic space (within the first minute after their attachment to polysaccharides) before secretion to the wall. It has also been proposed that the formation of dimerferulates, trimerferulates, and higher molecular oligoferulates is likely to take place extracellularly (apoplastic), being mediated by cell wall H2O2 and peroxidase (Grabber et al., 1995, 2000; Lindsay and Fry, 2008; Burr and Fry, 2009). Further evidence for oxidative coupling of feruloyl groups, in the apoplast with inter-strand dimer and trimer formation mediated by endogenous apoplastic H2O2 and wall-localized peroxidase, comes from wall-binding studies using radiolabeled model substrate FAXX from maize cell walls (Encina and Fry, 2005). Obel et al. (2003), using wheat cell suspension cultures fed with [14C]ferulic acid, have suggested that intracellular ferulate oxidative coupling is limited to 8,5'-diferulic acid, whereas other dimers are formed in muro. Recent studies (Lindsay and Fry, 2008), in which dicot and monocot cell-suspension cultures were fed with [14C]cinnamate, showed that at least six dehydrodimers were formed rapidly intra-protoplasmically but only gradually in muro. Feruloyl coupling taking place in the intracellular space indicates that part of the feruloylated polysaccharides are secreted into the cell wall already cross-linked, which would have crucial consequences for cell wall assembly mechanisms and reinforces the role of ferulate coupling. The bifunctional ability of FA to participate in ester linkages and phenol coupling reactions confers it with the ability to covalently attach polysaccharide with lignin. The resultant product is a ferulate–polysaccharide–lignin complex bonded through ester–ether linkages (Scalbert et al., 1985; Jacquet et al., 1995). Evidence for hydroxycinnamic acids (HCAs) being able to bridge lignin with polysaccharides comes from the release of ether-linked ferulates after hot alkaline hydrolysis of cell walls (Iiyama et al., 1990). Evidence for the incorporation of ferulates (attached to C5 of arabinose units) into ryegrass lignin comes from NMR spectrometry, demonstrating that arabinose-linked FA couples with coniferyl and sinapyl alcohol monomers (Ralph et al., 1995). This study indicated that ferulates could function as initiation or nucleation sites for lignification. Thus, FA deposition in the wall may not only lead to cell wall cross-linking during plant growth and development, but may also regulate the non-random pattern of lignin formation within the wall.
Implications of Diferulates Cross-Linking for Cell Wall Properties
Once these feruloylated polysaccharides are dimerized and incorporated into the cell wall, the cell wall undergoes a significant alteration in a number of properties.
Growth Cessation
One of the proposed consequences of FA cross-linking of the cell wall matrix polysaccharides is that it causes cell wall stiffening and growth deceleration. Evidence for a role of FA cross-linking during growth cessation comes from a number of studies on Avena coleoptiles, Festuca leaves, and rice internodes (Kamisaka et al., 1990; MacAdam and Grabber, 2002; Azuma et al., 2005). Kamisaka's group found that the amount of ferulates and diferulates bound to the cell wall polysaccharides of Avena coleoptiles correlated with mechanical stiffness of the walls (Kamisaka et al., 1990; Tan et al., 1992). Likewise, in Festuca leaves, the accumulation of ferulate dimers esterified to the cell wall was correlated with a deceleration in leaf elongation (MacAdam and Grabber, 2002). Azuma et al. (2005) also found that levels of ferulic and diferulic acids in the cell wall correlated with the cessation of rapid elongation of submerged floating rice internodes. Given the above observations, one can argue that the degree of cross-linking is highly regulated to facilitate normal cellular expansion associated with growth. Indeed, the plant growth regulator Gibberrellin is believed to lower the apoplastic peroxidase activity and thus encourage cell elongation/expansion (Fry, 1980).
Resistance to Pathogens and Insects
There is some evidence in the literature that ferulates and diferulates are also involved in plant protection against pathogen invasion (Lyons et al., 1993; Bergvinson et al., 1994; Bily et al., 2003; Garcia-Lara et al., 2004). Lyons et al. (1993) investigated the distribution of phenylpropanoids during disease development in resistant and susceptible maize cultivars to Helminthosporium maydis and reported greater levels of ferulates and p-coumarate produced in the resistant cultivar. Ikegawa et al. (1996) subsequently reported the formation of diferulic acid in oat leaves during the hypersensitive response to Puccinia coronata infection and suggested that these diferulates may contribute to locally induced resistance in that species by providing a barrier to the invasion of the pathogen. Similar results have also been found in maize pericarp and aleurone tissues in response to Fusarium gramianearum (Bily et al., 2003). A recent study with maize genotypes that differ in their resistance to the Mediterranean corn borer (Sesamia nonagrioides) also showed significant negative correlations between the level of cell wall esterified diferulic acid content in leaves of maize and larvae weight (Santiago et al., 2006).
Cell Wall Degradation
Ferulate substitution and diferulate cross-linking of xylans are also hypothesized to result in structurally hindering both the rate and extent of cell wall degradation by both ruminant microbes (Eraso and Hartley, 1990) and fungal enzymes (Grabber et al., 1998). The relationship between bound cell wall HCAs and their effects on the overall digestibility of plant material has interested plant scientists for many years. Van Soest (1963) was the first to show that forage grasses could be divided into two different classes based on their digestibility. One class was related to the very digestible material—the cellular content—whereas the second one was related to the less digestible—the cell wall. It was not until a couple of years later that a significant correlation between the digestibility of cell walls from perennial ryegrass and the p-coumaric/ferulic acid ratio was shown for the first time (Hartley, 1972). Since these initial studies, many other studies have confirmed the close relationship between the ferulate/diferulate ratio and cell wall degradability. Jung et al. (1991), for instance, used a synthetic model system, containing p-coumaric and ferulic acids esterified to hemicellulose, to show that the increased concentration of esterified phenolic acids was negatively correlated with in vitro digestibility. Iiyama and Lam (2001) and Lam et al. (2003) presented evidence for the negative effect of FA ester–ether bridges between lignin and AX on cell wall digestibility. Their results also support the conclusion that lignin alone in the cell wall of grasses is not in itself the most important factor regulating the in vitro digestibility. A negative correlation between the rate and extent of Festuca cell wall degradation on the one hand and the lignin and FA content on the other has also been reported (Vailhe et al., 2000). Grabber et al. (1995) developed an in vitro model system in which the level of ferulates, the formation of dehydrodimers, as well as the level and composition of lignin could be manipulated separately. They showed that increasing the level of ferulate dimerization resulted in a reduced initial hydrolysis of all sugars from the wall, suggesting that the access of hydrolytic enzymes to the polysaccharides was reduced as the xylan backbone was substituted. They also showed in a later study (Grabber et al., 1998) that reduction in ferulate–lignin cross-linking increased the initial and final extent of hydrolysis of the cell wall.
The studies on growth cessation and cell wall degradation described above reach a similar conclusion about the importance of wall feruloylation. However, they draw their conclusions from the correlations between the two processes. These studies would be strengthened by the ability to manipulate cell wall feruloylation and then examining the consequences for cell growth and cell wall properties.
It is well known that chemical treatment of low-quality feed such as cereal straw with alkali increases the biodegradability and nutritional value of such material (Jackson, 1997). The effect of alkali lies at least in part in the disruption of ester-linked HCAs. This observation supports the inhibitory role of phenolic cross-links for the degradability of grass cell walls. Taking a different approach, Buanafina et al. (2006, 2008) tested the expression of an Aspergillus ferulic acid esterase (FAEA), targeted to the vacuole, in Lolium multiflorum and Festuca arundinacea. Feruloyl esterases are a subclass of the carboxylic acid esterases that hydrolyze the ester bonds between hydroxycinnamic acids and sugars present in plant cell walls (Williamson et al., 1998). The enzyme was targeted to the vacuole to permit the release of the enzyme into the cell wall upon cell death, subsequently hydrolyzing FA esters in the cell wall and improving grass digestibility. They found that vacuole-targeted FAEA had the potential to break cell wall phenolic cross-links and to release cell wall monomers and dimers of FA, resulting in a more digestible grass. An experimental system in which the level of ferulates could be manipulated, as the cell wall is being formed, such as by targeting FAE expression to the apoplast, ER, or Golgi system, could prove to be ideal to test hypotheses about the cellular location of feruloylation and the importance of ferulate cross-linking for the control of plant growth, response of walls to wall-loosening enzymes, nucleation of lignin, degradability of walls by microbial and endogenous enzymes, and resistance to insect pests. More recently, Grabber et al. (2009), working with maize cell wall suspension cultures with normal and reduced feruloylation and artificially lignified with various monolignols, showed the impact of reducing ferulate–lignin cross-linking on fiber fermentability. Lignin, a complex hydrophobic polymer, in itself also appears to be a very significant factor hindering cell wall degradability. The two primary effects of lignin on the enzymatic hydrolysis of cellulose within the cell wall matrix comes from prohibiting cellulose fiber swelling, thus reducing the surface area exposed to the enzyme (Mooney et al., 1998) and by preventing cellulase action on cellulose because cellulase will adsorb to lignin (Palonen et al., 2004).
Understanding how the components of plant cell walls affect its degradability is a crucial factor that impacts the economics of animal nutrition and the utilization of these feedstocks for biofuel production. Much previous research was aimed at understanding the factors that limit forage cell wall degradability with the goal of improving their use as forage materials (Van Soest, 1963; Jung et al., 1983; Iiyama and Lam, 2001).
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THE BIOCHEMISTRY OF FERULOYLATION |
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TOPAbstractINTRODUCTIONFERULIC ACID: ITS ASSOCIATION...THE BIOCHEMISTRY OF...DISCUSSIONFUNDING |
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Evidence suggests that feruloylation in the Poaceae is an esterification reaction with high structural specificity. The fact that feruloyl groups are attached to cell wall polysaccharides in a very precise manner suggests that a ‘specific enzyme’ system is likely to be involved.
There are at least two possible potential mechanisms leading to arabinoxylan feruloylation as illustrated in Figure 4. First, AX may be synthesized (in the Golgi) and then feruloylated (possibly via feruloyl–CoA) (pathway 1), and then cross-linked, or, second, feruloyl–CoA reacted with UDP–Ara to make ‘Fer–Ara–UDP’, which could then conceivably act as a donor substrate, introducing a ready-made ‘Fer–Ara’ group into the nascent arabinoxylan via a feruloyl arabinoside transferase (pathway 2) and then cross-linked.
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While there are a number of feruloyl transferases that have been reported and characterized, their substrates are not of a similar structure to AX and it is postulated that they are involved in feruloylation of amines (Yu and Facchini, 1999), or hydroxyl-fatty acids (Lofty et al., 1992). As for the enzyme presumed to catalyze the feruloylation of AX, there has been one report on a feruloyl–CoA:arabinoxylan-trisaccharide O-hydroxylcinnamoyl transferase from rice (Yoshida-Shimokowa et al., 2001), which is suggested to catalyze the transfer of ferulic acid from Fer–CoA to AX trisaccharide.
As pointed out earlier, there is strong evidence showing that biosynthesis of the arabinoxylan backbone takes place intracellularly in the Golgi vesicles (Northcote and Pickett-Heaps, 1966; Moore et al., 1991; Zhang and Staehelin, 1992). Thus, it would be attractive to propose that the transfer of feruloyl groups onto polysaccharides occurs intra-protoplasmically, shortly after polysaccharide formation. This would occur prior to secretion to the cell wall, with little or no feruloylation occurring once polysaccharides were secreted to the wall. Evidence supporting this mechanism comes from work on spinach cell cultures (Fry, 1987) fed with [3H]arabinose, which demonstrated that arabinose residues of pectic polysaccharides began to be feruloylated intra-protoplasmically. Evidence for intracellular feruloylation of polysaccharides was also found from the kinetics of the labeling of polysaccharide-bound arabinose and feruloyl–arabinose residues in Festuca arundinacea cell cultures fed L-[1-3H]arabinose (Myton and Fry, 1994). In these cell cultures, non-cellulosic polysaccharides can fail to be retained by the wall and be released into the medium; it is therefore possible to estimate the time for a sugar to be incorporated into polymers and for those to be feruloylated. The authors show that [3H]arabinose residues were feruloylated about 1 min after incorporation into the polysaccharide, and 3H-polysaccharide appeared in the medium at least 15 min after first polysaccharide labeling (Myton and Fry, 1994). Intracellular synthesis of feruloylated arabinoxylan has also been reported in wheat cell cultures fed with [3H]arabinose and [14C]ferulic acid (Obel et al., 2003). It should be pointed out that [14C]ferulic acid substance can readily be oxidized by peroxidases in the apoplast, as free ferulic acid, prior to its uptake by the cells and possible future incorporation into AX. This limitation does not apply to [14C]cinnamic acid, which is not a substrate for peroxidase.
In contrast to this proposed mechanism, it is has also been suggested that feruloylation could take place in muro (Yamamoto and Towers, 1985), based on observations that in barley seedlings, ferulates bound to the wall continued to accumulate even after arabinose had stopped their deposition in the wall. However, no experimental evidence was actually given to support this. It is possible that the de novo synthesis of highly feruloylated arabinoxylans increases as cells age, thus increasing the ferulate:xylan ratio. It is also possible that ferulates might protect the AXs, to which they are esterified, from the natural enzymatic degradation process (Labavitch, 1981), leading to an increasing degree of arabinoxylan feruloylation.
More recently, Mastrangelo et al. (2009) provided evidence for feruloylation occurring not only intra-protoplasmically, but in muro as well. The study utilized wheat seedling root apical segments incubated with L-[1-14C]arabinose or trans-[U-14C]cinnamic acid as tracers and Brefeldin A (BFA) to block the secretory system in eukaryotic cells. They reported the appearance of apoplastic and protoplasmic [14C]ferulated polysaccharides shortly after radioactive feeding. The BFA interfered with the cell wall polysaccharides feruloylated into the endomembrane system but had no effect on in muro feruloylation.
The actual substrate for arabinoxylan feruloylation is also not well defined in this complicated process. So far, feruloyl–CoA is most often suggested as the donor substrate for the addition of FA to cell wall polysaccharides. In support of this, the transfer of FA from feruloyl–CoA to polysaccharides by a feruloyltransferase in microsomes from parsley suspension cultures has been reported (Meyer et al., 1991). This in vitro activity appeared to be localized in the Golgi-apparatus, although Kohler and Kauss (1997) later demonstrated that the incorporation of FA was into the protein fraction. Another study that supports feruloyl–CoA as the donor comes from experiments on maize cell cultures, which show that incorporation of radioactivity from [14C]cinnamate occurred first into hydroxycinnamoyl–CoA and then into feruloyl–polysaccharides (Fry et al., 2000). Yoshida-Shimokawa's rice cell suspension-culture assays also add additional evidence supporting feruloyl–CoA as the substrate donor for arabinoxylan feruloylation (Yoshida-Shimokawa et al., 2001). In their in vitro assay mixture, AX trisaccharide was the only acceptor substrate present. Furthermore, feruloyl–CoA as the only substrate donor present strongly suggests that Fea–CoA and AX are sufficient for AX feruloylation. One cannot, however, exclude the possibility of intermediates or changes of feruloyl–CoA before its incorporation as part of the picture.
In addition to FA–CoA as the donor substrate for the addition of FA to cell wall polysaccharides, feruloyl–glucose has also been suggested as a possible donor substrate for polysaccharide feruloylation (Bokern et al., 1991; Meyer et al., 1991; Obel et al., 2003). For example, Obel et al. (2003) reported that externally supplied FA was quickly taken up and converted to 1-0-feruloyl-β-glucose by wheat cell cultures and that the rate of arabinoxylan feruloylation correlated with the level of intracellular feruloyl–glucose. Their results are, however, inconclusive, mainly because the correlation that they reported was based on assuming that the feruloyl–arabinose released by mild hydrolysis originated from glycoproteins. In fact, feruloylated glycoproteins correspond to a minor cellular component.
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TOPAbstractINTRODUCTIONFERULIC ACID: ITS ASSOCIATION...THE BIOCHEMISTRY OF...DISCUSSIONFUNDING |
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Research has established that FA esters work as dimerization sites for feruloylated AXs and for the formation of ester–ether bridges between AX and lignin. Recently, larger products defined as oligoferulates that may predominate over ferulate dimers have been reported together with the presence of ether-like bonds formed between ferulates and polysaccharides, which reinforce polysaccharide cross-linking even further. Consequently, bonding between these two abundant polymers in lignified walls of grasses is the main cause for much of the difficulty in digestion of the lignified walls of grasses by ruminants and, in part, to the recalcitrance of grass tissues to direct attack by cellulases and arabinoxylanases. Despite these findings, the nature and control of cell wall feruloylation remain uncertain and controversial.
Examination of the possible reactants involved in the feruloylation of polysaccharides suggests that ferulic acid is unlikely to be the immediate reactant, as the activation of an acyl group is a requirement for the synthesis of an ester bond. It has been shown that both hydroxycinnamoyl–CoA and hydroxycinnamoyl–β-glucoside can act as acyl donors in enzymatic transesterification reactions in vitro (Zenk, 1979). Also, studies have shown that hydroxycinnamoyl–CoA and hydroxycinnamoyl-β-glucoside can be possible donor substrates for polysaccharide feruloylation. The hypothesis that feruloyl–glucosyl ester (1–Fer–Glc) is the donor substrate for adding Fer to AX in muro suffers from lack of evidence for the presence of this compound in the apoplast.
There is also controversy concerning the feruloyl acceptor and the hypothesis that UDP–arabinosyl is the first feruloylated intermediate and responsible for introducing a FA–Ara unit into the nascent polysaccharide via a feruloyl arabinoside transferase.
The exact location at which feruloylation takes place is another piece of the feruloylation puzzle to be solved. Studies have provided evidence supporting both the Golgi as well as the apoplast as sites for polysaccharide feruloylation. It is possible that both proposed locations are correct and that hydroxycinnamoyl–CoA and hydroxycinnamoyl–β-glucoside are both involved in polysaccharide feruloylation. It has been reported (Hu et al., 1999) that antisense down-regulation of 4-coumaroyl:CoA ligase in aspen leads to an increase in HCA esters in non-lignified cell wall material. This result suggests the existence of an alternate substrate for polysaccharide feruloylation, such as 1-O-feruloyl-β-glucose as proposed by Bokern et al. (1991). Previous attempts, as described above, to define the pathways for ferulic acid esters bond formation have used biochemical approaches with cell cultures of rice, Festuca, and wheat and have brought important information to light about different aspects of arabinoxylans-feruloylation. However, some aspects of AX feruloylation are still controversial and inconclusive. For instance, there has been one report of a feruloyl-CoA:arabinoxylans-trisaccharide O-hydroxycinnamoyl transferase, the enzyme presumed to catalyze the feruloylation of cell wall polysaccharide, but its isolation and extensive characterization have not come to light yet. Its characterization would elucidate some of the unknowns about feruloylation, such as the acceptor, donor for the enzyme, and where feruloylation takes place. To further investigate and elucidate the unknowns of feruloylation, it will be necessary to take both biochemical and cell biological approaches, such as addressing these issues by exploiting other approaches in which various possible intermediates in the feruloylation pathway would be separated and identified. Recently, Mitchell et al. (2007), using a bioinformatic approach, identified candidate genes in the GT61 (glycosyl transferase) family encoding feruloyl-AX B-1, 2-xylosyl transferase. This predicted protein, however, seems to lack signature motifs to direct it into the ER/Golgi system and does not seem to contain predicted transmembrane regions, indicating that it is likely to be located in the cytoplasm. This would pose a problem for its function in transferring ferulate onto AX. This approach, however, could be further explored by demonstrating the feruloyl transferase function by RNAi, for example, to evaluate the practical consequences of down-regulating expression in different grass species.
The spectacular advances in the last few years in genome sequencing and the availability of molecular markers in grasses such as SSRs, which provide efficient tools to link phenotype and genotypic variation (Alleman et al., 2006; Gale and Devos, 1998), together with model grasses with small genomes such as Brachypodium and the power of transgenics and induced tagged or chemical mutation emerge as strong tools to be used in the search for genes of interest. Once mutants in feruloylation are identified, cloning the genes responsible will provide tools to characterize their function. The identification of these genes in Brachypodium could work as a handle for gene discovery in other important crops because of conservation of genome organization and gene order in grasses (Devos and Gale, 2000; Freeling, 2001). Orthologous genes can be further manipulated in other important crops, such as the biofuel crop model switchgrass, to enhance cell wall degradation for a more efficient biomass conversion to biofuels. This is a strong focus of research at Penn State University at Buanafina's lab.
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TOPAbstractINTRODUCTIONFERULIC ACID: ITS ASSOCIATION...THE BIOCHEMISTRY OF...DISCUSSIONFUNDING |
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This work was supported by the National Research Initiative (2008-02863) from the USDA Cooperative State Research, Education and Extension Service; USDA-DOE Plant Feedstock Genomics Research Program (ER64701).
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Acknowledgements |
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The author would like to thank BBSRC and Genecor Inc. for previous funding of some of my own work while at the Institute of Grassland and Environmental Research (now IBERS), Aberystwyth, and Prof. Phil Morris for providing some of the figures and for useful discussions on the manuscript. No conflict of interest declared.
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