Skip to main content
SpringerLink
Log in

Xyloglucan exoglycosidases in the monocot model Brachypodium distachyon and the conservation of xyloglucan disassembly in angiosperms

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

Brachypodium distachyon has a full set of exoglycosidases active on xyloglucan, including α-xylosidase, β-galactosidase, soluble and membrane-bound β-glucosidases and two α-fucosidases. However, unlike in Arabidopsis, both fucosidases are likely cytosolic.

Abstract

Xyloglucan is present in primary walls of all angiosperms. While in most groups it regulates cell wall extension, in Poaceae its role is still unclear. Five exoglycosidases participate in xyloglucan hydrolysis in Arabidopsis: α-xylosidase, β-galactosidase, α-fucosidase, soluble β-glucosidase and GPI-anchored β-glucosidase. Mutants in the corresponding genes show alterations in xyloglucan composition. In this work putative orthologs in the model grass Brachypodium distachyon were tested for their ability to complement Arabidopsis mutants. Xylosidase and galactosidase mutants were complemented, respectively, by BdXYL1 (Bd2g02070) and BdBGAL1 (Bd2g56607). BdBGAL1, unlike other xyloglucan β-galactosidases, is able to remove both galactoses from XLLG oligosaccharides. In addition, soluble β-glucosidase BdBGLC1 (Bd1g08550) complemented a glucosidase mutant. Closely related BdBGLC2 (Bd2g51280), which has a putative GPI-anchor sequence, was found associated with the plasma membrane and only a truncated version without GPI-anchor complemented the mutant, proving that Brachypodium also has soluble and membrane-bound xyloglucan glucosidases. Both BdXFUC1 (Bd3g25226) and BdXFUC2 (Bd1g28366) can hydrolyze fucose from xyloglucan oligosaccharides but were unable to complement a fucosidase mutant. Fluorescent protein fusions of BdXFUC1 localized to the cytosol and both proteins lack a signal peptide. Signal peptides appear to have evolved only in some eudicot lineages of this family, like the one leading to Arabidopsis. These results could be explained if cytosolic xyloglucan α-fucosidases are the ancestral state in angiosperms, with fucosylated oligosaccharides transported across the plasma membrane.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Brennan M, Harris PJ (2011) Distribution of fucosylated xyloglucans among the walls of different cell types in monocotyledons determined by immunofluorescence microscopy. Mol Plant 4:144–156

    Article  CAS  PubMed  Google Scholar 

  • Claverie J, Balacey S, Lemaître-Guillier C, Brulé D, Chiltz A, Granet L, Noirot E, Daire X, Darblade B, Héloir MC, Poinssot B (2018) The cell wall-derived xyloglucan is a new DAMP triggering plant immunity in Vitis vinifera and Arabidopsis thaliana. Front Plant Sci 9:1725

    Article  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ (2018) Diffuse growth of plant cell walls. Plant Physiol 176:16–27

    Article  CAS  PubMed  Google Scholar 

  • Crombie HJ, Chengappa S, Hellyer A, Reid JSG (1998) A xyloglucan oligosaccharide-active, transglycosylating-d-glucosidase from the cotyledons of nasturtium (Tropaeolum majus L.) seedlings—purification, properties and characterization of a cDNA clone. Plant J 15:27–38

    Article  CAS  PubMed  Google Scholar 

  • Crombie HJ, Chengappa S, Jarman C, Sidebottom C, Reid JS (2002) Molecular characterisation of a xyloglucan oligosaccharide-acting α-d-xylosidase from nasturtium (Tropaeolum majus L.) cotyledons that resembles plant ‘apoplastic’ α-d-glucosidases. Planta 214:406–413

    Article  CAS  PubMed  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dardelle F, Le Mauff F, Lehner A, Loutelier-Bourhis C, Bardor M, Rihouey C et al (2015) Pollen tube cell walls of wild and domesticated tomatoes contain arabinosylated and fucosylated xyloglucan. Ann Bot 115:55–66

    Article  CAS  PubMed  Google Scholar 

  • de Alcantara PHN, Dietrich SMC, Buckeridge MS (1999) Xyloglucan mobilisation and purification of a (XLLG/XLXG) specific β-galactosidase from cotyledons of Copaifera langsdorffii. Plant Physiol Biochem 37:653–663

    Article  Google Scholar 

  • de Alcantara PHN, Martim L, Silva CO, Dietrich SMC, Buckeridge MS (2006) Purification of a β-galactosidase from cotyledons of Hymenaea courbaril L. (Leguminosae). Enzyme properties and biological function. Plant Physiol Biochem 44:619–627

    Article  CAS  PubMed  Google Scholar 

  • Dick-Pérez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, Hong M (2011) Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50:989–1000

    Article  CAS  PubMed  Google Scholar 

  • Edwards M, Bowman YJ, Dea IC, Reid JS (1988) A β-d-galactosidase from nasturtium (Tropaeolum majus L.) cotyledons. Purification, properties, and demonstration that xyloglucan is the natural substrate. J Biol Chem 263:4333–4337

    CAS  PubMed  Google Scholar 

  • Eklof JM, Brumer H (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol 153:456–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fry SC (1994) Oligosaccharins as plant growth regulators. Biochem Soc Symp 60:5–14

    CAS  PubMed  Google Scholar 

  • Galloway AF, Pedersen MJ, Merry B, Marcus SE, Blacker J, Benning LG et al (2017) Xyloglucan is released by plants and promotes soil particle aggregation. New Phytol 217:1128–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738

    Article  CAS  PubMed  Google Scholar 

  • Günl M, Pauly M (2011) AXY3 encodes a α-xylosidase that impacts the structure and accessibility of the hemicellulose xyloglucan in Arabidopsis plant cell walls. Planta 233:707–719

    Article  CAS  PubMed  Google Scholar 

  • Günl M, Neumetzler L, Kraemer F, de Souza A, Schultink A, Pena M et al (2011) AXY8 encodes an α-fucosidase, underscoring the importance of apoplastic metabolism on the fine structure of Arabidopsis cell wall polysaccharides. Plant Cell 23:4025–4040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi T, Takeda T (1994) Compositional analysis of the oligosaccharide units of xyloglucans from suspension-cultured poplar cells. Biosci Biotechnol Biochem 58:1707–1708

    Article  CAS  PubMed  Google Scholar 

  • Hoffman M, Jia Z, Pena MJ, Cash M, Harper A, Blackburn AR et al (2005) Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae. Carbohydr Res 340:1826–1840

    Article  CAS  PubMed  Google Scholar 

  • Hrmova M, Harvey AJ, Wang J, Shirley NJ, Jones GP, Stone B et al (1996) Barley β-d-glucan exohydrolases with β-d-glucosidase activity. Purification, characterization, and determination of primary structure from a cDNA clone. J Biol Chem 271:5277–5286

    Article  CAS  PubMed  Google Scholar 

  • Hsieh YSY, Harris PJ (2009) Xyloglucans of monocotyledons have diverse structures. Mol Plant 2:943–965

    Article  CAS  PubMed  Google Scholar 

  • Iglesias N, Abelenda JA, Rodino M, Sampedro J, Revilla G, Zarra I (2006) Apoplastic glycosidases active against xyloglucan oligosaccharides of Arabidopsis thaliana. Plant Cell Physiol 47:55–63

    Article  CAS  PubMed  Google Scholar 

  • Ishimizu T, Hashimoto C, Takeda R, Fujii K, Hase S (2007) A novel α1,2-l-fucosidase acting on xyloglucan oligosaccharides is associated with endo-β-mannosidase. J Biochem 142:721–729

    Article  CAS  PubMed  Google Scholar 

  • Kaewthai N, Gendre D, Eklöf JM, Ibatullin FM, Ezcurra I, Bhalerao R et al (2013) Group III-A XTH genes of Arabidopsis thaliana encode predominant xyloglucan endo-hydrolases that are dispensable for normal growth. Plant Physiol 161:440–454

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Lampropoulos A, Sutikovic Z, Wenzl C, Maegele I, Lohmann JU, Forner J (2013) GreenGate—a novel, versatile, and efficient cloning system for plant transgenesis. PLoS ONE 8:e83043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lampugnani ER, Moller IE, Cassin A, Jones DF, Koh PL, Ratnayake S et al (2013) In vitro grown pollen tubes of Nicotiana alata actively synthesise a fucosylated xyloglucan. PLoS ONE 8:e77140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Léonard R, Pabst M, Bondili JS, Chambat G, Veit C, Strasser R et al (2008) Identification of an Arabidopsis gene encoding a GH95 α1,2-fucosidase active on xyloglucan oligo- and polysaccharides. Phytochemistry 69:1983–1988

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Paulitz J, Pauly M (2015) The presence of fucogalactoxyloglucan and its synthesis in rice indicates conserved functional importance in plants. Plant Physiol 168:549–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Hsia M, Dama M, Vogel J, Pauly M (2016) A xyloglucan backbone 6-O-acetyltransferase from Brachypodium distachyon modulates xyloglucan xylosylation. Mol Plant 9:615–617

    Article  CAS  PubMed  Google Scholar 

  • McDougall GJ, Fry SC (1989) Anti-auxin activity of xyloglucan oligosaccharides: the role of groups other than the terminal α-l-fucose residue. J Exp Bot 40:233–238

    Article  CAS  Google Scholar 

  • Nakai H, Tanizawa S, Ito T, Kamiya K, Kim YM, Yamamoto T et al (2007) Function-unknown glycoside hydrolase family 31 proteins, mRNAs of which were expressed in rice ripening and germinating stages, are α-glucosidase and α-xylosidase. J Biochem 142:491–500

    Article  CAS  PubMed  Google Scholar 

  • Park YB, Cosgrove DJ (2012) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 158:465–475

    Article  CAS  PubMed  Google Scholar 

  • Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Keegstra K (2016) Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu Rev Plant Biol 67:235–259

    Article  CAS  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785

    Article  CAS  PubMed  Google Scholar 

  • Rahman M, Fujishige M, Maeda M, Kimura Y (2016) Rice α-fucosidase active against plant complex type N-glycans containing Lewis a epitope: purification and characterization. Biosci Biotechnol Biochem 80:291–294

    Article  CAS  PubMed  Google Scholar 

  • Rui Y, Anderson CT (2016) Functional analysis of cellulose and xyloglucan in the walls of stomatal guard cells of Arabidopsis. Plant Physiol 170:1398–1419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saffer AM (2018) Expanding roles for pectins in plant development. J Integr Plant Biol 60:910–923

    Article  CAS  PubMed  Google Scholar 

  • Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7(7):682–693

    Article  CAS  PubMed  Google Scholar 

  • Sampedro J, Pardo B, Gianzo C, Guitian E, Revilla G, Zarra I (2010) Lack of α-xylosidase activity in Arabidopsis alters xyloglucan composition and results in growth defects. Plant Physiol 154:1105–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampedro J, Gianzo C, Iglesias N, Guitián E, Revilla G, Zarra I (2012) AtBGAL10 is the main xyloglucan β-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158:1146–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampedro J, Guttman M, Li LC, Cosgrove DJ (2015) Evolutionary divergence of β-expansin structure and function in grasses parallels emergence of distinctive primary cell wall traits. Plant J 81:108–120

    Article  CAS  PubMed  Google Scholar 

  • Sampedro J, Valdivia ER, Fraga P, Iglesias N, Revilla G, Zarra I (2017) Soluble and membrane-bound β-glucosidases are involved in trimming the xyloglucan backbone. Plant Physiol 173:1017–1030

    Article  CAS  PubMed  Google Scholar 

  • Scholthof KB, Irigoyen S, Catalan P, Mandadi K (2018) Brachypodium: a monocot grass model system for plant biology. Plant Cell 30:1694

    Article  CAS  Google Scholar 

  • Schultink A, Liu L, Zhu L, Pauly M (2014) Structural diversity and function of xyloglucan sidechain substituents. Plants 3:526–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Sechet J, Frey A, Effroy-Cuzzi D, Berger A, Perreau F, Cueff G et al (2016) Xyloglucan metabolism differentially impacts the cell wall characteristics of the endosperm and embryo during Arabidopsis seed germination. Plant Physiol 170:1367–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeyama T, Watanabe A, Tokuchi K, Toh S, Sakurai N, Shibuya N et al (2016) α-Xylosidase plays essential roles in xyloglucan remodelling, maintenance of cell wall integrity, and seed germination in Arabidopsis thaliana. J Exp Bot 67:5615–5629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinohara N, Sunagawa N, Tamura S, Yokoyama R, Ueda M, Igarashi K et al (2017) The plant cell-wall enzyme AtXTH3 catalyses covalent cross-linking between cellulose and cello-oligosaccharide. Sci Rep 7:46099

    Article  PubMed  PubMed Central  Google Scholar 

  • Takahashi D, Kawamura Y, Uemura M (2016) Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. J Exp Bot 67:5203–5215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanthanuch W, Chantarangsee M, Maneesan J, Ketudat-Cairns J (2008) Genomic and expression analysis of glycosyl hydrolase family 35 genes from rice (Oryza sativa L.). BMC Plant Biol. 8:84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomson JG, Cook M, Guttman M, Smith J, Thilmony R (2011) Novel sul I binary vectors enable an inexpensive foliar selection method in Arabidopsis. BMC Res Notes 4:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan JX, Zhu XF, Wang YQ, Liu LY, Zhang BC, Li GX et al (2018) Xyloglucan fucosylation modulates Arabidopsis cell wall hemicellulose aluminium binding capacity. Sci Rep 8:428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang T, Park YB, Cosgrove DJ, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis primary cell walls: evidence from solid-state nuclear magnetic resonance. Plant Physiol 168:871–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang T, Cheng Y, Tabuchi A, Cosgrove DJ, Hong M (2016) The target of β-expansin EXPB1 in maize cell walls from binding and solid-state NMR studies. Plant Physiol 172:2107–2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao C, Zhang T, Zheng Y, Cosgrove DJ, Anderson CT (2015) Xyloglucan deficiency disrupts microtubule stability and cellulose biosynthesis in Arabidopsis, altering cell growth and morphogenesis. Plant Physiol 170:234–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeleny R, Leonard R, Dorfner G, Dalik T, Kolarich D, Altmann F (2006) Molecular cloning and characterization of a plant α1,3/4-fucosidase based on sequence tags from almond fucosidase I. Phytochemistry 67:641–648

    Article  CAS  PubMed  Google Scholar 

  • Ziaur Rahman M, Maeda M, Itano S, Hossain M, Ishimizu T, Kimura Y (2017) Molecular characterization of tomato α1,3/4-fucosidase, a member of glycosyl hydrolase family 29 involved in the degradation of plant complex type N-glycans. J Biochem 161:421–432

    PubMed  Google Scholar 

Download references

Funding

This work was supported by the Ministerio de Economía y Competividad [grant no. BIO2012-40032-C03-01]; and Xunta de Galicia [Grant Nos. GPC2013-044, ED431B 2016/021].

Author information

Authors and Affiliations

  1. Dpto. Biología Funcional, Facultad de Biología, Universidade de Santiago, 15782, Santiago de Compostela, Spain

    Diego Rubianes, Elene R. Valdivia, Gloria Revilla, Ignacio Zarra & Javier Sampedro

Authors
  1. Diego Rubianes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elene R. Valdivia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gloria Revilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ignacio Zarra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Javier Sampedro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The project was designed and conceived by JS and DR. Experiments were performed mostly by DR, with contributions by JS and ERV. DR, JS, IZ and GR analyzed the data. JS wrote the paper. All authors have revised and approved the final version of this manuscript.

Corresponding author

Correspondence to Javier Sampedro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1397 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rubianes, D., Valdivia, E.R., Revilla, G. et al. Xyloglucan exoglycosidases in the monocot model Brachypodium distachyon and the conservation of xyloglucan disassembly in angiosperms. Plant Mol Biol 100, 495–509 (2019). https://doi.org/10.1007/s11103-019-00875-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00875-1

Keywords

Search

Navigation