Purification, characterization, and cell wall localization of an α‐fucosidase that inactivates a xyloglucan oligosaccharin

Augur, Christopher; Benhamou, Nicole; Darvill, Alan G.; Albersheim, Peter

doi:10.1046/j.1365-313x.1993.t01-24-00999.x

Cited by 78 publications

(31 citation statements)

References 47 publications

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“…Within such oligosaccharides, the Fuc residue is not strictly required to promote growth but XXFG fragments were the most effective to stimulate growth in pea (Pisum sativum) stems (McDougall and Fry, 1989). Interestingly, XXFG was shown to antagonize the promotive effect of the synthetic auxin 2,4-D on growth of pea stem segments, whereas fragments lacking Fuc were not able to counterbalance the auxin effect (York et al, 1984;McDougall and Fry, 1989;Augur et al, 1993). Based on these observations, it is tempting to hypothesize that, in plants inactivated for ABP1, the inhibition of hypocotyl lengthening partially results from an increase in fucosylated oligosaccharides.…”

Section: Abp1 and Oligosaccharinsmentioning

confidence: 99%

“…A large set of apoplastic glycosidases or trans-glycosidases (b-glucosidases, a-xylosidases, b-galactosidases, and a-fucosidases) act specifically on XyGs. These enzymes modify XyG structure by modulating the length of side chains, which might change their susceptibility to XTH activity (Augur et al, 1993;Iglesias et al, 2006;Franková and Fry, 2011) and/or their cellulose binding properties (Levy et al, 1997). Modifications of XyGcellulose interaction or remodeling of XyG by metabolizing enzymes may modulate cell wall extensibility and thus facilitate cell expansion.…”

Section: Introductionmentioning

confidence: 99%

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AUXIN BINDING PROTEIN1 Links Cell Wall Remodeling, Auxin Signaling, and Cell Expansion in Arabidopsis

et al. 2014

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Cell expansion is an increase in cell size and thus plays an essential role in plant growth and development. Phytohormones and the primary plant cell wall play major roles in the complex process of cell expansion. In shoot tissues, cell expansion requires the auxin receptor AUXIN BINDING PROTEIN1 (ABP1), but the mechanism by which ABP1 affects expansion remains unknown. We analyzed the effect of functional inactivation of ABP1 on transcriptomic changes in dark-grown hypocotyls and investigated the consequences of gene expression on cell wall composition and cell expansion. Molecular and genetic evidence indicates that ABP1 affects the expression of a broad range of cell wall-related genes, especially cell wall remodeling genes, mainly via an SCF TIR/AFB -dependent pathway. ABP1 also functions in the modulation of hemicellulose xyloglucan structure. Furthermore, fucosidase-mediated defucosylation of xyloglucan, but not biosynthesis of nonfucosylated xyloglucan, rescued dark-grown hypocotyl lengthening of ABP1 knockdown seedlings. In muro remodeling of xyloglucan side chains via an ABP1-dependent pathway appears to be of critical importance for temporal and spatial control of cell expansion. INTRODUCTIONThe essential protein AUXIN BINDING PROTEIN1 (ABP1) functions in the control of growth and development throughout plant life. Initially identified by its capacity to bind the phytohormone auxin, ABP1 was first shown to affect plasma membrane hyperpolarization via the modulation of ion fluxes across the membrane (Thiel et al., 1993;Barbier-Brygoo et al., 1996;Leblanc et al., 1999aLeblanc et al., , 1999b. These rapid ionic changes indicate a possible involvement of ABP1 in the control of cell expansion, at least in shoot tissues, thus providing preliminary molecular evidence supporting the acid growth theory. This theory states that auxin promotes the excretion of protons at the apoplast resulting in cell wall loosening and increased growth rate (Rayle and Cleland, 1992). Binding of auxin to ABP1 and increased amount of ABP1 at the plasma membrane promote protoplast swelling and enhance expansion of leaf cells (Jones et al., 1998;Steffens et al., 2001;Christian et al., 2006). Conversely, the functional inactivation of ABP1 severely impairs cell expansion in shoot tissues irrespective of their DNA content (Braun et al., 2008;Xu et al., 2010) but does not affect root cell elongation (Tromas et al., 2009). The effect of ABP1 on cell expansion varies in a cell-or tissue-dependent manner. Recent data indicate that ABP1 acts both constitutively and in response to auxin (Robert et al., 2010;Tromas et al., 2013). The mechanism by which ABP1 controls cell expansion remains poorly understood. In shoot tissues, it remains unclear whether the contribution of ABP1 to cell expansion relies solely on nongenomic responses or acts also via the regulation of gene expression. ABP1 was reported to affect expression of various genes in response to auxin, but little is known on the broader effects of ABP1 on gene expression (Braun et al.,...

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Section: Abp1 and Oligosaccharinsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

AUXIN BINDING PROTEIN1 Links Cell Wall Remodeling, Auxin Signaling, and Cell Expansion in Arabidopsis

et al. 2014

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“…a-L-Fucosidase hydrolyzes a-L-fucosidic linkages (Augur et al, 1993;Torre et al, 2002). However, little is known about the in vivo roles of b-D-fucosidase and b-D-fucose.…”

Section: Pyk10 Exhibits Both B-d-glucosidase and B-d-fucosidase Activmentioning

confidence: 99%

NAI1 Gene Encodes a Basic-Helix-Loop-Helix–Type Putative Transcription Factor That Regulates the Formation of an Endoplasmic Reticulum–Derived Structure, the ER Body

et al. 2004

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Plant cells develop various types of endoplasmic reticulum (ER)-derived structures with specific functions. ER body, an ERderived compartment in Arabidopsis thaliana, is a spindle-shaped structure. The NAI1 gene regulates the development of ER bodies because mutation of NAI1 abolishes the formation of ER bodies. To better understand the role of NAI1, we cloned the NAI1 gene using a positional cloning strategy. The nai1-1 mutant had a single nucleotide change at an intron acceptor site of At2g22770 (NAI1 gene). Because of this mutation, aberrant splicing of NAI1 mRNA occurs in the nai1-1 mutant. NAI1 encodes a transcription factor that has a basic-helix-loop-helix (bHLH) domain. Transient expression of NAI1 induced ER bodies in the nai1-1 mutant. Two-dimensional electrophoresis and RT-PCR analyses showed that a putative lectin was depressed at both the mRNA and protein levels in nai1 mutants, as was a b-glucosidase (PYK10). Our results provide direct evidence that a bHLH protein plays a role in the formation of ER bodies.

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“…Isolation and Sequencing of Peptides from ␣-L-Fucosidase-The pea stem ␣-L-fucosidase was purified as described (5). Homogeneous ␣-Lfucosidase was used to obtain its amino acid composition and the sequences of four peptides.…”

Section: Methodsmentioning

confidence: 99%

“…This hypothesis led to the demonstration that pea stems have a developmentally regulated ␣-L-fucosidase with the ability to cleave the fucosyl residue of XG oligosaccharides. Indeed, the ␣-L-fucosidase, which was shown to reside in the primary cell walls of pea stems, has been purified to homogeneity (5).…”

Section: Xyloglucan (Xg)mentioning

confidence: 99%

Molecular Cloning and Pattern of Expression of an α-L-Fucosidase Gene from Pea Seedlings

Augur¹,

Stiefel

Darvill

et al. 1995

Journal of Biological Chemistry

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␣-L-Fucosidase is a cell wall protein purified from pea (Pisum sativum) epicotyls. The ␣-L-fucosidase hydrolyzes terminal fucosyl residues from oligosaccharides of plant cell wall xyloglucan. ␣-L-Fucosidase may be an important factor in plant growth regulation, as it inactivates fucose-containing xyloglucan oligosaccharides that inhibit growth of pea stem segments. The amino acid sequences of the NH 2 -terminal region and one internal peptide were used to design redundant oligonucleotides that were utilized as primers in a polymerase chain reaction (PCR) with cDNA, generated from pea mRNA, as the template. A specific PCR amplification product containing 357 base pairs was isolated, cloned, and sequenced. The deduced amino acid sequence included the two peptides used to design the primers for PCR plus two other peptides obtained by proteinase digestion of ␣-L-fucosidase. No sequence homology to other ␣-L-fucosidases was apparent, although the NH 2 -terminal region is strongly homologous to Kunitz-type trypsin inhibitors. cDNA and genomic copies were isolated and sequenced. In pea, the gene is present in two or three copies. Its mRNA is present in roots, leaves, and elongating shoots. The spatial pattern of expression of the ␣-L-fucosidase was determined by in situ hybridization. Xyloglucan (XG)1 is a hemicellulosic polysaccharide present in the primary cell walls of all of the higher plants that have been examined. XG forms strong noncovalent bonds to cellulose microfibrils and is believed to strengthen the cell walls by cross-linking the microfibrils (1). XG appears to have a regulatory as well as a structural role, as there is evidence that XG oligosaccharides regulate the rate of plant cell growth (2-4). Indeed, fucosylated subunits of XG inhibit auxin-stimulated growth in pea stem segments (4 -7). These oligosaccharins (oligosaccharides with biological regulatory properties) have relatively strict structural requirements for activity, including a critical terminal fucosyl residue. Hydrolysis of the ␣-L-fucosidic bonds abolishes the growth-inhibiting activity of the XG oligosaccharides. Thus, we hypothesized that plants have an ␣-Lfucosidase that participates in the regulation of plant growth by controlling the concentration of fucosylated XG oligosaccharides. This hypothesis led to the demonstration that pea stems have a developmentally regulated ␣-L-fucosidase with the ability to cleave the fucosyl residue of XG oligosaccharides. Indeed, the ␣-L-fucosidase, which was shown to reside in the primary cell walls of pea stems, has been purified to homogeneity (5).cDNAs encoding ␣-L-fucosidases have previously been isolated from human (8, 9) and rat (10) livers. The human and rat liver ␣-L-fucosidases have subunit molecular masses of approximately 50,100 and 55,000 Da, respectively. Both of these ␣-Lfucosidases hydrolyze artificial substrates such as p-nitrophenyl-␣-L-fucoside and 4-methylumbelliferyl fucoside. Both of these fucosidases have broad aglycon specificities such that they hydrolyze ␣-1,2-, ␣-1,3-, ␣-1,...

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Purification, characterization, and cell wall localization of an α‐fucosidase that inactivates a xyloglucan oligosaccharin

Cited by 78 publications

References 47 publications

AUXIN BINDING PROTEIN1 Links Cell Wall Remodeling, Auxin Signaling, and Cell Expansion in Arabidopsis

AUXIN BINDING PROTEIN1 Links Cell Wall Remodeling, Auxin Signaling, and Cell Expansion in Arabidopsis

NAI1 Gene Encodes a Basic-Helix-Loop-Helix–Type Putative Transcription Factor That Regulates the Formation of an Endoplasmic Reticulum–Derived Structure, the ER Body

Molecular Cloning and Pattern of Expression of an α-L-Fucosidase Gene from Pea Seedlings

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