Mannans in Primary and Secondary Plant Cell Walls†

New Zealand Journal of Forestry Science

39 (2009) 153-160

http://nzjfs.scionresearch.com

Mannans in primary and secondary plant cell walls†

Laurence D. Melton1,*, Bronwen G. Smith1, Roshita Ibrahim1 and Roswitha Schröder2

1Food Science, Department of Chemistry, University of Auckland, Auckland, New Zealand 2New Zealand Institute for Plant and Food Research, Mt Albert Research Centre, Auckland, New Zealand

(Submitted for publication 10 September 2008; accepted in revised form 18 May 2009)

*Corresponding author: [email protected]

Abstract A brief overview of the structure of mannans in plant cell walls and other organisms is presented. In particular, mannans, galactomannans and glucomannans in seed endosperm and vegetative tissues such as bulbs and tubers, galactoglucomannans (GGMs) in primary cell walls, and glucomannans and GGMs in secondary walls of hardwoods and softwoods are covered. Possible roles of mannans in primary plant cell walls other than as storage polysaccharides are discussed.

Keywords: galactomannans; galactoglucomannans; mannans; plant cell walls; polysaccharides

† Based on a paper presented at the 3 rd Joint New Zealand-German Symposium on Plant Cell Walls, 13-15 February 2008, Auckland, New Zealand.

Introduction the walls of the Chinese caterpillar fungus (Cordyceps Mannans are widely distributed among living militaris) consist of a (1→4)-α- D-mannose backbone organisms. They are found as pure mannans branched at O-3 with side chains of (1→4)-α- D-glucose (homomannans), galactomannans, glucomannans and (1→6)-β-D-galactose residues with β-D-galactose and galactoglucomannans. Also, cell walls from at the terminal position (Yu et al., 2009). From the non-plant sources such as fungi or bacteria contain edible mushrooms, Auriculana auricula-judae, (Sone mannose-based polysaccharides. However, here the et al., 1978) and Tremella fuciformis (Kakuta et al., mannose residues are alpha-linked, whereas in the 1979) heteromannans have been isolated in which the plant cell wall, mannose residues in polysaccharides backbone is (1→3)-α-D-mannan. Lichen (Thamnolia are beta-linked. In yeast cell walls, including bakers’ vermicularis var. subuliformis) had a galactofuranosyl yeast (Saccharomyces cerevisiae) (Korn & Northcote, oligosaccharide linked to an (1→6)-linked α-manno- 1960), Kluyveromyces lactis (Raschke & Ballou, 1972) oligosaccharide (Omarsdottir et al., 2006). As the and Candida utilis (Ruszova et al., 2008), mixed structures of the mannans from such organisms linkage mannans containing (1→6) and (1→2)-linked are generally unrelated to those of higher α-mannosyl residues have been reported. plant cell wall mannans, they will not be Galactomannan has been isolated from cell walls of discussed further. It is noteworthy that the the fungus Lineolate rhizophorae (Giménez-Albian galactoglucomannan found in moss (Fontinalis et al., 2007) and from the bacteria Rahnella aquatilis (Zdorovenko et al., 2006) with both containing (1→6) antipyretica) has a backbone of (1→4)-linked and (1→3)-linked α-mannosyl residues. Mannans from β-mannose and glucose residues (Geddes & Wilkie,

1972). The remainder of this review will focus on. galactose side chains arranged to give hairy and mannans in primary and secondary plant cell walls. smooth regions (Dea & Morrison, 1975). The mannose to galactose ratio is 3.5 : 1 in locust bean gum (Daas et Storage Mannans, Galactomannans and al., 2000), while the mannose to galactose ratio in guar Glucomannans gum is 1.5 : 1, with the galactose side chain randomly attached throughout the polymer. Tara ( Caesalpinia Mannans, glucomannans and galactomannans occur spinosa) gum has a mannose to galactose ratio of 3 : 1 as storage polysaccharides in the endosperm cell (BeMiller, 2007) (Figure 1b). Konjac gum from corms of walls of seeds (mostly mannans and galactomannans) Amorphophallus konjac is a well known glucomannan, or in vegetative tissues such as bulbs or tubers and is utilised in the food industry (BeMiller, 2007) (mostly glucomannans) (Matheson, 1990). Their (Figure 1c). It has a mannose to glucose ratio of 1.5- principal chemical structures are shown in Figure 1. 2.0 : 1 with the β-D-mannopyranosyl units linked (1 →4) in a straight chain. The glucose sugars appear to be

Mannan (a homopolymer of (1→4)-linked β-D-mannosyl randomly distributed along the chain (BeMiller, 2007). residues) (Figure 1a) has been found as the major For further information on storage mannans, consult component in endosperm cell walls of palm seeds Matheson (1990), Buckeridge et al. (2000), and such as ivory nut (Phytelephas macrocarpa), where it Srivastava and Kapoor (2005). can make up as much as 60% of the seed (Stephen, 1982; Matheson, 1990). Ivory nut mannan is highly Mannans in Primary Cell Walls water-insoluble, whereas the other storage mannans, galactomannan and glucomannan, are water-soluble. Apart from being storage polysaccharides, mannans are also structural polysaccharides in the primary plant Galactomannans found in seed endosperm such as cell wall. Although they are ubiquitous, they are usually locust bean (carob) (Ceratonia siliqua) gum and guar only present in small amounts. Generally, mannose is (Cyamopsis tetragonolobus) gum are well-known 2 mol % or less of the dry cell wall, and in some cases for their use in food products. They are found in the it was not detected (Thimm et al., 2002). For example, endosperm walls and vacuoles of the seeds (Brennan ripe kiwifruit (Actinidia chinensis) cell walls contain 1.2 et al., 1996). They consist of a (1→4)-linked β-mannan to 1.9 mol% depending on the tissue zone (Redgwell backbone with variable amounts of α-galactose et al., 1990) and cabbage (Brassica oleracea) cell residues linked (1→6) to mannose residues with the walls 2 mol% (Smith et al., 1998). A notable exception

(a) Ivory nut mannan

→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→

(b) Tara gum (galactomannan)

→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→

(1→6)- -(1→6)- - p p -Gal -Gal D -D - α α

→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→

FIGURE 1: Structures of: (a) ivory nut mannan, an example for a structure of a pure mannan; (b) tara gum, an example for a structure of a galactomannan; and (c) konjac gum, an example for a structure of a glucomannan.

is cell wall material isolated from ripe tomato which had isolated and characterised (Figure 2a) (Schröder et al., 11.7 mol % mannose (Seymour et al., 1990). The walls 2001). It has a mannose : glucose : galactose ratio of of the vegetative tissue of the palms Rhopalostylis 3 : 3 : 2. More recently, a GGM isolated from tomato sapida and Phoenix canariensis (Carnachan & Harris, (Lycopersicon esculentum ) peel and outer pericarp 2000) have been reported to contain small amounts has been shown to have a signifi cant amount of xylose, (2 mol % or less) of mannose. Fern walls have also with a mannose to glucose to galactose to xylose ratio been reported to contain mannans (Bremner & Wilkie, of 3 : 3 : 1 : 1 (Schröder et al., 2007). 1971). Popper and Fry (2003) found cell walls of some liverworts and mosses to be rich in mannose while the green algae Chara corallina and Ulva lactuca Mannans in Secondary Cell Walls contained much lower amounts. Interestingly, the β-D-mannan in green seaweed (Codium fragile) is It has been frequently noted that thickened cell walls found as crystalline microfi brils similar to cellulose contain higher levels of mannose. Arabidopsis thaliana microfi brils, therefore replacing cellulose as the stems which contain secondary cell walls were found principal skeletal component (Mackie & Preston, 1968). by one group (Brown et al., 2005) to contain ~ 8% of the noncellulosic neutral sugars in the cell wall material as Little work has been done on elucidating the structures mannose, while another group found ~7 mol% of the cell of mannans in primary cell walls. This is likely to be wall material (CWM) excluding cellulose was mannose due to a number of factors, the most obvious being (Harholt et al., 2006). However, a third group (Zhong the small amount of mannose present in primary cell et al., 2005) reported 4.8% mannose. Sclerenchyma walls (Thimm et al., 2002) and the diffi culty isolating cell walls in A. thaliana contain 5% mannose along them. A GGM from kiwifruit primary cell walls has been with 31% cellulose and 48% xylose (Ha et al., 2002).

β -D (a) GGM from kiwifruit -Gal p -(1→4)-

α - D α -Gal - D-Gal p -(1→6)- p -(1→6)-

→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→4)-β-D-Manp- (1→

(b) Typical gymnosperm GGM, acetylated and water-soluble α -D -Gal

p -(1→6)-

→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→4)-β-D-Manp- (1→

-(1→6)- -Acetyl- p O -Gal -D α

→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Manp- (1→4)-β-D-Glcp- (1→4)-β-D-Manp- (1→

-(1→6)- p -Gal -D α

FIGURE 2: Structures of galactoglucomannan from: (a) kiwifruit primary cell walls (Schröder et al., 2001); (b) a typical GGM isolated from gymnosperm softwood, water-soluble through acetylation (Timell, 1967); and (c) a typical water-insoluble GGM isolated from gymnosperm softwood (Timell, 1967).

Mannans in Wood wall of the poplar species, with a mannose to glucose ratio of 2 : 1 (Mellerowicz et al., 2001). An alkaline- Galactoglucomannans are the major hemicellulose in soluble GGM has also been isolated from poplar softwoods (gymnosperms) followed by glucuronoxylan, (Populus monilifera), consisting of 1→4 linked β- D- whereas in hardwoods (angiosperms) glucomannans mannopyranosyl and β- D-glucopyranosyl units in are a minor component and the major hemicellulose the backbone distributed at random, and (1 →6)-β-D- is glucuronoxylan (Timell, 1967). Softwoods have a galactopyranosyl units attached to mannose and range of compositions, but generally the mannose glucose with a mannose to glucose to galactose ratio to glucose to galactose ratio is 3.5 – 4.5 : 1 : 0.5-1.1 of 9.7 : 4.1 : 1 with a trace of xylose (Kubačková et (Willför et al., 2005a; 2008), although older literature al., 1992). Cottonwood (Populus spp.) had 2% (by dry favours a mannose to glucose to galactose ratio of weight) of mannan (Puls & Schuseil, 1993), equivalent 3 : 1 : 1 (Timell, 1967) (Figures 2b & c). In pine and to up to 5% GGM. Differences in the mannose to spruce wood, GGM is not uniformly distributed in the glucose ratio occur within a species depending on cell walls, but is greatest near the lumen and least in whether heartwood or sapwood was analysed, as the outer layer (Sjöström, 1993). The water-soluble shown in a survey of hardwoods (Willför et al., 2005b). O-acetyl-GGM from Norway spruce (Picea abies) has mannose to glucose to galactose ratio of 4 : 1 : 0.5, Interaction of Mannans with other Wall degree of acetylation of 0.3, with acetyl groups only Polysaccharides at C-2 and C-3 of mannose (Willför et al., 2008). New Zealand-grown radiata pine (Pinus radiata) gave a Mannans have long been known to be intimately similar ratio of 4.5 : 1 : 1.3 (Brasch, 1983) and 3.6 : 1 : associated with cellulose microfi brils and extensive 0.8 (McDonald et al., 1999) with O-acetyl groups only treatment with strong alkali or other chaotropic agents is at the C-3 of mannose. The GGM from radiata pine ineffective in removing them entirely from the cellulose contains regions of two or three contiguous glucose microfi brils. They are commonly found in the cellulose units as well as regions of manno-oligosaccharides residue after sequential extraction of walls. There is (Tenkanen et al., 1997). The molecular weight of other evidence that mannans interact with cellulose. 30 to 60 kDa indicates that they are relatively small Ivory nut mannan was reported to be “crystallised” on compared to other cell wall polysaccharides. The cellulose microfi brils (Chanzy et al., 1978). Moreover, alkali-soluble GGM from the secondary cell walls of it has been shown the lower the number of galactose Norway spruce has been reported to have few side sidechains on a guar galactomannan, and the lower the branches with a mannose to glucose to galactose of acetyl groups, the higher was their affi nity for bleached 33 : 8 : 1 (Capek et al., 2000) with branch points at O-6, kraft paper (Hannuksela et al., 2002). Likewise, the O-3 and O-2 of mannose and O-6 and O-3 of glucose. lower the acetyl content, the more a glucomannan was adsorbed onto commercial cellulose (Laffend & The ancient Chinese “fossil” conifer (Metasequoia Swenson, 1968). Neither the galactomannan locust glyptostroboides) contains distinctly less mannose bean gum nor xanthan gum (from the microorganism than other gymnosperms and it is present in two Xanthomonas campestris) will form a gel, but together different GGM forms (Wenda et al., 1990). One GGM they gel. Locust bean gum has been shown to adhere has a mannose to glucose to galactose ratio of 1.5 : to microcrystalline cellulose (Mishima et al., 1998) and 1 : 1 that makes up 6.3% of the wood. The other has solid-state 13 C NMR spectroscopy has confi rmed that a mannose to glucose to galactose ratio of 5.3 : 3 : 1 70% of the mannosyl residues (but not the galactosyl that makes up 4.8% of the wood. Antibody labelling residues) are bound to cellulose from softwood kraft of glucomannans was observed only in the secondary pulp (Newman & Hemmingson, 1998). Schröder et walls of the differentiating tracheids of cypress al. (2004; 2006) reported that galactoglucomannan (Chamaecyparis obtusa) wood (Maeda et al., 2000). isolated from kiwifruit adhered to cellulose of fi lter paper, whereas storage glucomannans and Water-soluble glucomannan from hardwoods had galactomannans from seeds did not. Whitney et a mannose to glucose ratio of 2 : 1, with very small al. (1998) has also shown that the unsubstituted amounts of galactose, xylose and arabinose present mannan portions of konjac glucomannan and for aspen (Populus spp.) and a mannose to glucose the galactomannans (locust bean gum, guar and ratio of 2.1 – 2.4 : 1 for birch ( Betula spp.) (Teleman fenugreek (Trigonella foenum-graecum ) with low et al., 2003). Both glucomannans are acetylated at levels of galactose side chains interact with bacterial O-2 and O-3 of mannose, with a degree of acetylation cellulose, as does glucomannan (mannose to glucose of 0.3. In the case of aspen, if it is a GGM and not ratio 1.8 : 1) from beech ( Fagus crenata) wood and a glucomannan, then the mannose to glucose to other hemicelluloses, including xyloglucan. However, galactose ratio would be ~ 20 : 10 : 1 and in the case of of all the hemicelluloses trialled, beech glucomannans birch, there would be even less galactose. Hornbeam showed the strongest affi nity for bacterial cellulose, (Carpinus betulus) wood has a glucomannan with a followed by xyloglucan and xylans, and with mannose to glucose ratio of 1.5 : 1 (Ebrigerová et al., arabinogalactan having the least (Iwata et al., 1998). 1972). Glucomannan makes up 5% of the secondary

Glucomannan-lignin-xylan complexes are thought Acknowledgements to exist in spruce wood (Lawoko et al., 2005). Alternatively, mannan might associate with another We wish to thank the Royal Society of New Zealand, hemicellulose such as xylan (Kerr & Fry, 2004; Rizk the German Research Foundation and Uniservices et al., 2000) and in lignifi ed cell walls including wood, of the University of Auckland for fi nancial support xylan interacts with lignin (Barakat et al., 2007). for the 2008 New Zealand-German Plant Cell Wall Conference, February 2008, in Auckland. We thank This, along with other evidence, has lead to the the New Zealand-German ISAT linkage coordinator Dr. hypothesis that like xyloglucan and xylans, the Frank Bruhn from the Ministry of Research, Science and glucomannans and the GGMs can act as cross-linking Technology, Wellington, for his enthusiastic support. tethers between cellulose microfi brils and so contribute to the three-dimensional structure of the plant cell wall. This idea received a considerable boost from recent References work in which an endo-β-mannanase from tomato fruit (Schröder et al., 2004; 2006) was shown to act not Barakat, A., Winter, H., Rondeau-Mouro, C., Saake, only as a hydrolase but also as a transglycosylase. B., Chabbert, B., & Cathala, B. (2007). Studies Here, mannans such as GGM from kiwifruit as well as of xylan interactions and cross-linking to glucomannans or galactomannans were cleaved and synthetic lignins formed by bulk and end-use attached to tritiated mannan-derived oligosaccharides polymerisation. Planta, 226, 267-281. in a transglycosylase reaction analogous to the BeMiller, J. N. (2007). Carbohydrate Chemistry for action of the transglycosylase reaction xyloglucan Food Scientists (2nd ed.), (pp. 258-261). St transglucosylase/ hydrolase (XTH) (Nishitani & Paul MN, USA: AACC International. Tominaga, 1992; Fry et al., 1992; Farkas et al., 1992). The role of XTH is to continuously modify the Bootten, T. J., Harris, P. J., Melton, L. D., & Newman, xyloglucan-cellulose network during different stages of R. H. (2004). Solid-state 13 C-NMR spectroscopy plant development by breaking and rejoining existing shows that the xyloglucans in the primary cell or newly synthesised xyloglucan molecules to existing walls of mung bean (Vigna radiata L.) occur in xyloglucan (Thompson & Fry, 2001), thereby probably different domains: a new model for xyloglucan- restoring and refi ning the xyloglucan-cellulose network cellulose interactions in the cell wall. Journal of during developmental processes. In this manner, endo- Experimental Botany, 55, 571-583. β-mannanase could cleave and lengthen glucomannan Brasch, D. J. (1983). The chemistry of Pinus radiata or GGM cross-links to allow cell expansion, or simply VI. The water-soluble galactoglucomannan. cleave the cross-links to contribute to softening of Australian Journal of Chemistry, 36, 947-954. texture that occurs on ripening. Beyond the enzyme work, the evidence to support this hypothesis is sparse. Bremner, I., & Wilkie, K. C. B. (1971). The hemicelluloses of bracken: Part II. A galactoglucomannan. In wood, GGMs could strengthen cell walls by Carbohydrate Research, 20, 193-203. acting as cross-links from cellulose microfi brils to a Brennan, C. S., Blake, D. E., Ellis, P. R., & Schofi eld, hemicellulose-lignin complex. J. D. (1996). Effects of guar galactomannan on wheat bread microstructure and on the in The relatively small amount of glucomannan or GGM vitro and in vivo digestibility of starch in bread. in primary cell walls does not negate their importance Journal of Cereal Science, 24, 151-160. as cross-linking molecules. We have calculated with mung bean (Vigna radiata ) hypocotyl cell walls that Brown, D. M., Zeef, L. A. H, Ellis, J., Goodacre, R., only 8% of the surface of the cellulose microfi brils is & Turner, S. R. (2005). Identifi cation of novel coated with adhering xyloglucan (Bootten et al., 2004). genes in Arabidopsis involved in secondary cell Nonetheless, the walls are perfectly functional and wall formation using expression profi ling and indeed a large number of cross-links are unnecessary. reverse genetics. Plant Cell, 17, 2281-2295. The fewer cross-links, the easier it would be to modify Buckeridge, M. S., dos Santos, H. P., & the walls during cell expansion and fruit ripening. Tiné, M. A. S. (2000). Mobilisation of storage cell wall polysaccharides in seeds. Plant Physiology and Biochemistry, 38, 141-156. Conclusion Capek, P., Kubačková, M., Alföldi, J., Bilisics, Mannans have been studied extensively in wood and L., Lišková, D., & Kákoniová, D. (2000). considerably less in other species but their various Galactoglucomannan from the secondary cell roles have not been fully elucidated. wall of Picea abies L. Karst. Carbohydrate Research, 329, 635-645.

Carnachan, S. M., & Harris, P. J. (2000). Polysaccharide Iwata, T., Indrarti, L., & Azuma, J-I. (1998). Affi nity compositions of primary cell walls of palms of hemicellulose for cellulose produced by Phoenix canariensis and Rhopalostylis sapida. Acetobacter xylinum. Cellulose, 5, 215-228. Plant Physiology and Biochemistry, 38, 699- Kakuta, M., Sone, Y., Umeda, T., & Misaki, A. 708. (1979). Comparative structural studies on Chanzy, H., Dube, M., & Marchessault, R. H. acidic heteropolysaccharides isolated from (1978). Shish-kebab morphology. Oriented “Shirokikurage”, fruit body of Tremella fuciformis recrystallization of mannan on cellulose. Tappi, Berk, and the growing culture of its yeast-like 61, 81-82. cells. Agricultural and Biological Chemistry, Tokyo, 43, 1659-1668. Daas, P. J. H., Schols, H. A., & de Jongh, H. H. J. (2000). On the galactosyl distribution of Kerr, E. M., & Fry, S. C. (2004). Extracellular cross- commercial galactomannans. Carbohydrate linking of xylan and xyloglucan in maize cell- Research, 329, 609-619. suspension cultures, the role of oxidative phenolic coupling. Planta, 219, 73-83. Dea, I. C. M., & Morrison, A. (1975). Chemistry and interaction of seed galactomannans. Advances Kubačková, M., Karácsonyi, S., & Bilisics, L. (1992). in Carbohydrate Chemistry and Biochemistry, Structure of galactogluconmannan from 31, 241-312. Populus monilifera H. Carbohydrate Polymers, 19, 125-129. Ebringerová, A., Kramar, A., & Domanský, R. (1972). Glukomannan aus dem Holz der Hagebuche Korn, E. D., & Northcote, D. H. (1960). Physical and (Carpinus betulus L.) Holzforschung, 26, 89-92. chemical properties of polysaccharides and glycoproteins of the yeast-cell wall. Biochemical Farkas, V., Sulova, Z., Stratilova, E., Hanna, R. Journal, 75, 12-17. and Maclachlan, G. (1992). Cleavage of xyloglucan by nasturtium seed xyloglucanase Laffend, K. B., & Swenson, H.A., (1968). Effect of acetyl and transglycosylation to xyloglucan subunit content of glucomannan on its sorption onto oligosaccharides. Archives of Biochemistry and cellulose and on its beater additive properties. Biophysics, 298,365-370. I. Effect on sorption. Tappi, 51, 118-123. Fry, S.C., Smith, R.C., Renwick, K.F., Martin, D.J., Lawoko, M., Henriksson, G., & Gellerstedt, G. Hodge, S.K., & Matthews, K. J. (1992). 2005). Structural differences between lignin- Xyloglucan endotransglycosylase, a new cell carbohydrate complexes present in wood and wall-loosening enzyme activity from plants. in chemical pulps. Biomacromolecules, 6, Biochemical Journal, 282, 821-828. 3467-3473. Geddes, D. S., & Wilkie, K. C. B. (1972). A Mackie, W., & Preston, R. D. (1968). The occurrence of galactomannan from the stem tissues of mannan microfi brils in the green algae Codium the aquatic moss Fontinalis antipyretica. fragile and Acetabularia crenulata. Planta, 70, Carbohydrate Research, 23, 349-357. 240-253. Giménez-Albian, M. I., Bernabé, M., Leal, J. A., Maeda, Y., Awano, T., Takabe, K., & Fujita, M. Jiménez-Barbero J., & Prieto, A. (2007). (2000). Immunolocalisation of glucomannans Structure of a galactomannan isolated from in the cell wall of differentiating tracheids in the cell wall of fungus Lineolata rhizophorae. Chamaecyparis obtusa. Protoplasma, 213, Carbohydrate Research, 342, 2599-2603. 148-156. Ha, M-A., MacKinnon, I. M., Šturcová, A., Apperley, Matheson, M. K. (1990). Mannose-based D. C., McCann, M. C., Turner, S. R., & Jarvis, polysaccharides. Methods in Plant Biochemistry, M. C. (2002). Structure of cellulose-defi cient 12, 371-413. secondary cell walls from the irx3 mutant of McDonald, A. G., Clare, A. B., & Meder, A. R. (1999). Arabidopsis thaliana. Phytochemistry, 61, 7-14. Chemical characterisation of the neutral water Hannuksela, T., Tenkanen M., & Holmborn, B. (2002). soluble components from radiata pine high Sorption of dissolved galactoglucomannans temperature TMP fi bre. Proceedings of 53 rd and galactomannans to bleached kraft pulp. Appita Annual Conference (Vol. 2) Melbourne: Cellulose, 9, 251-261. Appita. Harholt, J. Jensen, J. K., Sørensen, L. O., Orfi la, C., Mellerowicz E. J., Baucher, M., Sundberg, B., & Boerjan, Pauly, M., & Scheller, H. V. (2006). ARABINAN W. (2001). Unravelling cell wall formation in the DEFICIENT 1 is a putative arabinosyltransferase woody dicot stem. Plant Molecular Biology, 47, involved in biosynthesis of pectic arabinan in 239-274. Arabidopsis. Plant Physiology, 140, 49-58.

Mishima, T., Hisamatsu, M., York, W. S., Teranishi, K., Schröder, R., Sharma, N. N., Redgwell, R. & Yamada, T. (1998). Adhesion of β- D-glucans J., & Atkinson, R. G. (2007). Mannan to cellulose. Carbohydrate Polymers, 308, 389- transglycosylase/hydrolase from ripe tomato: 395. A cell wall enzyme in search of a function. Mitteilungen der Bundesforschungsanstalt für Newman, R. H., & Hemmingson, J. A. (1998). Forst- und Holzwirtschaft, 223, 43-52. Interactions between locust bean gum and cellulose characterized by 13 C NMR Schröder, R., Wegrzyn, T. F., Bolitho, K. M., & Redgwell, spectroscopy. Carbohydrate Polymers, 36, R. J. (2004). Mannan transglucosylase: a novel 167-172. enzyme activity in cell walls of higher plants. Planta, 219, 590-600. Nishitani, K., & Tominaga, R. (1992). Endo-xyloglucan transferase, a novel class of glycosyltransferase Schröder. R., Wegrzyn, T. F., Sharma, N. N., & that catalyzes transfer of a segment of Atkinson, R. G. (2006). LeMAN4 endo-β- xyloglucan molecule to another xyloglucan mannanase from ripe tomato fruit can act as a molecule. Journal of Biological Chemistry, 267, mannan transglycosylase or hydrolase. Planta, 21058-21064. 224, 1091-1102. Omarsdottir, S., Petersen, B. O., Paulsen, B. S., Seymour, G. B., Colquhoun, I. J., DuPont, M. S., Togola, A., Duus, J. Ø., & Olafsdottir, E. S. Parsley, K. R., & Selvendran, R. R. (1990). (2006). Structural characterisation of novel Composition and structural features of cell lichen heteroglycans by NMR spectroscopy and wall polysaccharides from tomato fruits. methylation analysis. Carbohydrate Research, Phytochemistry, 29, 725-731. 341, 2449-2455. Sjöström, E. (1993). Wood Chemistry: Fundamentals Popper, Z. A., & Fry, S. C. (2003). Primary cell wall and Applications (2nd ed. p 70). San Diego CA, composition of bryophytes and charophytes. USA: Academic Press. Annals of Botany, 91, 1-12. Smith, B. G., Harris, P. J., Melton, L. D., & Newman, Puls, J., & Schuseil, J. (1993). Chemistry of R. H. (1998). The range of mobility of the hemicelluloses: relationship between non-cellulosic polysaccharides is similar in hemicellulose structure and enzymes required primary cell walls with different polysaccharide for hydrolysis. In M. P. Coughlan and G. P. compositions. Physiologia Plantarum, 103, Hazlewood (Eds.), (pp 1-27). Hemicelluloses 233-246. and Hemicellulases. London, UK: Portland Sone, Y., Kakuta, M., & Misaki,A. (1978). Isolation Press. and characterization of polysaccharides of Raschke, W. C., & Ballou, C. E. (1972). “Kikurage”, fruiting body of Auricularia auricular- Characterization of a yeast mannan containing judae. Agricultural and Biological Chemistry N-acetyl-D-glucosamine as an immunochemical Tokyo, 42, 417-425. determinant. Biochemistry, 11, 3807-3816. Srivastava, M., & Kapoor, V. P. (2005). Seed Redgwell, R. J., Melton, L. D., & Brasch, D. J. (1990). galactomannans: An overview. Chemistry and Cell wall changes in kiwifruit following post Biodiversity, 2, 295-317. harvest ethylene treatment. Phytochemistry, 29, Stephen, A. M. (1982). Other plant polysaccharides. 399-407. In G. O. Aspinall (Ed.), The Polysaccharides, Rizk, S. E., Abdel-Massih, R. M., Baydoun, E. Vol .2 (pp 97-193). New York, USA: Academic A.-H., & Brett, C. T. (2000). Protein and Press. pH-dependent binding of nascent pectin and Teleman, A., Nordström, M., Tenkanen, M., Jacobs, glucuronoarabinoxylan to xyloglucan in pea. A., & Dahlman, O. (2003). Isolation and Planta, 211, 423-429. characterization of O-acetylated glucomannans Ruszova, E., Pavek, S., Hajkova, V., Jandova, from aspen and birch wood. Carbohydrate S., Velebny, V., Papezikova, I., & Kubala, Research, 338, 525-534. L. (2008). Photoprotective effects of Tenkanen, M., Makkonen, M., Perttula, M. Viikari, L., glucomannan isolated from Candida utilis. & Teleman, A. (1997). Action of Trichoderma Carbohydrate Research 343, 501-511. reesei mannanase on galactoglucomannan in Schröder, R., Nicolas, P., Vincent, S. J. F., Fischer, pine kraft pulp. Journal of Biotechnology, 57, M., Reymond, S., & Redgwell, R. J. (2001). 191-204. Puriﬁ cation and characterisation of a galactoglucomannan from kiwifruit (Actinidia deliciosa). Carbohydrate Research, 331, 291- 306.

Thimm, J. C., Burritt, D. J., Sims, I. M., Newman, R. H., & Melton, L.D. (2002). Celery (Apium graveolens L.) parenchyma cell walls: cell walls with minimal xyloglucan. Physiologia Plantarum, 224, 1091-1102. Thompson, J. E., & Fry, S. C. (2001). Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells. Plant Journal, 26, 23-24. Timell, T. E. (1967). Recent progress in the chemistry of wood hemicelluloses. Wood Science and Technology, 1, 45-70. Wenda, L., Wang, P., & Liao, P. (1990). Isolation and analysis of the hemicelluloses of the fossil tree (Metasequoia glyptostroboides). Journal of Wood Chemistry and Technology, 10, 123-132. Whitney, S. E. C., Brigham, J. E., Darke, A. H., Reid, J. S. G., & Gidley, M.J. (1998). Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose. Carbohydrate Research, 307, 299-309. Willför, S., Sundberg, K., Hemming, J., & Holmbom, B. (2005a). Polysaccharides in some industrially important softwood species. Wood Science and Technology, 39, 245-258. Willför, S., Sundberg, K., Pranovich, A., & Holmbom, B. (2005b). Polysaccahrides in some industrially important hardwood species. Wood Science and Technology, 39, 601-617. Willför, S., Sundberg, K., Tenkanen, M., & Holmbom, B. (2008). Spruce-derived mannans – a potential raw material for hydrocolloids and novel advanced natural materials. Carbohydrate Polymers, 72, 197-210. Yu, R., Yin, Y., Yang, W., Ma, W., Yang, L., Chen, X., Zhang, Z., Ye, B., & Song, L. (2009). Structural elucidation and biological activity of a novel polysaccharide by alkaline extraction from cultured Cordyceps militaris. Carbohydrate Polymers, 75, 166-171. Zdorovenko, E. L., Varbanets, L. D., Zatonsky, G. V., & Ostapchuk, A. N. (2006). Structures of two putative O-speciﬁ c polysaccharides from the Rahnella aquatilis 3-95 lipopolysaccharide. Carbohydrate Research, 341, 164-168. Zhong, R., Peña, M. J., Zhou, G.-K., Nairn, C. J ., Wood- Jones, A., Richardson, E. A., Morrison, W. H., Darvill, A. G., York, W. S., & Ye, Z.-H. (2005). Arabidopsis fragile ﬁ ber8 , which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell, 17, 3390-3408.