The Identification of Two Arabinosyltransferases from Tomato Reveals Functional Equivalency of Xyloglucan Side Chain Substituents

Schultink, Alex; Cheng, Kun; Park, Yong Bum; Cosgrove, Daniel J.; Pauly, Markus

doi:10.1104/pp.113.221788

Cited by 47 publications

(91 citation statements)

References 53 publications

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“…Such results are consistent with previous studies suggesting that the F side chain Gal accounts for the bulk of the O-acetylated glycoses in Arabidopsis leaf XyG (Pauly et al, 2001;Perrin et al, 2003). Our NMR data indicate that mur3-1 and mur3-2 XyGs contain approximately 7% and 14%, respectively, of the F side chain present in wild-type plants (Supplemental Table S1) and are consistent with the results of recent studies indicating that small amounts of the F side chain are present in the xyloglucan isolated from the mur3-1 mutant (Jensen et al, 2012;Schultink et al, 2013;Vinueza et al, 2013).…”

supporting

confidence: 91%

“…Arabidopsis fut1, xlt2, and xxt1 to xxt5 mutants that form structurally abnormal XyG (Vanzin et al, 2002;Madson et al, 2003;Perrin et al, 2003;Peña et al, 2004;Jensen et al, 2012;Schultink et al, 2013) or that have reduced Vuttipongchaikij et al, 2012;Zabotina et al, 2012) or no discernible amounts of XyG have no severe developmental or growth phenotypes. This has led plant scientists to question the biological role of XyG in wall assembly and architecture as well as its function in plant growth and development Cosgrove, 2012a, 2012b).…”

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confidence: 99%

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Galactose-Depleted Xyloglucan Is Dysfunctional and Leads to Dwarfism in Arabidopsis

Peña²,

et al. 2015

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Xyloglucan is a polysaccharide that has important roles in the formation and function of the walls that surround growing land plant cells. Many of these plants synthesize xyloglucan that contains galactose in two different side chains (L and F), which exist in distinct molecular environments. However, little is known about the contribution of these side chains to xyloglucan function. Here, we show that Arabidopsis (Arabidopsis thaliana) mutants devoid of the F side chain galactosyltransferase MURUS3 (MUR3) form xyloglucan that lacks F side chains and contains much less galactosylated xylose than its wild-type counterpart. The galactose-depleted xyloglucan is dysfunctional, as it leads to mutants that are dwarfed with curled rosette leaves, short petioles, and short inflorescence stems. Moreover, cell wall matrix polysaccharides, including xyloglucan and pectin, are not properly secreted and instead accumulate within intracellular aggregates. Near-normal growth is restored by generating mur3 mutants that produce no detectable amounts of xyloglucan. Thus, cellular processes are affected more by the presence of the dysfunctional xyloglucan than by eliminating xyloglucan altogether. To identify structural features responsible for xyloglucan dysfunction, xyloglucan structure was modified in situ by generating mur3 mutants that lack specific xyloglucan xylosyltransferases (XXTs) or that overexpress the XYLOGLUCAN L-SIDE CHAIN GALACTOSYLTRANSFERASE2 (XLT2) gene. Normal growth was restored in the mur3-3 mutant overexpressing XLT2 and in mur3-3 xxt double mutants when the dysfunctional xyloglucan was modified by doubling the amounts of galactosylated side chains. Our study assigns a role for galactosylation in normal xyloglucan function and demonstrates that altering xyloglucan side chain structure disturbs diverse cellular and physiological processes.

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supporting

confidence: 91%

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confidence: 99%

Galactose-Depleted Xyloglucan Is Dysfunctional and Leads to Dwarfism in Arabidopsis

Peña²,

et al. 2015

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“…Previous studies showed that overexpressing Eucalyptus grandis and tomato MUR3 in the Arabidopsis mur3 and xlt2 mur3.1 mutants also led to XyG overgalactosylation but not complete galactosylation. However, none of these plants were reported to exhibit a dwarfed phenotype (Lopes et al, 2010;Schultink et al, 2013). It, thus, seems that proper functionality of XyG is not retained when XyG galactosylation is below or above a certain threshold, which was found in the mur3 xlt2 double-mutant and the OsMUR3 overexpression lines or mur3-3 knockout plants, respectively.…”

Section: The Rice Genome Contains the Biosynthetic Genes To Generate mentioning

confidence: 97%

“…These data indicate that Os06g12870, termed OsAXY4, exhibits XyG O-acetyltransferase activity but is not functionally equivalent to AtAXY4. The Arabidopsis double-mutant xlt2 mur3.1 contains an XyG that consists predominantly of XXXG (Jensen et al, 2012;Schultink et al, 2013). Expression of the Arabidopsis MUR3 homolog, Os03g05110, in this double mutant resulted in the generation of additional XyG oligosaccharides consistent by mass and retention time with XXLG and XXFG as well as their O-acetylated forms (Supplemental Figs.…”

Section: Impact Of Rice Candidate Genes On Xyg Structures In Arabidopsismentioning

confidence: 99%

The Presence of Fucogalactoxyloglucan and Its Synthesis in Rice Indicates Conserved Functional Importance in Plants

2015

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The predominant structure of the hemicellulose xyloglucan (XyG) found in the cell walls of dicots is a fucogalactoXyG with an XXXG core motif, whereas in the Poaceae (grasses and cereals), the structure of XyG is less xylosylated (XXGG n core motif) and lacks fucosyl residues. However, specialized tissues of rice (Oryza sativa) also contain fucogalactoXyG. Orthologous genes of the fucogalactoXyG biosynthetic machinery of Arabidopsis (Arabidopsis thaliana) are present in the rice genome. Expression of these rice genes, including fucosyl-, galactosyl-, and acetyltransferases, in the corresponding Arabidopsis mutants confirmed their activity and substrate specificity, indicating that plants in the Poaceae family have the ability to synthesize fucogalactoXyG in vivo. The data presented here provide support for a functional conservation of XyG structure in higher plants.

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“…Ara is also found in xyloglucans of some plant species (9). The XXGG-type xyloglucan found in Solanaceous species is characterized by branches extended with Ara instead of D-galactose (Gal) (10). Ara residues are also critical for signaling processes because mature signaling peptides such as CLAVATA3 require posttranslational arabinosylation in the Golgi apparatus to be biologically active and bind to their receptors (11).…”

mentioning

confidence: 99%

The elaborate route for UDP-arabinose delivery into the Golgi of plants

Rautengarten

Birdseye

Pattathil

et al. 2017

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

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In plants, L-arabinose (Ara) is a key component of cell wall polymers, glycoproteins, as well as flavonoids, and signaling peptides. Whereas the majority of Ara found in plant glycans occurs as a furanose ring (Araf), the activated precursor has a pyranose ring configuration (UDP-Arap). The biosynthesis of UDP-Arap mainly occurs via the epimerization of UDP-xylose (UDP-Xyl) in the Golgi lumen. Given that the predominant Ara form found in plants is Araf, UDP-Arap must exit the Golgi to be interconverted into UDP-Araf by UDP-Ara mutases that are located outside on the cytosolic surface of the Golgi. Subsequently, UDP-Araf must be transported back into the lumen. This step is vital because glycosyltransferases, the enzymes mediating the glycosylation reactions, are located within the Golgi lumen, and UDP-Arap, synthesized within the Golgi, is not their preferred substrate. Thus, the transport of UDP-Araf into the Golgi is a prerequisite. Although this step is critical for cell wall biosynthesis and the glycosylation of proteins and signaling peptides, the identification of these transporters has remained elusive. In this study, we present data demonstrating the identification and characterization of a family of Golgi-localized UDP-Araf transporters in Arabidopsis. The application of a proteoliposome-based transport assay revealed that four members of the nucleotide sugar transporter (NST) family can efficiently transport UDP-Araf in vitro. Subsequent analysis of mutant lines affected in the function of these NSTs confirmed their role as UDP-Araf transporters in vivo.

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The Identification of Two Arabinosyltransferases from Tomato Reveals Functional Equivalency of Xyloglucan Side Chain Substituents

Cited by 47 publications

References 53 publications

Galactose-Depleted Xyloglucan Is Dysfunctional and Leads to Dwarfism in Arabidopsis

Galactose-Depleted Xyloglucan Is Dysfunctional and Leads to Dwarfism in Arabidopsis

The Presence of Fucogalactoxyloglucan and Its Synthesis in Rice Indicates Conserved Functional Importance in Plants

The elaborate route for UDP-arabinose delivery into the Golgi of plants

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