Xyloglucan Antibodies Inhibit Auxin-Induced Elongation and Cell Wall Loosening of Azuki Bean Epicotyls but Not of Oat Coleoptiles

Hoson, Takayuki; Sone, Yoshitsugu; Misaki, Akira

doi:10.1104/pp.96.2.551

Cited by 62 publications

(22 citation statements)

References 32 publications

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“…In fact, microfibrils seem to be coated with xyloglucan, which is located both on and between microfibrils throughout cell elongation (3). Masking xyloglucans in cell walls should prevent xyloglucan metabolism; in agreement with this prediction, an antibody specific to xyloglucan prevented an auxin-induced decrease in molecular size of xyloglucan and inhibited indole-3-acetic acid (IAA)-induced cell elongation in azuki hypocotyl segments (4). Xyloglucan endotransglycosylase (XET) has been proposed to participate in the dynamic changes of xyloglucan cross-linking (5,6), but there is little direct evidence for this hypothesis.…”

supporting

confidence: 55%

Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments

Takeda

Furuta

Awano

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

184

141

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Xyloglucan is a key polymer in the walls of growing plant cells. Using split pea stem segments and stem segments from which the epidermis had been peeled off, we demonstrate that the integration of xyloglucan mediated by the action of wall-bound xyloglucan endotransglycosylase suppressed cell elongation, whereas that of its fragment oligosaccharide accelerated it. Whole xyloglucan was incorporated into the cell wall and induced the rearrangement of cortical microtubules from transverse to longitudinal; in contrast, the oligosaccharide solubilized xyloglucan from the cell wall and maintained the microtubules in a transverse orientation. This paper proposes that xyloglucan metabolism controls the elongation of plant cells.X yloglucan, which occurs widely in the primary walls of higher plants, possesses a 1,4-␤-glucan backbone with 1,6-␣-xylosyl residues along the backbone. Because the 1,4-␤-glucan backbone can bind specifically to cellulose microfibrils by hydrogen bonds (1), the xyloglucan probably contributes to the rigidity of the cell wall by cross-linking adjacent microfibrils (2). In fact, microfibrils seem to be coated with xyloglucan, which is located both on and between microfibrils throughout cell elongation (3). Masking xyloglucans in cell walls should prevent xyloglucan metabolism; in agreement with this prediction, an antibody specific to xyloglucan prevented an auxin-induced decrease in molecular size of xyloglucan and inhibited indole-3-acetic acid (IAA)-induced cell elongation in azuki hypocotyl segments (4). Xyloglucan endotransglycosylase (XET) has been proposed to participate in the dynamic changes of xyloglucan cross-linking (5, 6), but there is little direct evidence for this hypothesis. The question at issue concerns the structural function of xyloglucan, namely whether xyloglucan contributes to the extensibility of the wall by cross-linking adjacent microfibrils.Fucose-containing xyloglucan oligosaccharides have been shown to inhibit auxin-induced elongation of pea stems (7,8). Their inhibitory activity is approximately maximal at a concentration of 10 Ϫ8 to 10 Ϫ9 M. In the absence of auxin, a high concentration (Ͼ10 Ϫ8 M) of xyloglucan oligosaccharide did not inhibit but slightly promoted cell elongation in pea stem segments (9). Thus, the oligosaccharides may provide either negative or positive feedback control during cell elongation. However, the positive feedback reaction has not been reproducibly observed in pea stems (T.T. and T.H., unpublished results) and also was not observed in maize primary roots (10). In the present communication, we examine whether xyloglucan oligosaccharides control the elongation growth of plant cells.In cylindrical plant organs such as roots or stems, cells expand anisotropically, with the direction of most rapid growth parallel to the long axis of the organ, leading to elongation of the organ. It has been known for many years that the direction of elongation is perpendicular to the direction of net orientation of cellulose microfibrils (11). Therefore, paral...

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supporting

confidence: 55%

Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments

Takeda

Furuta

Awano

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

184

141

View full text Add to dashboard Cite

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“…XG molecules that contain repeats with trisaccharide sidechains (XXFG) appear to be able to both enhance the rate of XG--cellulose association over subunits that possess mono-and disaccharide sidechains (XXXG, XXLG and XLLG) as well as maintaining a more stable association with cellulose. Since cell growth appears to require XGcellulose association and modification (Fry, 1986;Hayashi 1989;Hoson et aL, 1991;McQueen-Mason and Cosgrove 1995;McQueen-Mason et al, 1992), it is appropriate that XG from growing tissue possesses large amounts of subunits that bind cellulose rapidly, as observed for pea epicotyl XG. Seed forms of XG are stored in cotyledons in non-growing tissue and tend to accumulate in a layer between the cellulose-containing part of the cell wall and the plasma membrane (Ruel et al, 1990).…”

Section: Mechanisms Of Xg Binding To Cellulosementioning

confidence: 99%

Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations

1997

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SummaryCross-links between cellulose microfibrils and xyloglucan (XG) molecules play a major role in defining the structural properties of plant cell walls and the regulation of growth and development of dicotyledonous plants. How these cross-links are established and how they are regulated has yet to be determined. In a previous study, preliminary data were presented which suggested that the different sidechains of XG may play a role in controlling cellulose microfibriI-XG interactions. In this study, this question is addressed directly by analyzing to what extent the different sidechains of pea cell wall XG and nasturtium seed storage XG affect their binding to cellulose microfibrils. Of particular importance to this study are the chemical data indicating that pea XG possesses a trisaccharide sidechain, which is not found in nasturtium XG. To this end, conformational dynamic simulations have been used to predict whether oligosaccharides representative of pea and nasturtium XG can adopt a hypothesized cellulosebinding conformation and which of these XGs exhibits a preferential ability to bind cellulose. Extensive analysis of the conformational forms populated during 300 K and high-temperature Monte Carlo simulations established that a planar, sterically accessible, glucan backbone is essential for optimal cellulose-binding. For the trisaccharide sidechain-containing oligosaccharide as found in pea XG, sidechain orientation appeared to regulate the gradual acquisition of this hypothesized cellulose binding conformation. Thus, conformational forms were identified that included the twisted backbone (non-planar) putative solution form of XG, forms in which the trisaccharide sidechain orientation enables increased backbone planarity and steric accessibility, and finally a planar, sterically accessible, backbone. By applying these conformational requirements for cellulose binding, it has been Received 25 May 1996; revised 11 October 1996; accepted 12 November 1996. *For correspondence (fax +1 303 492 7744; e-mail levy@spot.colorado.edu).determined that pea XG possesses a two-to threefold occurrence of the cellulose binding conformation than nasturtium XG. Based on this finding, it was predicted that pea XG would bind to cellulose at a higher rate than nasturtium XG. In vitro binding assays showed that pea XG-avicel binding does indeed occur at a twofold higher rate than nasturtium XG-avicel binding. The enhanced ability of pea cell wall XG over nasturtium seed storage XG to associate with cellulose is consistent with a structural role of the former during epicotyl growth where efficient association with cellulose is a requirement. In contrast, the relatively low ability of nasturtium XG to bind cellulose is consistent with the need to enhance the accessibility of this polymer to glycanases during germination. These findings suggest potential roles for XG sidechain substitution, enabling XG to function in a variety of different biological contexts.

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“…From the same laboratory comes a curious report that implicates another fraction of low molecular mass proteins other than the glucanases (Hatfield and Nevins, 1988). Gugsch and Klambt (1991) proposed that this low molecular mass protein might actually have been the soluble auxin-binding protein reported by Lobler and Klambt (1 985) Hoson et al (1991) were able to inhibit growth in legumes but not grasses with antibodies to the XG nonasaccharide. Resolution of these apparent inconsistencies must await further work.…”

Section: Future Goals and Directionsmentioning

confidence: 99%

Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth

1993

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SummaryAdvances in determination of polymer structure and in preservation of structure for electron microscopy provide the best view to date of how polysaccharides and structural proteins are organized into plant cell walls. The walls that form and partition dividing cells are modified chemically and structurally from the walls expanding to provide a cell with its functional form. In grasses, the chemical structure of the wall differs from that of all other flowering plant species that have been examined. Nevertheless, both types of wall must conform to the same physical laws. Cell expansion occurs via strictly regulated reorientation of each of the wall's components that first permits the wall to stretch in specific directions and then lock into final shape. This review integrates information on the chemical structure of individual polymers with data obtained from new techniques used to probe the arrangement of the polymers within the walls of individual cells. We provide structural models of two distinct types of walls in flowering plants consistent with the physical properties of the wall and its components.

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Xyloglucan Antibodies Inhibit Auxin-Induced Elongation and Cell Wall Loosening of Azuki Bean Epicotyls but Not of Oat Coleoptiles

Cited by 62 publications

References 32 publications

Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments

Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments

Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations

Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth

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