<i>In muro</i> fragmentation of the rhamnogalacturonan I backbone in potato (<i>Solanum tuberosum</i> L.) results in a reduction and altered location of the galactan and arabinan side‐chains and abnormal periderm development

Oomen, Roelof; Doeswijk-Voragen, Chantal H. L.; Bush, Maxwell S.; Vincken, Jean‐Paul; Borkhardt, Bernhard; Broek, L.A.M. van den; Corsar, Julia; Ulvskov, Peter; Voragen, A.G.J.; McCann, Maureen C.; Visser, Richard G. F.

doi:10.1046/j.1365-313x.2002.01296.x

Cited by 87 publications

(62 citation statements)

References 53 publications

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“…Not only was the number of transformants low but also the level of enzyme expression in the transformed plants was low, indicating a strong selective pressure against plants expressing AnPGII. Similarly, the transformation efficiency of potatoes with the genes encoding rhamnogalacturonan lyase and arabinanase of A. aculeatus has been reported to be very low (Skjot et al, 2001;Oomen et al, 2002). Interestingly in a situation where we did not limit the effects of the enzyme activity by using tissue-specific promoters and/or specific targeting signals, the plant was capable of performing its own control of AnPGII by proteolytically processing and inactivating the enzyme.…”

Section: Discussionmentioning

confidence: 94%

“…Galactanase, rhamnogalacturonan lyase, and arabinanase from Aspergillus aculeatus, which attack RG-I, have been used to transform potatoes (Solanum tuberosum). Plants expressing galactanase displayed no altered phenotype (Oxenboll et al, 2000), while those expressing rhamnogalacturonan lyase had more wrinkled tubers than the wild type (Oomen et al, 2002) and those expressing arabinanase suffered serious developmental disruption and produced no side shoots, flowers, stolons, or tubers (Skjot et al, 2001).…”

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Targeted Modification of Homogalacturonan by Transgenic Expression of a Fungal Polygalacturonase Alters Plant Growth

et al. 2004

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Pectins are a highly complex family of cell wall polysaccharides comprised of homogalacturonan (HGA), rhamnogalacturonan I and rhamnogalacturonan II. We have specifically modified HGA in both tobacco (Nicotiana tabacum) and Arabidopsis by expressing the endopolygalacturonase II of Aspergillus niger (AnPGII). Cell walls of transgenic tobacco plants showed a 25% reduction in GalUA content as compared with the wild type and a reduced content of deesterified HGA as detected by antibody labeling. Neutral sugars remained unchanged apart from a slight increase of Rha, Ara, and Gal. Both transgenic tobacco and Arabidopsis were dwarfed, indicating that unesterified HGA is a critical factor for plant cell growth. The dwarf phenotypes were associated with AnPGII activity as demonstrated by the observation that the mutant phenotype of tobacco was completely reverted by crossing the dwarfed plants with plants expressing PGIP2, a strong inhibitor of AnPGII. The mutant phenotype in Arabidopsis did not appear when transformation was performed with a gene encoding AnPGII inactivated by site directed mutagenesis.Although biochemical events causing structural changes of cell walls are expected to influence plant growth and development (Pilling et al., 2000;Bouton et al., 2002), the degradation and remodeling of cell wall constituents during development appear to be of considerable complexity and far from being fully understood. For example, the remodeling of pectin, which is thought to impact upon processes such as adhesion between cells and plant growth, requires the action of several different enzyme classes (Ridley et al., 2001). The complex role of pectin in the dynamics of cell walls is further indicated by the presence of large families of these pectic enzymes in plant genomes. For example, more than 50 genes encoding putative polygalacturonases (PGs) have been identified in Arabidopsis (Arabidopsis Genome Initiative, 2000).Indications that the pectic polymers homogalacturonan (HGA), rhamnogalacturonan-I (RG-I), and rhamnogalacturonan-II (RG-II) play an important role in plant development have been obtained by analyzing several cell wall mutants, most of which have been obtained by mutagenesis of Arabidopsis. Among these, Arabidopsis emb30 mutants, having a mutation in a gene putatively involved in the secretory pathway, show an abnormal localization and accumulation of pectin in intercellular/interstitial spaces rather than in the corners. Cells of emb30 mutants are larger than those of the wild type and do not adhere well to each other; the seeds are impaired in the control of cell division, expansion, and polarity and do not develop as wild type (Shevell et al., 2000). The Arabidopsis quartet mutants have microspores that fail to separate during pollen development as a result of the persistence of pectin in the pollen mother cell wall (Rhee and Somerville, 1998). The Arabidopsis mur1 mutation, leading to a deficiency in fucosyl residues, affects RG-II, reducing its capacity to dimerize through the formation of boron diest...

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Section: Discussionmentioning

confidence: 94%

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confidence: 99%

Targeted Modification of Homogalacturonan by Transgenic Expression of a Fungal Polygalacturonase Alters Plant Growth

et al. 2004

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“…The altered HG network and reduced cell adhesion observed in the Cnr tomato mutant could be a consequence of disrupted arabinan deposition in this tomato cell wall (Orfila et al, 2001(Orfila et al, , 2002. A role for arabinans in anchoring pectin in the wall was suggested by these authors, but the decreased abundance and altered location of arabinan side chain when RG I was fragmented in muro by a rhamnogalacturonan lyase in transgenic potato plants indicated that cross-linkage between arabinans and other components of the wall is unlikely (Oomen et al, 2002). However, if the arabinans were preventing enzymatic hydrolysis of HG, as we propose here, their absence would produce loss of pectin network integrity without any direct attachment.…”

Section: Discussionmentioning

confidence: 96%

Loss of Highly Branched Arabinans and Debranching of Rhamnogalacturonan I Accompany Loss of Firm Texture and Cell Separation during Prolonged Storage of Apple

2004

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Growth and maturation of the edible cortical cells of apples (Malus domestica Borkh) are accompanied by a selective loss of pectin-associated (1/4)-b-D-galactan from the cell walls, whereas a selective loss of highly branched (1/5)-a-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 (1/5)-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 ripeningassociated 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 rec...

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“…13 Furthermore, it has been shown that 'in muro' fragmentation of the RG1 backbone in Solanum tuberosum results in abnormal development of the periderm. 14 This suggests that these side chains may play at least some role in normal cell attachment and cell development. However, the real problem is that no obvious phenotypic differences between wild type and mutant plants (in which neutral side chains have been modified) have been observed.…”

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confidence: 99%

A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress

Moore

Farrant

Driouich

2008

Plant Signaling & Behavior

122

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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

Cited by 87 publications

References 53 publications

Targeted Modification of Homogalacturonan by Transgenic Expression of a Fungal Polygalacturonase Alters Plant Growth

Targeted Modification of Homogalacturonan by Transgenic Expression of a Fungal Polygalacturonase Alters Plant Growth

Loss of Highly Branched Arabinans and Debranching of Rhamnogalacturonan I Accompany Loss of Firm Texture and Cell Separation during Prolonged Storage of Apple

A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress

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