Mobilisation of storage cell wall polysaccharides in seeds

Mobilisation of storage cell wall polysaccharides in seeds

Marcos S. Buckeridge*, Henrique Pessoa dos Santos, Marco Aurélio S. Tiné

Instituto de Botânica de São Paulo, Seção de Fisiologia e Bioquímica de Plantas, CP 4005, CEP 01061-030 São Paulo SP, Brazil

(Received June 7, 1999; accepted August 9, 1999)

Abstract — Plants store carbohydrate polymers in a number of forms. Starch is the principal form, followed by fructans and cellwall storage polysaccharides (CWSP). The latter are present mainly in seeds and consist of magnifications of one of thepolysaccharides present in one of the cell wall matrices. CWSPs are classified as mannans, xyloglucans and galactans, the firstbeing subdivided into pure mannans, galactomannans and glucomannans. The present review updates the principal discoveriesconcerning occurrence, structure, metabolism and eco-physiological significance of the seed storage cell wall polysaccharideswith emphasis on their importance for plant metabolism and adaptation to their respective environments during evolution. Theproperties of CWSPs as storage polysaccharides are compared with starch and fructans and the current knowledge on thecatabolism (including control) of mannan/galactomannan, xyloglucan, and galactan is reviewed. On the basis of these data, theidea that the CWSPs are multifunctional molecules is proposed and this feature is used as evidence for the hypothesis that, duringevolution, the CWSPs were involved in cycles of transference of functions which led them to become storage polysaccharides,yet preserving some of their previous primary cell wall functions. © 2000 Éditions scientifiques et médicales Elsevier SAS

Arabinogalactan / galactomannan / mannan / polysaccharides / seed / storage / xyloglucan

1. INTRODUCTION

Plants display different strategies that include accu-mulation of large amounts of some compounds, whichfavours their adaptation to different environments.These substances are mobilised during developmentand their products are used for several purposes suchas energy generation and production of raw materials(protein, nucleic acids, carbohydrates and lipids) forbuilding cells and tissues [52].

Among the principal substances stored by plants,many carbohydrate polymers have been selected dur-ing evolution. Starch is the most widespread, followedby fructans and cell wall polysaccharides (galactoman-nans, xyloglucans and galactans). As storage com-pounds, starch and fructans have the advantages ofbeing composed of glucose and mainly fructose,respectively. These carbohydrates are promptly incor-porated into the energy-generation metabolism, culmi-nating in rapid production of ATP and also yieldingcarbon for biosynthesis of most biomolecules in theplant cells. Starch is a polysaccharide particularlyadapted to storage function, being mobilised either byhydrolysis or by a mechanism that involves direct

phosphorylation of the terminal glucosyl residues.Such a mechanism appears to be exclusive to starchand no consistent work has demonstrated beyond anydoubt that fructans or storage cell wall polysaccharidescan be mobilised by phosphorylation. Somme pro-posed that phosphorylation mechanisms occur forgalactomannan mobilisation [73], but this line of workwas not confirmed [59]. Indeed, a phosphorylation-based mobilisation of cell wall carbohydrates wouldrequire the secretion of phosphate or phosphorylatedcompounds, as well as the absorption of the phospho-rylated carbohydrate. This traffic of charged com-pounds through the membrane would be energeticallyexpensive.

Each one of these storage compounds (cell wallpolysaccharides, fructans and starch) presents charac-teristics that make them more convenient for the cell incertain situations. First, none of them have free reduc-ing radicals. This is an advantage when compared withthe accumulation of free monosaccharides, since itcould lead to unspecific glycosylation of cellularelements. The second is their osmotic activity. Beinginsoluble, starch is less active (osmotically) thanfructans and its higher packing also makes it less

* Author to whom correspondence should be addressed (fax +55 21 11 5773678; e-mail [email protected])

Plant Physiol. Biochem.,2000,38 (1/2), 141−156 / © 2000 Éditions scientifiques et médicales Elsevier SAS. All rights reservedS0981942800001625/REV

Plant Physiol. Biochem., 0981-9428/00/1-2/© 2000 E´ ditions scientifiques et médicales Elsevier SAS. All rights reserved

reactive. On the other hand, the unpacked state of thefructans found in nature makes them useful in thecontrol of the osmotic potential of the cell [5].

Cell wall polysaccharides are chemically inert anddisplay different degrees of solubility in water. Thisfeature prompts advantages that are similar to starch(packing and low reactivity) and makes possible theexistence of a cell ‘compartment’ (the cell wall) whichpermits water to flow with considerable degree offreedom, as happens with fructans stored in vacuoles.However, costs of production are higher, since cellwall polymers need a complex machinery of biosyn-thesis, secretion and assembly during deposition. Thisis especially true when compared to fructans, whichare quickly synthesised, by transference of fructosemoieties from sucrose, without the involvement ofnucleotide sugars.

Table I summarises the principal features of thethree main groups of storage polysaccharides fromplants. The features discussed above highlight thedifferent functions played by these polysaccharides,regarding how they are synthesised, how they aredegraded and where they are in the cell and in theplant. Whereas starch appears to have a storage func-tion exclusively, fructans and cell wall polysaccharidesseem to hold other functions. Fructans participate inthe osmotic control of plant cells and tissues and thecell wall polysaccharides are linked to hardness (man-nans in endosperms of seeds of palms, tomato andlettuce), water relationships (xyloglucan in cotyledonsand galactomannan in endospermic legume seeds) andcell expansion (lupin galactans). In fact, the multifunc-tional character of at least one seed storage cell wallpolysaccharide (galactomannan) has been demon-strated [61] and a possible mechanism for the evolu-tion of this second function has been proposed [10].

Wall mobilisation is an important phenomenon inother systems such as fruit ripening and cell expansion(see [68] for a review). The present review updates theprincipal discoveries concerning occurrence, structure,metabolism and eco-physiological significance of the

seed storage cell wall polysaccharides with emphasison their importance for plant metabolism and adapta-tion to their respective environments during evolution.

2. CELL WALL STORAGEPOLYSACCHARIDES (CWSP)

The cell wall storage polysaccharides (CWSP) havebeen usually classified into three groups: mannans,xyloglucans and galactans [10, 60, 62]. This classifi-cation is based essentially on structure, the mannansbeing also divided into pure mannans, glucomannansand galactomannans (table II).

Considering the recent model proposed for the plantcell wall [15, 53] in which three matrices (cellulose-hemicellulose, pectin and protein) are thought to exist,the storage cell wall polysaccharides might be consid-ered as magnifications of these carbohydrate matri-ces [10] (figure 1). Mannans and xyloglucans are poly-mers which, when present as CWSPs, form a matrixthat apparently lack cellulose and pectin in the sameproportions as in primary cell walls. Galactans, on theother hand, are neutral branching points of rhamnoga-lacturonan, therefore belonging to the matrix of pec-tins. When occurring as a CWSP, galactans are largelyamplified in relation to the acid proportion of themolecules.

As will be discussed below, in many cases theCWSPs appear to be special depositions of a singlepolysaccharide below a ‘normal’ primary cell wall(figure 1 G, H). It is therefore reasonable to supposethat during its deposition, either cellulose biosynthesisis suppressed or synthesis of cross-linked glycans areenhanced. It is not understood, however, how can astable cell wall be assembled without (or with minimalamounts of) cellulose, but this might be related withthe facilitation of mobilisation processes, which couldbe considerably more complex if cellulose werepresent.

Table I. Features of the principal storage polysaccharides in plants.

Storage compound Biosynthesis Mobilisation Cellular location Plant location

Starch From ADP-glucose Hydrolysis, phosphorylation Plastids, starch granules Seeds, leaves, roots, fruits,flowers and undergroundorgans

Fructans From sucrose by transglyco-sylation

Hydrolysis Vacuoles Leaves, roots, stems andunderground organs

Cell wallpolysaccharides

From UDP/GDP-sugars intothe Golgi apparatus

Hydrolysis, transglycosylation Cell wall Seeds, underground organs

142 M.S. Buckeridge et al.

Plant Physiol. Biochem.

3. OCCURRENCE, STRUCTUREAND PROPERTIES OF THE CWSPs

3.1. The mannan group

Species from different plant families of mono- anddicots store mannose-containing polysaccharides intheir seeds. All are based on variations of aâ-mannanbackbone, which might be interrupted with D-glucose,and/or branched withα-(1→6)-linked galactose.Depending on their structure and branching degree,these CWSPs may play distinct roles, from hardness inPalmae to water-related control in Leguminosae, butall having in common the storage function.

3.1.1. Mannans

The pure mannans are artificially defined as having90 % or more mannan with a linear chain ofâ-(1→4)-linked manopyranosyl residues with up to 10 % of themannose residues substituted by single units ofα-(1→6)-linked galactoses. At or under this percent-age, galactomannans become insoluble and precipitaterapidly from solution [19]. Thus, mannans are struc-turally related to galactomannans, but with fewergalactosyl branch-points. For this reason, they are(unlike galactomannans) insoluble in water and self-interactive, being to some extent crystalline in the cellwall. Mannans are found in monocotyledons (e.g.Phoenyx dactyliferaand Phytelephas macrocarpa(ivory nut mannan)) and in dicotyledons [60].

P. dactylifera seed germination was studied bySachs [69] and extended by Keusch [45]. In these

seeds, a small conical embryo develops slowly and itscotyledon is transformed into a haustorium, whichabsorbs the products of degradation of the reservesfollowing germination. In those seeds,â-mannanaseand â-mannosidase were detected in the dissolutionzone near the haustorium. Besides, it has been pro-posed that the haustorium might not be responsible forthe production of these enzymes [45]. Instead,enzymes would be activated in the endospermic cells,which are living and metabolically active, by anunknown signal coming from the haustorium. Theauthors, however, did not rule out the hypothesis thatinactive enzymes could have been secreted by thehaustorium and activated in the endosperm.

Mannans possibly have other functions apart frombeing reserve substances. The great hardness of thedate seed has been attributed to the presence of thispolymer in endosperm cell walls. In fact, mannan-containing seeds are, in general, very hard and resis-tant to mechanical damage.

Species, such as pepper [78], celery [44],tomato [36], lettuce [38], coffee [80] and datura [70],have been reported to possess mannan or to have anendosperm capable of producing endo-â-mannanase.Usually they have thinner endosperms which havebeen related to a constriction to radicle protrusion. Inmost of these cases, endosperm degradation is inducedby gibberellic acid and in some cases inhibited byabscisic acid (ABA).

Recently, Bewley et al. [4] cloned a cDNA encodingfor an endo-â-mannanase from tomato. They found alow homology with fungal mannanases (28–30 %) and

Table II. Some features of the principal cell wall storage polysaccharides and their occurrence.

Polysaccharide Residuein the mainchain

Branchingresidues

Nucleotidesugar neededforbiosynthesis

Hydrolytic enzymes involvedin mobilisation

Location in the plant

Mannans Mannose None,scarcelygalactose

GDP-man,UDP-gal

Endo-â-mannanase Seeds (Palmae, coffee, sesame)

Glucomannans Mannoseglucose

Galactose GDP-man,UDP-glc,UDP-gal

Endo-â-mannanase, Endo-â-glu-canase,α-galactosidase

Seeds(lettuce,tomato),andsubterra-nean organs (lily)

Galactomannans Mannose Galactose GDP-man,UDP-gal

Endo-â-mannanase,α-galactosi-dase, exo-â-mannanase

Seeds (Leguminosae, Convolvula-ceae, Annonaceae)

Xyloglucans Glucose Xylose,galactose,arabinose

UDP-glc,UDP-xyl,UDP-gal,

Xyloglucan-endo-â-transglycosy-lase, Xyloglucan-endo-â-gluca-nase,â-galactosidase,α-xylosi-dase,â-glucosidase

Seeds (Leguminosae, Tropaeola-ceae, Myrcinaceae)

Galactans Galactose Arabinose UDP-gal,UDP-ara

Exo-galactanase,α-arabinosidase Seeds (legumes), coffee

Storage polymer mobilisation 143

vol. 38 (1/2) 2000

also found that it is expressed in the endosperms butnot in other parts of the plant. This will possibly be avaluable tool for studying the control of one of themost important enzymes involved in mannan mobili-sation, especially concerning the mechanism of actionof the hormones (gibberellin and ABA) in mannan-containing seeds.

It is believed that in tomato and lettuce, mannanfunctions by increasing the hardness of the endosperm.The mannan present in the endosperm surrounding theroot cap of tomato has been shown to be an importantconstraint to radicle protrusion [34, 36]. It was foundthat the weakening of the endosperm, which is inducedby gibberellin, facilitates germination. Groot andKarssen [35] presented results showing that the effecton galactomannan degradation induced by gibberellincan be reversed by abscisic acid. Some authors affirmthat mannans present in the endosperm are also mobi-lised after germination (for example in tomato [77]and coffee [31, 75]) so that they can, to a certainextent, be considered as storage compounds.

The observations cited above on palms and othernon-legume mannan-containing seeds, suggest thatthis polymer may be considered as a bifunctionalmolecule. This polysaccharide might play a role as aconstrictor of radicle protrusion during germination(probably setting the time when radicle should startgrowing) as a storage polysaccharide after germina-tion, the latter mainly in palms and coffee seeds wheremannan yield is higher.

3.1.2. Galactomannans

Galactomannans are composed of a linear backboneof â-(1→4)-linked D-mannose residues to whichD-galactose residues are attached byα-(1→6)-linkages. Galactomannans are typical of the legumeseed endosperm (figure 1 A, B), but they also occur inseeds of other plant families such as Compositae andConvolvulaceae for example [18, 37]. Being one of thebiggest families in the plant kingdom, the Legumino-sae (with 18 000 species) has the highest number ofspecies studied to date. The ratio mannose:galactoseand the statistical distribution of galactosyl residues

along the mannan backbone vary from species tospecies, being of chemotaxonomical value [7, 13, 63].The three subfamilies of the Leguminosae (Caesalpin-ioideae, Mimosoideae and Faboideae) can be distin-guished by the mannose:galactose ratios of their seedgalactomannans.

Although a large number of plant species have beenrecorded to possess galactomannan in their seeds [3,13, 18, 30], only a few have their post-germinativemetabolism studied in detail. Among legumes, themost studied species are guar (Cyamopsis tetragonolo-bus), fenugreek (Trigonella foenum-graecum) andcarob (Ceratonia siliqua).

In seeds of fenugreek and guar, the endosperm isnon-living and the cells are almost totally filled withgalactomannan [56, 59]. In seeds of these species, analeurone layer is present which is thought to beresponsible for the production of the hydrolyticenzymes that promote the breakdown of the cell wallstorage polysaccharides following germination [60].On the other hand in seeds ofC. siliqua, endospermcells are living and galactomannan can be viewed aswall thickenings. In this case, there is no clear distinc-tion between endosperm and aleurone layer and theenzymes are probably produced and liberated into thecell walls by the endospermic cells.

The mobilisation in some other legumes was stud-ied [8, 12, 55, 64], confirming the presence of the threeenzymes mentioned above and also confirming thatgalactomannan mobilisation is performed throughhydrolysis. In all cases studied, the polysaccharide isdisassembled to its monosaccharide constituents (freemannose and galactose) at the same time as sucrose isproduced (figure 2). Apparently, sucrose is the sugar oftransport that will take the products of storage mobili-sation (carbon and energy) to the growing embryo.Starch is transiently produced in the cotyledons [8, 59]and recently Dirk et al. [22] proposed that storage cellwall degradation and starch synthesis might be bio-chemically related. McCleary and coworkers [54, 55]performed careful studies on the fate of the products ofguar galactomannan after mobilisation. They detectedthe activities of phosphomannoisomerase and phos-

Figure 1. Microscopic view of some legume seeds that store galactomannan (A, B), xyloglucan (C, D) and galactan (E–H). A, Seed ofSesbaniamarginata, with testa (t), endosperm (e) and cotyledons (c);B, higher magnification showing endosperm cells which accumulate large amounts ofgalactomannan;C, D, transversal cut of the cotyledons ofHymenaea courbaril, showing thickened xyloglucan-containing walls (stained in bluewith iodine) before and after mobilisation, respectively;E–H, galactan-containing lupin (Lupinus angustifolius) cotyledons before (E, G) and after(F, H) mobilisation.E, G, Light microscopy: f, pit fields; sw, storage wall; P, protein bodies.F, H, Transmission electron microscopy showing:c, cytoplasm; sw, storage wall; m, middle lamela; pr, primary wall. The dark staining spots are colloidal gold particles complexed with pureexo-â-galactanase fromL. angustifolius. In H, some galactan (sw) is still present at the end of mobilisation. PhotosE to H are by M.S. Buckeridgeand J.S.G. Reid. Magnifications:C, D = 400 ×;G = 22 500 ×;H = 18 000 ×;E, F, bars = 50µm.


vol. 38 (1/2) 2000

phoglucoisomerase in the endosperm and suggestedthat these enzymes are probably responsible for theepimerisation of mannose into glucose, which willprobably be used for sucrose synthesis. These authorsfed growing embryos with radioactive mannose andgalactose and demonstrated that the products of galac-tomannan mobilisation in guar are used for severalbiochemical processes in the growing plantlet [54].

In all legume species studied, galactomannanmobilisation starts after germination (i.e. radicle pro-trusion). It has been demonstrated that in endospermsof seeds of T. foenum-graecumand C. siliqua,α-galactosidase and endo-â-mannanase in the formerand α-galactosidase in the latter are synthesised de

novo [65, 72]. It is reasonable to think that eithermobilisation is induced after or held during germina-tion by some factor. The few attempts to inducepolysaccharide degradation using gibberellic acidfailed, suggesting that legume systems have a differentmetabolic control when compared with other mannan-containing seeds. On the other hand, jasmonic acid andits precursor linolenic acid have recently been shownto inhibit galactomannan degradation in carob andfenugreek [46].

Abscisic acid has been shown to act as a potentinhibitor of galactomannan degradation infenugreek [65] and carob [72]. It is possible to specu-late that ABA has a general role (in legumes and

Figure 2. Biochemical pathwaysinvolved in the catabolism of galacto-mannan and further metabolism of itsproducts by the embryo. When an aleu-rone layer is not present, it is likely thathydrolases are produced within eachendosperm cell and secreted outwards tothe cell wall where the same reactionoccurs (man, mannose; gal, galactose;SPS, sucrose phosphate synthase; Man-6-P, mannose-6-phosphate; Fru-6-P,fructose-6-phosphate; UDP-gal, uridinediphosphate galactose; Suc-6-P, sucrose-6-phosphate).



non-legumes) as a modulator of the biochemical andphysiological interactions between the endosperm andthe embryo following germination and early growth.Its presence inhibits galactomannan degradation andonly when it is leaked out or metabolised, does itswater-related function finish and the transference ofcarbon and energy between both organs, i.e. storagefunction, starts.

Besides playing a role as a post-germinative reserve,galactomannans can also serve as imbibing substancesin early stages of germination. It takes up proportion-ally high amounts of water and distributes it aroundthe embryo. The imbibed endosperm, protects theembryo against desiccation by buffering it againstwater-loss during post-imbibition drought [61]. Othertropical legumes on which similar studies have beenperformed (faveiro and sesbania) present a similarbehaviour, playing a role as the principal imbibingsubstance during the early periods of germination [8,12].

The emphasis on hardness instead of the storagefunction of galactomannan in non-legume species (seeabove) is probably due to the fact that they occur insmaller quantities in relation to many legumes andpalms. However, it is important to remember that somelegumes belonging to the subfamily Faboideae storerelatively small amounts of galactomannan in a thinendosperm as soybean for instance (see [18] for otherexamples). It is possible that a similar hardness func-tion is still preserved in legumes, but no studies of thiskind have been performed yet. Such experimentswould be important for understanding the ecologicalfunctions of galactomannan for seed germination andplantlet growth as well as the mechanisms of selectiondeveloped during evolution that led to these types ofadaptations.

3.1.3. Glucomannans

Of the CWSPs of the mannan group, the glucoman-nans are the least studied. They can be extracted withalkali from seeds of some species of Liliaceae(Asparagus offıcinalis[33] andEdymion mutans[32],Scilla nonscripta[76]) and Iridaceae (Iris ochroleucaand I. sibirica [2]). The structures of glucomannanshave been determined by methylation analysis. Theyhave a linearâ-(1→4)-linked backbone containingalmost equal numbers ofâ-glucopyranosyl andâ-mannopyranosyl residues. Some branching (3–6 %),with single (1→6) (probablyα-linked) galactopyrano-syl residues occurs.

3.2. The cell wall function in the mannan group

It seems quite clear from the information discussedabove on the mannan group as a whole, that there is astructure-function relationship which has a centralpoint in the degree and/or positioning of the galactoseresidues on theâ-mannan backbone. As galactosebranching approaches zero (pure mannans), their bio-logical function seems to be more related to hardness.This can be clearly seen in Palmae and other non-legume species. Conversely with higher degrees ofgalactosylation (fenugreek being the extreme case),the biological function of galactomannan includeswater-related functions. In both extremities, however,the storage function remains. Nevertheless, it is notknown which function is ‘primary’. Storage or water-related functions/hardness? It is certain, however, thatin both cases, (galacto)mannans are multifunctionalmolecules, playing their role during distinct phases ofthe plant’s lifetime. How this may have happenedduring evolution will be discussed later.

3.3. Xyloglucans

3.3.1. Occurrence and structure

The presence and mobilisation of xyloglucans fol-lowing seed germination were first reported in seeds ofImpatiens balsamina, Tropaeolum majusand Cycla-men europaeum[41, 67].

The botanical distribution of xyloglucans has beenreviewed by Kooiman [47] who used the ability ofxyloglucan to stain with iodine (showing a distinctiveblue colour) as a form of detection of these polymersin seeds (figure 1 C).

Seed xyloglucans have a mainâ-D-(1→4)-glucanbackbone branched withα-(1→6) linked D-xylo-pyranosyl or â-D-galactopyranosyl-(1→2)-D-xylo-pyranosyl residues [79]. Except for the absence ofterminal fucosyl unitsα-L-(1→2)-linked to theâ-D-galactosyl groups, there is a remarkable similaritybetween seed reserve xyloglucan and structural xylo-glucan from primary walls of dicotyledonous vegeta-tive tissues [39].

Using microbial cellulase, Kooiman [48] found thattamarind seed xyloglucan is composed of the hep-tasaccharide Glc4:Xyl3, with variation in the substitu-tion with galactose residues. The structure of theconstitutive oligosaccharide blocks of xyloglucansfrom several different sources, including seeds, waselucidated using microbial enzyme hydrolysis fol-lowed by analyses by methylation, mass spectra andnuclear magnetic resonance during the 80s and 90s


vol. 38 (1/2) 2000

(see [39] for a review). On the basis of the dataproduced until 1992, an unambiguous nomenclaturefor the structural blocks of xyloglucan has beenproposed [29]. This nomenclature takes the backboneas a central point. Unsubstituted glucose is assignedG;glucose branched with xylose is assignedX and ifgalactose is branching xylose, the trisaccharide isassignedL .

A comparative study of xyloglucans from seeds ofTropaeolum majus, Tamarindus indicaandCopaiferalangsdorffıi using highly purifiedTrichodermacellu-lase, showed the same four basic structural unitsXXXG, XLXG, XXLG and XLLG [11]. The ratiosbetween these units give rise to highly specific finestructures in different species and even between popu-lations of the same species growing in different envi-ronments. The analysis of the proportions among thestructural blocks were variable indicating differencesin galactose distribution along the main chain [11]. Adifference in xylose branching was recently found inxyloglucan from seeds ofHymenaea courbaril, thispolymer being composed of a mixture of XXXG andXXXXG which may be branched with galactose atdifferent positions [14].

In spite of these differences in fine structure, all seedxyloglucans examined present very close proportionsamong monosacharides, thus preserving the totaldegree of branching. Santos and Buckeridge (submit-ted) observed differences in the fine structure (distri-bution of blocks with different degrees of galactosy-lation) of xyloglucan from seeds ofH. courbarilrelated to seed imbibition speed. This can be taken asan evidence that seed xyloglucan may play anotherrole, besides storage.

3.3.2. Xyloglucan metabolism

The reserve function of xyloglucan in cotyledonshave been demonstrated for seeds ofT. majus[23], T.indica [66], C. langsdorffıi[11], H. courbaril (Tinéand Buckeridge, submitted). It was shown that xylo-glucan mobilisation in vivo is accompanied by the riseand fall of the activities of four hydrolases:â-galactosidase, endo-â-(1→4)-glucanase (or XET),α-xylosidase andâ-glucosidase.

Reid and co-workers have already isolated the fourmain enzymes responsible for xyloglucan degradationin T. majus. They are (a) xyloglucan-specific endo-â-(1→4)-D-glucanase or xyloglucan endotransglycosy-lase (XET) [24, 28]; (b) aâ-galactosidase with highspecificity towards xyloglucan [25]; (c) a xyloglucan-specific oligosaccharide-specificα-xylosidase or oli-

goxyloglucan exo-xylohydrolase [27]; and (d) a trans-glycosylatingâ-glucosidase [17].

On the basis of these results plus other studies onthe mode of action of XET [24, 28], Crombie etal. [17] proposed a tentative model for xyloglucanmobilisation in nasturtium. In this model, the fourenzymes are thought to work in a concerted fashionproducing galactose, glucose and xylose. In nastur-tium, XET andâ-galactosidase are the only enzymescapable of attacking the polymer. Under low concen-trations of xyloglucan oligosaccharides (acceptors),the hydrolytic activity predominates over XET [28].Thus, when in contact with high molecular massxyloglucan, hydrolysis predominates, producing oli-gosaccharides which are promptly attacked by theexo-glycosidases (α-xylosidase andâ-glucosidase),therefore reducing the polymer to its monosaccharideconstituents.

Reis et al. [66] described cytochemically the diges-tion of the xyloglucan-containing cell walls ofT.indica cotyledons. Using the techniques of iodinestaining and a gold-probe prepared by complexingEscherichia coliâ-galactosidase with gold particles,they were able to study xyloglucan mobilisation incotyledonary cell walls at the ultrastructural level withgreat specificity. They observed the presence of aninner and an outer wall, which are not degraded andbecome more apparent following xyloglucan mobili-sation. Also, a fibrous material was left after mobili-sation, showing that not all the wall is mobilised. Theyalso found that as xyloglucan is degraded, the propor-tions among monosaccharides (glucose:xylose:galac-tose) do not change significantly.

In C. langsdorffıi, the mobilisation of the thicken-ings of cotyledonary cell walls has been observedcytochemically, physiologically and biochemically byBuckeridge et al. [11]. They have studied two differentpopulations, from two distinct phytosociologicalregions (forest and savannah) and did not find apparentdifferences in xyloglucan mobilisation between seedsof the two environments. Recently, aâ-galactosidasewas purified fromCopaifera’s cotyledons (Alcântaraet al. submitted). Differently from nasturtiumâ-galactosidase, this enzyme showed very high speci-ficity towards certain xyloglucan oligosaccharides(XLXG and XLLG, where the Ls in bold representpositions attacked byâ-galactosidase) and was notactive on the polymer at all. Furthermore, its pHoptimum showed a very sharp peak at 3.2, out of theoptima of the other hydrolases which are around 4.5.

In cotyledons ofH. courbaril, Tiné et al. (unpub-lished) showed (physiologically and cytochemically,



figure 1 C, D) that xyloglucan is mobilised aftergermination. Concomitantly to xyloglucan disassem-bling, fructose, glucose and sucrose are produced.These authors detected the same four activities foundin nasturtium. They also found evidence for thepresence of transglycosylation activity (XET) in thisspecies. As happens withCopaifera, all â-galac-tosidase activity that can be detected usingp-nitrophenyl-galactopyranoside had a pH optimum at3.2, whereas the other hydrolases detected were activeat 4.5. The results obtained forCopaifera’s andHymenaea’s â-galactosidases suggest that this enzymemight be one of the important steps in the control ofseed xyloglucan metabolism in legumes.

Unlike galactomannans, no work has apparentlybeen published on the further metabolism of xyloglu-

can products. Preliminary evidence from our lab pointsto the existence of transient starch- and sucrose-basedtransport of the free sugars derived from the disassem-bling of xyloglucan of Hymenaea.On the basis ofthese discoveries, a tentative general model for xylo-glucan degradation was depicted (figure 3).

Recent results from our laboratory suggest that thecontrol of xyloglucan disassembling in muro may beexerted by changes in the wall pH, at least in legumes,as one of the enzymes (â-galactosidase) has a differ-ential optimum. The control of xyloglucan mobilisa-tion in vivo was studied [40]. They found that themobilisation of storage xyloglucan present in cotyle-dons of nasturtium is under control of auxin. Further-more, cotyledons appear to be receptive to the hor-mone only within a certain period of time so that auxin

Figure 3. Schematic representation of xyloglu-can degradation in seeds. A sequence ofXLXGXLLGXXXGXXLG is used as anexample of a segment of a xyloglucan polymerwith the non-reducing end towards the left. Thefirst attack is made by xyloglucan-endo-â-transglycosylase (XET) andâ-galactosidase(â-gal from nasturtium only). The oligosaccha-rides produced by the endo action are attackedbyâ-galactosidases (Nâ-gal, nasturtiumâ-galac-tosidase; Câ-gal,Copaiferaâ-galactosidase, thelatter being able to attack only oligosaccharidesat certain positions (galactose towards the non-reducing end)).α-Xylosidase andâ-glucosidaseperform alternate hydrolysis of terminal posi-tions at the non-reducing end. (*) In legumes(Copaifera langsdorffıiand Hymenaea cour-baril), after one round of action of these twoenzymes, galactose will be close to the non-reducing end again.â-Galactosidase can nowact on the oligosaccharide XLG, thus releasinggalactose and permitting the continuity of actionof the other two exo-glycosidases. In these twospecies, galactose retrieved from oligosaccha-rides are possibly limiting degradation, sincethey have a pH optima at 3.2, whereas the otherenzymes have an optima at pH 4.5.


vol. 38 (1/2) 2000

probably modulates the relationship between plantletgrowth and storage mobilisation in the cotyledons.

3.3.3. The wall function in seed xyloglucans

Although no direct evidence has been produced thatseed xyloglucans are dual-purpose molecules, such aproposition can be made on the basis of the fact thatxyloglucan possesses hydrodynamic properties whichare very close to galactomannans, suggesting similarfunctions as in imbibition and xeroprotection. Theobservations by Santos and Buckeridge (see above)that the degree of branching with galactose correlateswith seed size and imbibition speed inHymenaea,support this hypothesis. As pointed out for galacto-mannans, xyloglucan’s structure-function relationshipresides on changes in fine structure which are alsorelated to positioning of galactose in the molecule.

4. GALACTANS

Galactose-containing material in seed cell walls wasfirst detected in 1892 [71]. However, the identity of thegalactan as a distinct polysaccharide in seeds of thewhite lupin (Lupinus albus) was demonstrated in1947 [42]. On the basis of chemical structural deter-minations including methylation analysis, they con-cluded that the polysaccharide was aâ-(1→4)-linkedD-galactan.

In a thorough study of galactans from four speciesof lupins, Al-Kaisey and Wilkie [1] found that thereare two types of galactans in lupins seeds. One is aâ-(1→3),(1→6)-linked polysaccharide with some4-linkages, whereas the other, which is dominant, iscomposed ofâ-(1→4) linkages, having one in every16–21 residues 6-substituted by L-arabinofuranose.

Brillouet and Riochet [6] found a high positivecorrelation between the ratio galactose:arabinose inthe cell wall polysaccharides and the percentage of cellwall material in the seed. They also found a positivecorrelation between the amount of cell wall material inlupin cotyledons and the rhamnose:galacturonic acidratio. This correlation was attributed to an increase insites (rhamnosyl residues) for anchoring galactan side-chains to a pectic core.

The biochemistry of the post-germinative mobilisa-tion of CWSP (rich in galactan) fromLupinus angus-tifolius cotyledons has been described by Crawshawand Reid [16], and the ultrastructural changes accom-panying the mobilisation process have been docu-mented by Parker [58]. Before germination, the coty-

ledonary cell wall material is very rich in galactosyl(71 %) and arabinosyl (20 %) residues, the remainderbeing composed of small amounts of glucose, uronicacid and rhamnose. After germination most of thegalactose and arabinose were removed from the cellwall, leaving a residual wall enriched in rhamnose,uronic acid and glucose [16].

Matheson and Saini [51] reported the presence oftwo α-arabinosidases and threeâ-galactosidases ingerminating cotyledons ofLupinus luteus. Theseenzymes were reported to increase after germinationand the authors discussed the possibility of galactanbeing involved in cell expansion as well as a reservepolysaccharide.

Buckeridge and Reid [9] isolated a novel exo-â-(1→4)-galactanase from germinated cotyledons ofL.angustifolius. In fact, a family of immunologically-relatedâ-galactosidases, which increase after germi-nation and decrease after the period of reserve mobili-sation, was detected using affinity purified antibodiesagainst the main band of the exo-galactanase. Theâ-galactosidases are synthesised de novo, since nocross-reacting peptides were present in extracts fromquiescent lupin seeds.

The exo-galactanase is clearly a key enzyme in themobilisation of cell wall storage polysaccharides fromL. angustifoliuscotyledons after germination. It has avery high specificity towardsâ-(1→4)-galactan, thedominant structural component of the storage cellwalls. The levels of galactanase activity and galacta-nase protein vary in step with CWSP mobilisation.When the pure galactanase was incubated in vitro withsoluble lupin seed ‘galactan’, this enzyme was capableof releasing 82 % of the galactosyl residues in thepolysaccharide and 63 % of the galactosyl residuespresent in intact cell walls as free galactose (Buck-eridge, Hutcheon and Reid, unpubl. obs.).

On the basis of the structural and biochemical dataavailable, a tentative model for galactan degradation inlupin is depicted (figure 4). The galactan molecules aredrawn as being covalently attached via their reducingtermini to a pectic rhamnogalacturonan backbone.Indeed, it was confirmed that after CWSP mobilisationin vivo or treatment of cell walls with pure exo-galactanase in vitro, the residual wall material wasenriched in galacturonic acid and rhamnose residues.Furthermore, after galactan mobilisation, the cell wallscontain a residual fibrous material which did not stainwith the galactanase-gold probe (figure 1 H; Buck-eridge and Reid, unpubl.). If lupin galactan is presentas pectic side-chains, then it is reasonable to view it inthe same way as the storage xyloglucans present in



seeds of other species, namely as an amplification andadaptation to a storage role of a normal polysaccharidecomponent of the primary cell wall.

The exo-â-(1→4)-galactanase isolated by Buck-eridge and Reid [9] seems to be the most importantenzyme as far as storage cell wall mobilisation in lupincotyledons is concerned. However, post-germinativechanges in the cotyledonary cell wall as a whole gobeyond galactan mobilisation. Galactosyl residues,which may be present in molecules other thanâ-(1→4)-galactan and arabinose-containing polymersare also mobilised after germination. Besides, thecollapse of the cell walls in certain regions of thecotyledons with the simultaneous formation of airpockets after galactan mobilisation implies degrada-tion of components of the primary cell wall sensustrictu (see [58]). This suggests that pectinases and

perhaps cellulases may be active during the period ofaerenchyma formation. Whether or not the presence ofheavy branching of rhamnogalacturanan with galac-tans and arabinans is a major factor in preventing theaction of cellulases and pectinases during early stagesof germination, it is reasonable to think that theseneutral branching points could be controlling, to acertain extent, expansion and morphogenesis of thecotyledons.

Although the galactan in lupin cotyledons is areserve polysaccharide, it is not irrelevant to theprocess of cotyledonary expansion which followsreserve mobilisation. It may therefore be appropriateto characterise galactan as a dual purpose molecule,being not only a reserve substance, but also a molecu-lar restraint to expansion of cotyledons during devel-opment.

Figure 4. Reactions involved inthe mobilisation of storage poly-saccharides in lupins.â-(1→4)-D-Galactan is the dominant polymer.It is depicted as branching pointsof rhamnogalacturannan core withsome α-(1→5)-arabinan branchesnear the reducing end. One mol-ecule ofâ-(1→3),(1→6)-D-galac-tan is also represented although itoccurs in minor amounts. In thisdegradation system, only exo-enzymes have been detected, oneof which (exo-â-(1→4)-galacta-nase fromLupinus angustifolius) iscapable of releasing most (approxi-mately 60 %) of the intact cellwalls of the same species. In vivo,other galactosidases and arabinosi-dases are thought to act on thebranches leaving only rhamnoga-lacturonan. The fate of the prod-ucts is merely hypothetical in thisscheme.


vol. 38 (1/2) 2000

5. TRANSFERENCE OF FUNCTIONSIN WALL POLYSACCHARIDES

In 1996, Buckeridge and Reid [10] proposed thatthe cell wall storage polysaccharides of legumes mighthave been involved in cycles of transference of func-tions during evolution, which were part of the ‘trans-formations’ that led them from the primary cell wall tobecome storage compounds. The concept of cycles oftransference of functions (see [74]), could explain whymost CWSPs are considered multifunctional mol-ecules.

The general way by which cycles of transfer offunctions may have operated on CWSPs during evo-lution is depicted infigure 5. According to this hypoth-esis, a given polysaccharide would have a ‘primary’and at least one ‘secondary’ function. Different func-tions are played in different proportions so that inlegumes, for example, most storage polysaccharidespresent in seeds have their primary function as storage,but still preserving functions that were already part oftheir functions in primary walls, such as hardness inthe case of mannans or wall porosity in the case ofgalactans.

Considering the current model accepted for thearchitecture of the primary plant cell walls [15], inorder to arrive at the present stage, the transference offunctions probably demanded some key transforma-tions in the metabolism and properties of some cellwall polysaccharides. Three obvious steps were: 1)temporal displacement between biosynthesis and

hydrolysis; 2) severe increase in proportion of one ofthe polysaccharides either from the hemicellulosic orpectic matrix; and 3) changes in (fine) structureconcerning mainly the degree of branching of bothhemicellulose and pectins.

In the first two cases, the transformations probablyinvolved the mechanism of turnover of cell wallcomponents. During growth, it is currently assumedthat biosynthesis and degradation occur at the sametime and approximately with the same intensity, thisturnover being liable to be used transiently as storageunder certain conditions [50]. The exchange of carbon(in carbohydrates) between wall and intracellularmetabolism is balanced. Thus, the first change wouldhave been either the enhancement of biosynthesisand/or suppression of degradation of one of thepolysaccharides in the cell wall during seed matura-tion. At the same time, following germination, thereverse happens, i.e. hydrolysis is the principal bio-chemical event whereas synthesis is either absent orvery low.

If the phenomenon described above really hap-pened, one can assume that the basic changes probablyoccurred at the genetic level, i.e. the expression of thegenes that encode for the synthases and hydrolaseswere selected to be performed during different periodsof development and with varying intensities. Thishighlights the importance of studies on the moleculargenetics of the systems described, since it will benecessary to understand the control of expression ofthose genes in order to understand how evolutionoperated. Nevertheless, at present, only a few geneshave been cloned from seeds containing CWSPs andvery little has been done concerning their expression.However, the scarce evidence available is conducive tothe idea that hydrolases present in CWSP-containingsystems, are unique to them [4, 17, 21].

In the third case, it is clear that certain key structuralchanges occurred, while the function of some cell wallpolysaccharides such as galactomannans, xyloglucansand galactans were transferred to storage. In the threecases cited, the changes in distribution and degree ofgalactosylation are very apparent. This involves themechanisms of biosynthesis, which have been rela-tively less studied than hydrolysis. The only genecloned until now appears to be the one that encodes forfenugreek galactosyl transferase (Reid, pers. comm.).It is important to note that here some hydrolysisappears to be important too. This was proposed byEdwards et al. [26] and De Mason et al. [20] whoshowed thatα-galactosidase is involved in the finalchanges of galactomannan during seed maturation.

Figure 5. Representation of two possible steps of cycles of transfer-ence of function involved in cell wall polysaccharides during evolu-tion. In the first cycle, functions of the polymers when in the primarywall is boxed and in bold, whereas the storage function is consideredonly in the sense that turnover occurs and the polysaccharides can becompletely degraded and re-absorbed by the cell. From the first to thesecond cycle, the main function turns to storage (thick arrows), stillmaintaining secondary functions (italic) which play a role sometimeduring germination. This characterises the cell wall storage polysac-charides as multifunctional molecules.



Some changes in the fine structure of the polysac-charides were also necessary in order to constitute afunctional storage wall. One was the degree of galac-tosylation and/or the distribution of galactoses. Thischange, together with the lower content of cellulose,allowed the production of water soluble polysaccha-rides, possibly avoiding imbibition problems and at thesame time facilitating mobilisation, since intermolecu-lar interactions are not as strong as in the primary wall.In the case of mannans in non-legumes, the depletionof galactose permits intermolecular interactions tooccur among the main chains, conferring hardness tothe endosperm. This is probably related to the phe-nomenon of post-maturation that occurs in species ofPalmae and in other species and might be related to thecontrol of radicle protrusion.

In the specific case of xyloglucan, the suppressionof fucosylation was apparently an important step in thetransference of function from the primary to thestorage wall. This is possibly related to the facts thatfucosylated xyloglucan oligosaccharides have anti-auxin effect [57] and also that they interfere withintermolecular interactions [49].

Mixed-linked glucans (â-(1→3),(1→4)-linked) andarabinoxylans in grass seeds may be considered inter-mediate steps in the transference of functions. Despitethe changes in matrix proportions (these polysaccha-rides constitute up to 90 % of the cell wall [43]), thetotal amount of carbohydrate stored in the cell wall isfar less than the amount of starch, which is consideredthe main reserve in these seeds. However, as seen inmannans, small amounts of cell wall polysaccharidescan be a key element in the physiology of the seed.

In spite of the changes performed during evolutionthat led to alterations of the mobilisation systems inseeds, these systems still have much in common withthe primary wall, in relation to both metabolism andchemical properties of polysaccharides. Thus, it isreasonable to assume that the studies on CWSP are andwill lead to information that might help understandother important biochemical processes that are cur-rently under investigation, such as fruit ripening andcell expansion during growth.

REFERENCES

[1] Al-Kaisey M.T., Wilkie C.B., The polysaccharides ofagricultural lupin seeds, Carbohydr. Res. 227 (1992)147–161.

[2] Andrews P., Hough L., Jones J.K.N., Mannose-containing polysaccharides. Part 3. The polysaccha-rides in the seeds ofIris ochroleucaand I. sibirica, J.Chem. Soc. 79 (1953) 1186–1192.

[3] Anulov O.V., Smirnova N.I., Mestechkina N.M.,Shcherbukhin V.D., Content and composition of non-starch water-soluble polysaccharides in seeds of someFabaceae, Russ. J. Plant Physiol. 45 (1998) 802–804.

[4] Bewley J.D., Burton R.A., Morohashi Y., FincherG.B., Molecular cloning of a cDNA enconding a(1→4)-â-mannan endohydrolase from the seeds oftomato (Lycopersicon esculentum), Planta 203 (1997)454–459.

[5] Bieleski R.L., Fructan hydrolysis drives petal expan-sion in the ephemeral daylily flower, Plant Physiol.103 (1993) 213–219.

[6] Brillouet J.M., Riochet D., Cell wall polysaccharidesand lignin in cotyledons and hulls of seeds fromvarious lupins (LupinusL.) species, J. Sci. Food Agric.34 (1983) 861–868.

[7] Buckeridge M.S., Dietrich S.M.C., Galactomannanfrom Brasilian legume seeds, Rev. Bras. Bot. 13 (1990)109–112.

[8] Buckeridge M.S., Dietrich S.M.C., Mobilisation of theraffinose family oligosaccharides and galactomannanin germinating seeds ofSesbania marginataBenth.(Leguminosae-Faboideae), Plant Sci. 117 (1996)33–43.

[9] Buckeridge M.S., Reid J.S.G., Purification and prop-erties of a novelâ-galactosidase or exo-(1,4)-â-D-galactanase from the cotyledons of germinatedLupi-nus angustifoliusL. seeds, Planta 192 (1994) 502–511.

[10] Buckeridge M.S., Reid J.S.G., Major cell wall polysac-charides in legume seeds: Structure, catabolism andbiological functions, Ciênc. Cult. 48 (1996) 153–162.

[11] Buckeridge M.S., Rocha D.C., Reid J.S.G., DietrichS.M.C., Xyloglucan structure and post-germinativemetabolism in seeds ofCopaifera langsdorffıifromsavana and forest populations, Physiol. Plant. 86(1992) 145–151.

[12] Buckeridge M.S., Panegassi V.R., Dietrich S.M.C.,Storage carbohydrate mobilisation in seeds ofDimor-phandra mollisBenth. (Leguminosae) following ger-mination, Rev. Bras. Bot. 18 (1995) 171–175.

[13] Buckeridge M.S., Panegassi V.R., Rocha D.C.,Dietrich S.M.C., Seed galactomannan in the classifi-cation and evolution of the leguminosae, Phytochem-istry 38 (1995) 871–875.

[14] Buckeridge M.S., Crombie H.J., Mendes C.J.M., ReidJ.S.G., Gidley M.J., Vieira C.C.J., A new family ofoligosaccharides from the xyloglucan ofHymenaeacourbaril L. (Leguminosae) cotyledons, Carbohydr.Res. 303 (1997) 233–237.

[15] Carpita N.C., Gibeaut D.M., Structural models ofprimary cell walls in flowering plants: consistency ofmolecular structure with the physical properties of cellwall during growth, Plant J. 3 (1993) 1–30.


vol. 38 (1/2) 2000

[16] Crawshaw L.A., Reid J.S.G., Changes in cell-wallpolysaccharides in relation to seedling developmentand the mobilisation of reserves in the cotyledons ofLupinus angustifoliuscv. Unicrop, Planta 160 (1984)449–454.

[17] Crombie H.J., Chengappa S., Hellyer A., Reid J.S.G.,A xyloglucan oligosaccharide-active, transglycosilat-ing â-D-glucosidase from the cotyledons of nasturtium(Tropaeolum majusL.) seedlings-purification, proper-ties and characterization of a cDNA clone, Plant J. 15(1998) 27–38.

[18] Dea I.C.M., Morrison A., Chemistry and interactionsof seed galactomannans, Adv. Carbohydr. Chem. Bio-chem. 31 (1975) 241–312.

[19] Dea I.C.M., Clark A.H., McCleary B.V., Effect ofgalactose substitution-pattern on the interaction prop-erties of galactomannans, Carbohydr. Res. 147 (1986)275–294.

[20] De Mason D.A., Madore M.A., Sekhar K.N.C., HarrisM.J., Role ofα-galactosidase in cell wall metabolismof date palm (Phoenix dactylifera) endosperm, Proto-plasma 166 (1992) 177–184.

[21] de Silva J., Jarman C.D., Arrowsmith D.A., StronachM.S., Sumant Sidebotton C., Reid J.S.G., Molecularcharacterization of a xyloglucan-specific endo-(1→4)-â-D-glucanase (xyloglucan endo-transglycosylase)from nasturtium seeds, Plant J. 3 (1993) 701–711.

[22] Dirk L.M.A., van der Krol A.R., Vreugdenhil D.,Hilhorst H.W.M., Bewley J.D., Galactomannan,soluble sugar and starch mobilization following ger-mination of Trigonella foenum-graecumseeds, PlantPhysiol. Biochem. 37 (1999) 41–50.

[23] Edwards M., Dea I.C.M., Bulpin P.V., Reid J.S.G.,Xyloglucan (amyloid) mobilisation in the cotyledonsof Tropaeolum majusL. seeds following germination,Planta 163 (1985) 133–140.

[24] Edwards M., Dea I.C.M., Bulpin P.V., Reid J.S.G.,Purification and properties of a novel xyloglucan-specific endo-â-(1,4)-D-glucanase from germinatingnasturtium seeds (Tropaeolum majusL.), J. Biol.Chem. 261 (1986) 9489–9494.

[25] Edwards M., Bowman J.L., Dea I.C.M., Reid J.S.G., Aâ-D galactosidase from nasturtium (Tropaeolum majusL.) cotyledons, J. Biol. Chem. 263 (1988) 4333–4337.

[26] Edwards M., Scott C., Gidley M.J., Reid J.S.G.,Control of mannose galactose ratio during galactoman-nan formation in developing legume seeds, Planta 187(1992) 67–74.

[27] Fanutti C., Gidley M.J., Reid J.S.G., A xyloglucanoligosaccharide specificα-D-xylosidase or exo-oligoxyloglucan-α-xylohydrolase from germinatednasturtium (Tropaeolum majusL.) seeds. Purification,properties and its interaction with a xyloglucan-specific endo-â-(1,4)-glucanase and other hydrolasesduring storage xyloglucan mobilisation, Planta 184(1991) 137–147.

[28] Fanutti, C., Gidley M.J., Reid J.S.G., Action of a purexyloglucan endo-transglycosilase (formerly calledxyloglucan-specific endo-(1,4)-â-D-glucanase) fromthe cotyledons of germinated nasturtium seeds, Plant J.3 (1993) 691–700.

[29] Fry S.C., York W.S., Albersheim P., Darvill A.,Hayashi T., Joseleau J.P., Kato Y., Lorences E.P.,MacLachlan G.A., McNeil M., Mort A.J., Reid J.S.G.,Seitz H.U., Selvendran R.R., Voragen A.G.J., WhiteA.R., An unambiguous nomenclature for xyloglucan-derived oligosaccharides, Physiol. Plant. 89 (1993)1–3.

[30] Ganter J.L.M.S., Zawadzkibaggio S.F., Leiter S.C.S.,Sierakowski M.R., Reicher F., Structural studies ongalactomannans from Brazilian seeds, J. Carbohydr.Chem. 12 (1993) 753–767.

[31] Giorgini J.F., Comoli E., Effect of embryo and exog-enous GA3 on endospermic endo-â-mannanase activ-ity of Coffea arabicaL. during germination and earlyseedling growth, Braz. J. Plant Physiol. 8 (1996)43–49.

[32] Goldberg R., Étude des polysaccharides de reserve dedeux graines de liliacées :Asparagus offıcinalisL. etEndymion nutans, Phytochemistry 8 (1969)1783–1792.

[33] Goldberg R., Guillou L., Prat R., Dubacq J.P., RolandJ.C., Structure and biochemistry of endosperm break-down inAsparagus offıcinalisseedlings, Plant Physiol.Biochem. 30 (1992) 477–485.

[34] Groot S.P.C., Karssen C.M., Gibberellins regulateseed-germination in tomato by endosperm weakening– a study with gibberellin-deficient mutants, Planta171 (1987) 525–531.

[35] Groot S.P.C., Karssen C.M., Dormancy and germina-tion of abscissic acid-deficient tomato seeds – studieswith the sitiens mutant, Plant Physiol. 99 (1992)952–958.

[36] Groot S.P.C., Kieliszewskarokicka B., Vermeer E.,Karssen C.M., Gibberellin-induced hydrolysis ofendosperm cell walls and gibberellin-deficient tomatoseeds prior to radicle protrusion, Planta 174 (1988)500–504.

[37] Guzmán J.M., Hernandez G.L., Anatomía de la semillay germinación deTurbina corumbosa(L.) Raf., Con-volvulaceae, Phyton 42 (1982) 1–8.

[38] Halmer P., Bewley J.D., Mannanase production by thelettuce endosperm: control by the embryo, Planta 144(1979) 333–340.

[39] Hayashi, T., Xyloglucans in the primary cell wall,Annu. Rev. Plant Physiol. Plant Mol. Biol. 40 (1989)139–168.

[40] Hensel A., Brummell D.A., Hanna R., MacLachlan G.,Auxin-dependent breakdown of xyloglucan in cotyle-dons of germinating nasturtium seeds, Planta 183(1991) 321–326.

[41] Heinricher E., Zur Biologie der gattungImpatiens,Flora Jena 71 . (1888)

[42] Hirst E.L., Jones J.K.N., Walder W.O., Pectic sub-stances. Part 7: the constitution of the galactan fromLupinus albus, J. Chem. Soc. (1947) 1225–1229.



[43] Hrmova M., Banik M., Harvey A.J., Garret T.P.J.,Varghese J.N., Hol P.B., Fincher G.B., Polysaccharidehydrolases in germinated barley and their role in thedepolymerisation of plant and fungal cell walls, Int. J.Bio. Macromol. 21 (1997) 67–72.

[44] Jacobsen J.V., Pressmann E.A., Structural study ofgermination in celery (Apium graveolensL.) seed withemphasis on endosperm breakdown, Planta 144 (1979)241–248.

[45] Keusch L., Die mobilisierung des reservemannans imkeimenden Dattelsamen, Planta 78 (1968) 321–350.

[46] Kontos F., Spyropoulus C.G., Effect of linoleic, lino-lenic and jasmonic acid on the production ofα-galactosidase and endo-â-mannanase in theendosperms of carob and fenugreek seeds, J. PlantPhysiol. 149 (1996) 629–632.

[47] Kooiman P., On the occurence of amyloids in plantseeds, Acta Bot. Neerl. 9 (1960) 208–219.

[48] Kooiman P., The constitution ofTamarindus-amyloid,Rec. Trav. Chim. Pays-Bas 80 (1961) 849–865.

[49] Levy S., MacLachlan G., Staehelin L.A., Xyloglucansidechains modulate binding to cellulose duringinvitro binding assays as predicted by conformationaldynamic simulations, Plant J. 11 (1997) 373–386.

[50] Lozovaya V.V., Zabotina O.A., Widholm J.M., Synthe-sis and turnover of cell-wall polysaccharides andstarch in photosynthetic soybean suspension cultures,Plant Physiol. 111 (1996) 921–929.

[51] Matheson N.K., Saini H.S.,α-L-arabinofuranosidasesand â-D-galactosidases in germinating-lupin cotyle-dons, Carbohydr. Res. 57 (1977) 103–116.

[52] Mayer A.M., Poljakoff-Mayber A., The Germinationof Seeds, Pergamon Press, Exeter, 1975.

[53] McCann M.C., Roberts K., Architecture of the primarycell wall, in: Lloyd C.W. (Ed.), The Cytoskeletal Basisof Plant Growth and Form, Academic Press, London,1991, pp. 109–129.

[54] McCleary B.V., Enzymic interactions in the hydrolysisof galactomannan: the role of exo-â-mannanase, Phy-tochemistry 22 (1983) 649–658.

[55] McCleary B.V., Matheson N.K., Galactomannan utili-sation in germinating legume seeds, Phytochemistry15 (1976) 43–47.

[56] McClendon J.H., Nolan W.G., Wenzler H.F., The roleof the endosperm in the germination of legumes:galactomannan, nitrogen, and phosphorus changes inthe germination of guar (Cyamopsis tetragonolobus,Leguminosae), Am. J. Bot. 63 (1976) 790–797.

[57] McDougall G.J., Fry S.C., Xyloglucan oligosaccha-rides promote growth and activate cellulase: Evidencefor a role of cellulase in cell expansion, Plant Physiol.93 (1990) 1041–1048.

[58] Parker M.L., Cell wall storage polysaccharide in coty-ledons of Lupinus angustifoliusL. II mobilisationduring germination and seedling development, Proto-plasma 120 (1984) 233–241.

[59] Reid J.S.G., Reserve carbohydrate metabolism in ger-minating seeds ofTrigonella foenun-graecumL.(Legum.), Planta 100 (1971) 131–142.

[60] Reid J.S.G., Structure and function in legume-seedpolysaccharides, in: Brett C., Hillman J.R. (Eds.),Biochemistry of the Plant Cell Walls, Cambridge Univ.Press, 1985, pp. 259–268.

[61] Reid J.S.G., Bewley J.D., A dual role for theendosperm and its galactomannan reserve in the ger-minative physiology of fenugreek (Trigonella foenun-graecumL.) an endospermic leguminous seed, Planta147 (1979) 145–150.

[62] Reid J.S.G., Edwards M., Galactomannans and othercell wall storage polysaccharides in seeds, in: StephenM.A. (Ed.), Food Polysaccharides and their Applica-tions, 1995, pp. 155–186.

[63] Reid J.S.G., Meier H., Chemotaxonomic aspects of thereserve galactomannan in leguminous seeds, Z. Pflan-zenphysiol. 62 (1970) 89–92.

[64] Reid J.S.G., Meier H., The function of the aleuronelayer during galactomannan mobilization in germinat-ing seeds of fenugreek (Trigonella foenum-graecumL.), crismon clover (Trifolium incarnatumL.): a cor-relative biochemical and ultrastructural study, Planta106 (1972) 44–60.

[65] Reid J.S.G., Meier H., Enzyme activities and galacto-mannan mobilisation in germinating seeds offenugreek (Trigonella foenum-graecumL. Legumino-sae). Secretion ofα-galactosidases andâ-mannosidaseby aleurone layer, Planta 112 (1973) 301–308.

[66] Reis D., Vian B., Darzens D., Roland J.C., Sequentialpatterns of intramural digestion of galactoxyloglucanin tamarind seedlings, Planta 170 (1987) 60–73.

[67] Reiss R., Über die Natur der Reservecellulose undüber ihre Auflösungweise bei der Keimung der Samen,Landwirtsch Jahrb. 18 (1889) 711–765.

[68] Rose J.K.C., Bennett A.B., Cooperative disassemblingof the cellulose-xyloglucan network of plant cell walls:parallels between cell expansion and fruit ripening,Trends Plant Sci. 4 (1999) 176–183.

[69] Sachs J., Zur Keimungsgeschichte der Dattel, Bot.Zeitung 20 (1862) 241–246; 249–252.

[70] Sánchez R.A., Sunell L., Labavitch J.M., Bonner B.A.,Changes in the endosperm cell walls of twoDaturaspecies before radicle protrusion, Plant Physiol. 93(1990) 89–97.

[71] Schulze E., Steiger E., Zur Kenntnis des Paragalak-tans, Landwirtsch. Vers. Stn. 41 (1892) 220–223.

[72] Seiler A., Glaktomannanabbau in keimenden Johanis-brotsamen (Ceratonia siliquaL.), Planta 134 (1977)209–221.

[73] Somme R., Glycosidases and monosaccharides ingerminating leguminous seeds, Acta Chem. Scand. 24(1970) 72–76.

[74] Stebbins G.L., Seeds, seedlings and the origin ofangiosperms, in: Beck C.B. (Ed.), Columbia Univer-sity Press, New York, 1974, pp. 300–311.

[75] Takaki M., Dietrich S.M.C., Effect of GA3 and light onpolysaccharide levels and metabolism in germinatingcoffee seeds, J. Exp. Bot. 31 (1980) 1643–1649.

[76] Thompson J.L., Jones J.K.N., The glucomannan ofbluebell seed (Scylla nonscriptaL.), Can. J. Chem. 42(1964) 1088–1091.


vol. 38 (1/2) 2000

[77] Toorop P.E., Bewley J.D., Hilhorst H.W.M., Endo-mannanase isoforms are present in the endosperm andembryo of tomato seeds, but are not essentially linkedto the completion of germination, Planta 200 (1996)153–158.

[78] Watkins J.T., Cantliffe D.J., Huber D.J., Nell T.A.,

Gibberellic acid stimulated degradation of endospermin pepper, J. Am. Soc. Hort. Sci. 110 (1985) 61–65.

[79] White E.V., Rao P.S.,J. Am. Chem. Soc.75 (1953)2617, [47] Apud Kooiman, (1960).

[80] Wolfron M.L., Laver M.L., Patin D.L., Carbohydratesof the coffee bean. II isolation and characterization ofmannan, J. Org. Chem. 26 (1961) 4533–4531.



Mobilisation of storage cell wall polysaccharides in seeds

Documents

Transcript of Mobilisation of storage cell wall polysaccharides in seeds