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First published online July 9, 2004; 10.1104/pp.104.043679 Plant Physiology 135:1305-1313 (2004) © 2004 American Society of Plant Biologists Loss of Highly Branched Arabinans and Debranching of Rhamnogalacturonan I Accompany Loss of Firm Texture and Cell Separation during Prolonged Storage of Apple1Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana 47907–2054
Growth and maturation of the edible cortical cells of apples (Malus domestica Borkh) are accompanied by a selective loss of pectin-associated (1  4)- -D-galactan from the cell walls, whereas a selective loss of highly branched (15)- -L-arabinans occurs after ripening and in advance of the loss of firm texture. The selective loss of highly branched arabinans occurs during the overripening of apples of four cultivars (Gala, Red Delicious, Firm Gold, and Gold Rush) that varied markedly in storage life, but, in all instances, the loss prestages the loss of firm texture, measured by both breaking strength and compression resistance. The unbranched (15)-linked arabinans remain associated with the major pectic polymer, rhamnogalacturonan I, and their content remains essentially unchanged during overripening. However, the degree of rhamnogalacturonan I branching at the rhamnosyl residues also decreases, but only after extensive loss of the highly branched arabinans. In contrast to the decrease in arabinan content, the loss of the rhamnogalacturonan I branching is tightly correlated with loss of firm texture in all cultivars, regardless of storage time. In vitro cell separation assays show that structural proteins, perhaps via their phenolic residues, and homogalacturonans also contribute to cell adhesion. Implications of these cell wall modifications in the mechanisms of apple cortex textural changes and cell separation are discussed.
Loss of firm texture and cell adhesion are ripening-associated processes that affect fruit quality and postharvest storage. Because the pectin substances are enriched in the walls of fruit cells compared to primary walls of other growing cells and because they constitute major components of the middle lamellae, these acidic polysaccharides have long been suspected to play key roles in fruit ripening (Jarvis, 1984  ; Brummel and Harpster, 2001). Over the years changes in pectin composition during fruit ripening have been studied extensively in many species, but the association of biochemical changes with changes in fruit texture is still unclear. Pectin depolymerization has little impact on wall swelling and softening during tomato (Lycopersicon esculentum) fruit ripening (Smith et al., 1988), and in other instances the swelling state of several fruit walls may change markedly without significant pectin depolymerization (Redgwell et al., 1997). Rose et al. (1998) show that wall swelling and softening may be accompanied by pectin depolymerization events, but the events are either not the only requirements or they may be unrelated to ripening. One of the surprises that emerged from the completion of the Arabidopsis genome sequence is the large number of genes that putatively encode polysaccharide degrading enzymes (Arabidopsis Genome Initiative, 2000). For example, Arabidopsis contains more than 250 genes that encode enzymes that are related to those that depolymerize pectins (Henrissat et al., 2001). This significant allotment of the genome toward pectin hydrolysis forces plant biologists to reconsider subtle roles of pectins in wall swelling and softening.
Most cell walls of growing tissues from edible fruit have a composition and architecture characteristic of the Type I primary cell wall, a wall generally found among all dicotyledonous and about one-half of the monocotyledonous species (Carpita and Gibeaut, 1993
The edible portion of apple (Malus domestica Borkh) is not a true fruit but fleshy tissue derived from floral tube (hypanthium; Esau, 1977
Growth of Red Delicious Apples
The pattern of growth of Red Delicious apples is typical of pomes (Fig. 1, A and B). These apples enlarge quickly during the first 3 to 4 weeks, with growth a result of both cell division and extension, but after 1 month, growth is primarily a result of cell expansion (Tukey and Young, 1942
Monosaccharide Composition and Linkage Structure of Apple Cell Walls during Development and Ripening
Ara (approximately 30%), Gal (approximately 20%), and GalA (approximately 20%) are the major monosaccharides in the walls of rapidly enlarging apples (cv Red Delicious). Gal and Ara levels decrease drastically during development but at distinctly different stages. Gal is lost primarily during the cell enlargement phase and is at its lowest levels upon maturation (approximately 8 mol%), whereas Ara is at its highest levels during maturation and ripening (approximately 25 mol%) and is lost primarily upon subsequent storage at ambient temperature. Linkage analysis shows that galactosyl residues are mostly nonreducing terminal and 4-linked, the latter indicating unbranched (1
Loss of Firm Texture during Storage To determine the role of Ara in the softening that accompanies apple overripening, we studied four cultivars that varied markedly in storage life: Gala, which ripens earliest and exhibits rapid overripening, followed by later-ripening Red Delicious, Firm Gold, and Gold Rush, the latter of which ripens the latest in the season and exhibits a protracted shelf life. Texture analysis included determination of the breaking strength of tissue cylinders and resistance to compression of tissue plugs. These experiments allowed us to differentiate between physical behavior and physiological age in our correlations of the biochemical changes in polysaccharide structure. Texture analysis showed that these apples exhibit different firm textures at harvest and soften at different rates during the storage (Fig. 3). Of the four cultivars studied, Gala showed the least firm texture at harvest (Fig. 3). The force necessary to compress or break the apple tissue continuously decreased during the 6 weeks of ambient temperature storage, after which cell separation became obvious. Red Delicious apples displayed firmer texture at harvest than Gala (Fig. 3). After the first week of storage, their breaking forces were lowered, whereas there was little change in the resistance to compression during the first 3 weeks of storage. Afterward, the firm texture was lost quickly, and loss of cell adhesion was observed after 6 weeks. A different behavior is found in Firm Gold apples (Fig. 3), which displayed firmer textures at harvest than Red Delicious and Gala but softened faster. In only 4 weeks the force required for breakage decreased to a level that was maintained during the remainder of storage. Gold Rush apples had the firmest texture at harvest and were capable of much longer storage (11 weeks without cell separation) than the other cultivars (Fig. 3). Gold Rush and Red Delicious apples maintained firm textures at 4°C for more than 12 weeks. Gala apples softened slightly during the cold storage. On the other hand, Firm Gold apples conserved at 4°C softened at the same rate as apples at ambient temperature but with a 1-week delay. Because the tissue compression assay is independent of the cell turgor and more dependent on cell separation, the similarity of compression and breaking strength tests indicated that cell turgor is not a principal factor in firm texture. After 5 week of storage, Gold Rush apples exhibited a noticeable loss of turgor, and the resultant increase in tissue flexibility made it impossible to break under the standardized conditions. However, loss of turgor was independent from the compression behavior of the tissue, and significant loss of texture was observed only after 6 weeks of storage. With the exception of Firm Gold, maintenance of firm texture was correlated with lateness of harvest.
Changes in Composition of the Cell Wall during Apple Softening Given the marked differences in the storage behavior, we examined sugar composition and linkage structure to determine the principal changes that might be linked to the textural changes. Despite the differences of firm texture found between apples of the four cultivars, sugar analyses showed similar cell wall compositions at harvest. Ripe apple cell walls contained GalUA, Ara, and Xyl as predominant noncellulosic sugars (Table I). GalUa was the most abundant monosaccharide, with values between 32 and 40 total mol%. GalUA levels slightly decreased in the four cultivars during the storage, and for Red Delicious and Gold Rush they decreased more notably coincident with cell separation. Ara is the principal neutral sugar at this stage, with values between 24 and 27 mol%. The major event associated with the storage in the four cultivars was a marked decrease in Ara content that always preceded the loss of firm texture. The Ara contents also decreased before fruit softening in Firm Gold apples that softened early at 4°C. On the other hand, Gal levels were very low and were maintained without change through the storage period. Gold Rush apples had higher levels of Gal at harvest than the others, but the content decreased quickly during the first week of storage and then maintained levels observed in the other cultivars. Xyl content was between 14 and 19 mol% at harvest and increased relatively during storage. In the end of the storage period, Xyl became the predominant neutral sugar.
Linkage Analysis Linkage compositions of these apple cell walls were consistent with the predominant polysaccharides reported for ripe apples (Table I). Most of the GalA in ripe apples was 4-linked. The 3,4-GalA residues (4%–6%) indicated the presence of a xylogalacturonans in these apples. Although total uronic acid content decreased slightly, 3,4-GalA increased relative to 4-GalA, indicating that xylogalacturonans enriched relative to HG during the apple softening. The exception was in Gala, where the ratio of 4-GalA to 3,4-GalA remained constant. The major linked neutral sugar was 5-Ara, which accounted for about one-half of the total Ara in the cell wall. The remainder of the Ara was in the branch-point residues 3,5- and 2,5-Ara, with corresponding nonreducing t-Ara residues. The degree of branching decreased markedly during the apple softening, with concomitant loss of t-Ara residues. The decrease in total Ara is primarily a result of loss of these branched and terminal furanosyl residues (Fig. 4). Most of the Ara remaining in the cell wall upon loss of texture was 5-Ara. In all instances, the loss of branched Ara prestages the softening. Firm Gold apples soften faster than all others, and even soften during the cold storage, and even in this different behavior the loss of branched arabinans precedes fruit softening. The degree of branching of the RG I was determined from the ratio of 2-Rha to 2,4-Rha (Fig. 4). At harvest, Gala and Red Delicious give ratios of about 0.6, and higher values were found for the firmer cultivars: 0.92 for Firm Gold and 1.38 for Gold Rush. The degree of branching decreased through the storage period in each of the four cultivars. This decrease was strongly correlated with the loss of apple firm texture in all cultivars. However, the decrease of degree of branching of the RG I was not accounted for by the decrease in branched arabinan side chains. About 50% of the total decrease in Gala and Red Delicious apples and between 25% to 30% in Firm Gold and Gold Rush occurred after the extensive loss of branched arabinans.
We tested different chemical solvents and enzymes that could mimic the cell separation in vitro to determine other cell wall components that could be implicated in the maintenance of cell adhesion. All four cultivars exhibited a similar behavior, and an example of this behavior in Gold Rush is shown in Figure 5. Separation was enhanced by CDTA, which disrupts the pectin association in the middle lamella. A similar response was obtained by oxidation of the phenolic substances with acidic sodium chlorite. Incubation with pectinase separated the tissue in clumps rather than effecting complete cell separation. Tissues maintain integrity after incubation for 2 h with water at ambient temperature, water at 70°C, or proteinase K.
The microcompression tests showed that CDTA, polygalacturonase, proteinase K, hot water, and acidic sodium chlorite each decreased tissue stiffness similarly in all four cultivars (Fig. 6A). Because sodium chlorite can oxidize phenolic residues in structural proteins, we determined if the proteinase K and the sodium chlorite had the same target molecule. Using Gold Rush as a model with the firmest texture suitable for sequential treatments, sodium chlorite treatment of tissues preincubated with proteinase K produced an additional softening of the tissue (Fig. 6B). On the other hand, Ca2+ added to the incubation solution during the sodium chlorite treatment prevented part of the softening that occurred by heating the tissue but did not prevent the softening produced by treatment with sodium chlorite.
We found that the Gal- and Ara-rich side chains of pectins are extensively degraded in the cell wall of Red Delicious apple during development and ripening, but at distinctly different stages. Gal was mostly lost from the 4-linked galactan side chains of the RG I before fruit maturity, whereas loss of Ara is associated with the ripening, especially with the onset of the overripened state. The deposition of (1 4)--D-galactan is associated with the increase of firmness of pea cotyledons (McCartney et al., 2000). In intact Arabidopsis seedlings, the (14)--D-galactan epitope occurs in a restricted manner in epidermal, cortical, and endodermal cell walls and marks the transition zone at or near the onset of rapid cell elongation (McCartney et al., 2003). In apples, galactan is lost primarily during the cell enlargement phase, and the lowest levels were found upon maturation (Fig. 2). After this stage the neutral side chains attached to the RG I are basically arabinans. In the ripe stage, Ara, Xyl, and GalA are the predominant noncellulosic sugars in cell walls of apples of the four cultivars. Similar results have been reported before for ripe apples (Aspinall and Fanous, 1984; Schols et al., 1995; Redgwell et al., 1997). Most of the GalA in ripe apples was 4-linked, but the 3,4-GalA residues and the corresponding nonreducing t-Xyl residues present indicated the presence of a xylogalacturonans in these apples, as has been reported (Schols et al., 1995). Xylogalacturonans enriched relative to HG during the apple overripening with the exception of Gala, where the relative proportions remain constant. This result suggests no association of the xylogalacturonans with the wall softening process. Curiously, the degrees of branching decrease in the overripe apples in all four cultivars, whereas the amounts of 5-linked arabinan remain essentially unchanged or decrease only slightly (Table I). These results indicate that two populations of arabinan, one with relatively unbranched (15)--L-Ara residues and the other highly branched, are present in different locations in the wall and exhibit different behaviors during ripening. The highly branched arabinan should be more susceptible to enzymatic degradation and extractions with the traditional methods for pectin isolation, and their structure and extractability are consistent with behavior of these pectic arabinans reported previously (Aspinall and Fanous, 1984; Redgwell et al., 1997; Perez et al., 2000). The linear (15)--L-arabinans that are tightly associated with cellulose and less accessible for enzymes may be responsible for the high amount of Ara that remains in the alkali-insoluble -cellulose residue in apple (Watt et al., 1999), even after endopolygalacturonase treatment of this residue (Redgwell et al., 1997). Arabinans are attached to the O-4 position of rhamnose in the RG I (Brett and Waldron, 1996). The extensive loss of short, highly branched arabinan chain may be responsible for the initial decrease observed of the degree of branching of RG I (Fig. 4). However, the degree of branching of RG I continually decreased through the storage period in each of the four cultivars, indicating that other side branches were present.
Our results and those from studies of other fruit (Redgwell et al., 1997
Texture analysis of apple during overripening allowed us to correlate between the physical behavior and physiological age and the biochemical changes in polysaccharide linkage structure. These comparisons reveal that the loss of the highly branched arabinan prestaged the loss of texture in all instances (Fig. 4). Since arabinan loss is almost complete before softening, it is unlikely to be directly responsible but perhaps a prerequisite to permit other wall components to become susceptible to enzymatic modification. Loss of firm texture in apple is strongly correlated with the debranching of RG I (e.g. Figs. 3 and 4). The debranching of RG I is unrelated to the earlier loss of the highly branched arabinans, so both of the major neutral side groups of RG I, arabinan, and galactan have been hydrolyzed at the time of the greatest loss of RG I branch-point residues. Vincken et al. (2003)
The decrease in the highly branched arabinans that prestage the loss of texture may permit RG I-associated HG to be susceptible to enzymatic hydrolysis to effect cell separation. In the tobacco (Nicotiana plumbaginifolia) mutant nolac-H14, RG Is with low levels of associated arabinans were not retained in the cells walls and middle lamella (Iwai et al., 2001
Fruit softening and loss of cell adhesion may involve changes in other minor cell wall components. In vitro cell separation (Fig. 5) and tissue softening (Fig. 6) can be produced by substances or enzymes that modify pectins, but oxidation of phenols is equally effective. Sodium chlorite has been shown to be an effective means to oxidize phenolic substances without appreciable change in the carbohydrate structure of the wall (Carpita, 1984
The presence and role of phenolic compounds in apple cell walls are somewhat controversial. Phenolic compounds are associated with apple pectin (Stevens and Selvendran, 1984
Plant Materials Apples (Malus domestica cv Borkh) were grown at Purdue University Department of Horticulture experimental orchard, West Lafayette, Indiana. Apples were picked at different stages of development and ripening from the tree. Ripe fruit were kept at ambient temperature in darkness during overripening stages. Upon harvest, weights and volumes of individual apples were measured, and the fruit were then peeled, the outer parenchyma cut into small portions, and immediately frozen with liquid nitrogen. Tissue samples were stored at –80°C until all had been collected. Apples of four cultivars, Red Delicious, Gala, Firm Gold, and Gold Rush, were picked at ripe stages from trees grown at the same farm. For each cultivar, the apple collection was divided in two, one was kept at ambient temperature and the other at 4°C, until cell separation had occurred in those at ambient temperature. Two apples from each cultivar and storage condition were harvested weekly and used for the texture analysis. Immediately after the fruit was peeled, the outer cortex was prepared and stored as described above for biochemical analyses performed subsequently.
Every 1 to 2 weeks, two apples of each cultivar and storage condition were harvested for compression and breaking strength assays with a TA-XT2i texture analyzer (Stable Microsystems, distributed by Texture Technologies, Scarsdale, NY). For the fracture force measurements, 9- x 40-mm cylinders of apple cortex were removed from the fruit and placed on a stainless steel support with 2 anvils set 3 cm apart. Force was applied perpendicularly to the apple cylinder with a blunt-edged anvil descending at a creep rate of 0.5 mm s–1. The force to break the cylinder was digitally recorded. Compression upon a cylindrical plug of apple cortex 1.8-cm diameter x 1-cm thick resting on a flat platform was performed on tissues from the same apple used for fracture force measurements. Force was applied to the piece using a round probe, 1 cm in diameter, descending at a rate of 0.5 mm s–1. The force required to compress the apple tissue to a depth of 5 mm was recorded.
Cortex cylinders (6-mm diameter x 5-mm long) or slices (6-mm diameter x 1-mm thick) of cultivar Gold Rush were incubated in 80% (v/v) ethanol at 70°C for 30 min and washed twice with fresh 80% hot ethanol. After rehydration of the tissues, the cylinders were incubated by gentle rocking for up to 24 h at ambient temperature in water, 50 mM CDTA, pH 6.5, pectinase from Aspergillus niger (Sigma, St. Louis) in 100 mM sodium acetate buffer, pH 4.0, and proteinase K in 50 mM Tris[HCl] buffer, pH 7.5.
Other cylinders were incubated with sodium chlorite to selectively oxidize phenolic compounds without altering the polysaccharide composition (Carpita, 1984 After incubation the tissues were washed several times with water. The slices were stained with 0.02% aqueous toluidine blue O for 5 min, then washed with water. Before examination by microscopy, the slices were mounted in water on a glass slide, and the glass coverslip was moved gently left and right two times. The tissue was observed in the light microscope, and the degree of cell separation produced by the different treatments was compared. Microcompression tests were done as described above but using a flat probe 7 mm descending at a creep rate of 0.1 mm s–1. The force required to puncture the apple cylinder (6-mm diameter x 5-mm long) to a depth of 3 mm was recorded.
Frozen portions of the cortex were homogenized in 1% SDS in 100 mM Tris[HCl], pH 7.2, by Polytron (Brinkmann Instruments, Westbury, NY). The cell walls were collected on nylon cloth (Nitex, 47 µm-mesh; Tetko, Depew, NY) to filter out the starch grains and washed sequentially with ethanol and water. The material was then homogenized in acetone and washed with acetone and water. Finally, the material was homogenized in 100 mM sodium chloride and washed with 100 mM sodium chloride and then water. The washes were repeated until no starch was detected upon staining with iodine/iodide solution as observed by brightfield microscopy. Negligible uronic acid containing material was detected in the SDS-soluble extract and subsequent washes of the cell wall material.
The carboxyl groups of uronosyl in the cell walls were activated with 1-cyclohexyl-3-(-2-morpholinyl-4-ethyl) carbodiimide (methyl-p-toluene sulfonate) powder and reduced with NaBD4 to their respective 6,6-didueterio sugars (Kim and Carpita, 1992
Uronosyl-reduced wall materials were suspended in DMSO in sonication bath and after 2 h were per-O-methylated with 2.5 M n-buthyllitium in hexane and methyl iodide according to Gibeaut and Carpita (1991)
We thank Nicholas Rozzi, Department of Food Science, Purdue University, for his assistance in teaching us the operation of the texture analyzer, and Dr. Peter Hirst, Department of Horticulture, Purdue University, for the selection of apple cultivars with varied ripening textures and storage characteristics. This is journal paper Number 17,232 of the Purdue University Agricultural Experiment Station. Received March 28, 2004; returned for revision April 8, 2004; accepted April 8, 2004.
1 This work was supported by a grant from the U.S.-Israel Bi-National Research and Development Fund (BARD) and by the Indiana 21st Century Research and Technology Fund. 
2 Present address: Complex Carbohydrate Research Center, 315 Riverbend Road, University of Georgia, Athens, GA 30602–4712. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.043679. * Corresponding author; e-mail carpita{at}purdue.edu; fax 765–494–0363.
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815[CrossRef][Medline] Aspinall GO, Fanous HK (1984) Structural investigations on the non-starchy polysaccharides of apples. Carbohyd Polym 4: 193–214[CrossRef] Brett CT, Waldron KW (1996) Physiology and Biochemistry of Plant Cell Walls, Ed 2. Chapman and Hall, London Brummel DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47: 311–340[CrossRef][ISI][Medline] Bush MS, Marry M, Huxham IM, Jarvis MC, McCann MC (2001) Developmental regulation of pectic epitopes during potato tuberisation. Planta 213: 869–880[ISI][Medline] Carpita NC (1984) Fractionation of hemicelluloses from maize cell walls with increasing concentrations of alkali. Phytochemistry 23: 1089–1093[CrossRef] Carpita NC, Gibeaut DM (1993) Structural models of primary-cell walls in flowering plants: consistency of molecular structure with the physiological properties of the cell wall during the growth. Plant J 3: 1–30[CrossRef][ISI][Medline] Carpita NC, McCann MC (1996) Some new methods to study plant polyuronic acids and their esters. In R Townsend, A Hotchkiss, eds, Progress in Glycobiology. Marcel Dekker, New York, pp 595–611 Carpita NC, Shea EM (1989) Linkage structure by gas chromatography-mass spectrometry of partially-methylated alditol acetates. In CJ Biermann, GD McGinnis, eds, Analysis of Carbohydrates by GLC and MS. CRC Press, Boca Raton, FL, pp 155–216 Esau K (1977) Fruit. In Anatomy of Seed Plants. John Wiley & Sons, NY
Gibeaut DM, Carpita NC (1991) Tracing the biosynthesis of the cell wall in intact cells and plants. Selective turnover and alteration of cytoplasmic and cell wall polysaccharides of proso millet cells in liquid culture and Zea mays seedlings. Plant Physiol 97: 551–561 Henrissat B, Coutinho PM, Davies GJ (2001) A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol Biol 47: 55–72[CrossRef][ISI][Medline]
Ishii T, Matsunaga T, Hayashi N (2001) Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiol 126: 1698–1705 Iwai H, Ishii T, Satoh S (2001) Absence of arabinan in the side chains of pectin polysaccharides strongly associated with cell walls Nicotiana plumbaginifolia non-organogenic callus with loosely attached constituent cells. Planta 213: 907–915[ISI][Medline] Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7: 153–164
Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci USA 100: 11783–11788
Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1
Kim J-B, Carpita NC (1992) Changes in esterification of the uronic acids groups of cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol 98: 646–653
Kobayashi M, Nakagawa H, Asaka T, Matoh T (1999) Borate-rhamnogalacturonan II bonding reinforced by Ca2+ retains pectic polysaccharides in higher-plant cell walls. Plant Physiol 119: 199–203 Kravtchenko TP, Penci M, Voragen AGJ, Plinik W (1993) Enzymatic and chemical degradation of some industrial pectins. Carbohyd Polym 20: 195–205[CrossRef]
McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (1
McCartney L, Steele-King CG, Jordan E, Knox JP (2003) Cell wall pectic (1
O'Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294: 846–849
O'Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. In vitro conditions for the formation and hydrolysis of the dimer. J Biol Chem 271: 22923–22930 Oomen RJFJ, Doeswijk-Voragen CHL, Bush MS, Vincken J-P, Borkhardt B, van den Broek LAM, Corsar J, Ulvskov P, Voragen AGJ, McCann MC, et al (2002) In muro fragmentation of the rhamnogalacturonan I backbone in potato (Solanum tuberosum L.) results in a reduction and altered location of the galactan and arabinan side-chains and abnormal periderm development. Plant J 30: 403–413[CrossRef][ISI][Medline] Orfila C, Huisman MMH, Willats WGT, van Alebeek GJWM, Schols HA, Seymour GB, Knox JP (2002) Altered cell wall disassembly during ripening of Cnr tomato fruit: implications for cell adhesion and fruit softening. Planta 215: 440–447[CrossRef][ISI][Medline]
Orfila C, Knox JP (2000) Spatial regulation of pectin polysaccharides in relation to pit fields in cell walls of tomato fruit pericarp. Plant Physiol 122: 775–781
Orfila C, Seymour GB, Willats WGT, Huxham IM, Jarvis MC, Dover CJ, Thompson AJ, Knox JP (2001) Altered middle lamella homogalacturonan and disrupted deposition of (1 Perez S, Mazeau K, Hervé du Penhoat C (2000) The three-dimensional structures of the pectin polysaccharides. Plant Physiol Biochem 38: 37–55[CrossRef] Redgwell J, Fisher M, Kendal E, MacRae EA (1997) Galactose loss and fruit ripening: high-molecular-weight arabinogalactans in the pectin polysaccharides of fruit cell walls. Planta 203: 174–181[CrossRef] Renard CMGC, Baron A, Guyot S, Drilleau J-F (2001) Interactions between apple cell walls and native apple polyphenols: quantification and some consequences. Int J Biol Macromol 29: 115–125[Medline]
Rose JKC, Hadfield KA, Labavitch JM, Bennett AB (1998) Temporal sequence of cell wall disassembly in rapidly ripening melon fruit. Plant Physiol 117: 345–361
Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter W-D, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132: 1033–1040 Schols HA, Bakx EJ, Schipper D, Voragen AGJ (1995) A xylogalacturonan subunit present in the modified hairy regions of apple pectin. Carbohydr Res 279: 265–279[CrossRef] Smith CJS, Watson CF, Ray I, Bird CR, Morris PC, Schuch W, Grierson D (1988) Antisense RNA inhibition of polygalacturonase gene-expression in transgenic tomatoes. Nature 334: 724–726[CrossRef] Stevens BJH, Selvendran RR (1984) Structural features of cell wall polymers of the apple. Carbohydr Res 135: 155–166[CrossRef] Tukey HB, Young JO (1942) Gross morphology and histology of developing fruit of the apple. Bot Gaz 104: 3–25[CrossRef]
Vincken JP, Schols HA, Oomen RJFJ, McCann MC, Ulvskov P, Voragen AGJ, Visser RGF (2003) If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol 132: 1781–1789 Watt DK, Brasch DJ, Larsen DS, Melton LD (1999) Isolation, characterisation, and NMR study of xyloglucan from enzymatically depectinised and non-depectinised apple pomace. Carbohyd Polym 39: 165–180 Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47: 9–27[CrossRef][ISI][Medline] Willats WGT, Steele-King CG, Markus SE, Knox JP (1999) Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J 20: 619–628[CrossRef][ISI][Medline] Related articles in Plant Physiol.:
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ABSTRACT
RESULTS
, t-Ara; 
, 3,5-Ara; 
, 5-Ara; 
, t-Gal; 
, 4-Gal; 
, 3,4-Gal. Bars represent variance of two samples. Variance did not extend beyond the symbol in values without bars. Absolute mol% of monosaccharides was determined by quantitative analysis of alditol acetate derivatives.
) and 4°C (
