Xyloglucan Octasaccharide XXLGol Derived from the Seeds of<i>Hymenaea courbaril</i> Acts as a Signaling Molecule1

Vargas-Rechia, Carem Gledes; Reicher, Fany; Sierakowski, Maria Rita; Heyraud, A.; Driguez, Hugues; Liénart, Y.

doi:10.1104/pp.116.3.1013

Cited by 42 publications

(28 citation statements)

References 40 publications

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“…One explanation for these apparently counterintuitive observations is that altering XEH activity directly affects the levels of small xyloglucan oligosaccharides in the apoplast, which may act as signaling molecules affecting growth (York et al, 1984;McDougall and Fry, 1989;Vargas-Rechia et al, 1998;Salamoni et al, 2008). Here, AtXTH31 may be the dominant player in Col-0, as it is significantly up-regulated (Supplemental Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Notably, XET activity also appeared to be slightly reduced in the double knockout, perhaps indicating a compensatory mechanism or secondary effects leading to altered transcript levels of other XTH family members. In the absence of a detailed global analysis, it is tempting to speculate that a reduction in xyloglucan oligosaccharide release from the apoplast may affect a wall-sensing signal mechanism (York et al, 1984;McDougall and Fry, 1989;Vargas-Rechia et al, 1998;Salamoni et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

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Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

et al. 2012

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The molecular basis of primary wall extension endures as one of the central enigmas in plant cell morphogenesis. Classical cell wall models suggest that xyloglucan endo-transglycosylase activity is the primary catalyst (together with expansins) of controlled cell wall loosening through the transient cleavage and religation of xyloglucan-cellulose cross links. The genome of Arabidopsis (Arabidopsis thaliana) contains 33 phylogenetically diverse XYLOGLUCAN ENDO-TRANSGLYCOSYLASE/ HYDROLASE (XTH) gene products, two of which were predicted to be predominant xyloglucan endohydrolases due to clustering into group III-A. Enzyme kinetic analysis of recombinant AtXTH31 confirmed this prediction and indicated that this enzyme had similar catalytic properties to the nasturtium (Tropaeolum majus) xyloglucanase1 responsible for storage xyloglucan hydrolysis during germination. Global analysis of Genevestigator data indicated that AtXTH31 and the paralogous AtXTH32 were abundantly expressed in expanding tissues. Microscopy analysis, utilizing the resorufin b-glycoside of the xyloglucan oligosaccharide XXXG as an in situ probe, indicated significant xyloglucan endohydrolase activity in specific regions of both roots and hypocotyls, in good correlation with transcriptomic data. Moreover, this hydrolytic activity was essentially completely eliminated in AtXTH31/AtXTH32 double knockout lines. However, single and double knockout lines, as well as individual overexpressing lines, of AtXTH31 and AtXTH32 did not demonstrate significant growth or developmental phenotypes. These results suggest that although xyloglucan polysaccharide hydrolysis occurs in parallel with primary wall expansion, morphological effects are subtle or may be compensated by other mechanisms. We hypothesize that there is likely to be an interplay between these xyloglucan endohydrolases and recently discovered apoplastic exo-glycosidases in the hydrolytic modification of matrix xyloglucans.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

et al. 2012

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“…The reported inhibitory effect of the fucose-containing oligosaccharide may result not from a direct interaction with XET but instead from a signal transduction cascade, such as the induction of wall-associated peroxidase (35) and͞or ␣-fucosidase activities (36).…”

Section: Discussionmentioning

confidence: 99%

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.

181

140

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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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“…Biological effects of xyloglucan derivatives are related to the intrinsic physiological function of polymeric xyloglucan in plant cells, comprising the control of extensibility and mechanics of the cell wall and cell expansion. Most research in this field highlights their regulatory activity on cell growth and elongation, which relies in the molecular size, distribution, and levels of substituted xylosyl units with galactosyl and fucosyl residues [63]. It has been observed active xyloglucan oligomers (XGOs) accelerate cell elongation in peeled stem segments of Pisum sativum [64], and in suspension-cultured cells of Nicotiana tabacum, expansion led to cell division [65].…”

Section: Hemicellulose-derived Oligosaccharinsmentioning

confidence: 99%

Plant Cell Wall Polymers: Function, Structure and Biological Activity of Their Derivatives

et al. 2012

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Xyloglucan Octasaccharide XXLGol Derived from the Seeds ofHymenaea courbaril Acts as a Signaling Molecule1

Cited by 42 publications

References 40 publications

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

Group III-AXTHGenes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth

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

Plant Cell Wall Polymers: Function, Structure and Biological Activity of Their Derivatives

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