Skip to main content
SpringerLink
Log in

Structural diversity of xylans in the cell walls of monocots

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Xylans in the cell walls of monocots are structurally diverse. Arabinofuranose-containing glucuronoxylans are characteristic of commelinids. However, other structural features are not correlated with the major transitions in monocot evolution.

Most studies of xylan structure in monocot cell walls have emphasized members of the Poaceae (grasses). Thus, there is a paucity of information regarding xylan structure in other commelinid and in non-commelinid monocot walls. Here, we describe the major structural features of the xylans produced by plants selected from ten of the twelve monocot orders. Glucuronoxylans comparable to eudicot secondary wall glucuronoxylans are abundant in non-commelinid walls. However, the α-d-glucuronic acid/4-O-methyl-α-d-glucuronic acid is often substituted at O-2 by an α-l-arabinopyranose residue in Alismatales and Asparagales glucuronoxylans. Glucuronoarabinoxylans were the only xylans detected in the cell walls of five different members of the Poaceae family (grasses). By contrast, both glucuronoxylan and glucuronoarabinoxylan are formed by the Zingiberales and Commelinales (commelinids). At least one species of each monocot order, including the Poales, forms xylan with the reducing end sequence -4)-β-d-Xylp-(1,3)-α-l-Rhap-(1,2)-α-d-GalpA-(1,4)-d-Xyl first identified in eudicot and gymnosperm glucuronoxylans. This sequence was not discernible in the arabinopyranose-containing glucuronoxylans of the Alismatales and Asparagales or the glucuronoarabinoxylans of the Poaceae. Rather, our data provide additional evidence that in Poaceae glucuronoarabinoxylan, the reducing end xylose residue is often substituted at O-2 with 4-O-methyl glucuronic acid or at O-3 with arabinofuranose. The variations in xylan structure and their implications for the evolution and biosynthesis of monocot cell walls are discussed.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AGX:

Arabinoglucuronoxylan

AIR:

Alcohol-insoluble residue

Araf :

Arabinofuranose

Arap :

Arabinopyranose

2AB:

2-Aminobenzamide

GlcpA:

Glucuronic acid

MeGlcpA:

4-O-Methyl glucuronic acid

13C NMR:

Carbon nuclear magnetic resonance spectroscopy

GAX:

Glucuronoarabinoxylan

GX:

Glucuronoxylan

1H NMR:

Proton nuclear magnetic resonance spectroscopy

MALDI-TOF:

MS matrix-assisted laser desorption time-of-flight mass spectrometry

Xylp :

Xylopyranose

References

  • Bacic A, Harris P, Stone B (1988) Structure and function of plant cell walls. In: Preiss J (ed) The biochemistry of plants. Academic Press, San Diego, pp 297–371

    Chapter  Google Scholar 

  • Bigge J, Patel T, Bruce J, Goulding P, Charles S, Parekh R (1995) Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid. Anal Biochem 230:229–238

    Article  CAS  PubMed  Google Scholar 

  • Bremer B, Bremer K, Chase M, Fay M, Reveal J, Soltis D, Soltis P, Stevens P (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linnean Soc 161:105–121

    Article  Google Scholar 

  • Buanafina M (2009) Feruloylation in grasses: current and future perspectives. Mol Plant 2:861–872

    Article  CAS  Google Scholar 

  • Carnachan SM, Harris PJ (2000) Polysaccharide compositions of primary cell walls of the palms Phoenix canariensis and Rhopalostylis sapida. Plant Physiol Biochem 38:699–708

    Article  CAS  Google Scholar 

  • Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Biol 47:445–476

    Article  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Chase M, Soltis DE, Olmstead RG, Morgan D, Les D, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu Y-L (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann Mo Bot Garden 80:528–580

    Article  Google Scholar 

  • Chase M, Fay MF, Devey DS, Maurin O, Rønsted N, Davies TJ, Pillon Y, Petersen G, Seberg O, Tamura M (2006) Multigene analyses of monocot relationships: a summary. Aliso 22:63–75

    Google Scholar 

  • Chong S-L, Koutaniemi S, Juvonen M, Derba-Maceluch M, Mellerowicz EJ, Tenkanen M (2015) Glucuronic acid in Arabidopsis thaliana xylans carries a novel pentose substituent. Int J Biol Macromol 79:807–812

    Article  CAS  PubMed  Google Scholar 

  • Darvill JE, McNeil M, Darvill AG, Albersheim P (1980) Structure of plant cell walls: XI. Glucuronoarabinoxylan, a second hemicellulose in the primary cell walls of suspension-cultured sycamore cells. Plant Physiol 66:1135–1141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domon B, Costello C (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconjug J 5:397–409

    Article  CAS  Google Scholar 

  • Ebringerova A, Hromadkova Z, Heinze T (2005) Hemicellulose. Adv Polym Sci 186:1–67

    Article  CAS  Google Scholar 

  • Fangel J, Ulvskov P, Knox JP, Mikklelsen M, Harholt J, Popper Z, Willats W (2012) Cell wall evolution and diversity. Front Plant Sci 3:1–8

    Article  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 

  • Givnish TJ, Ames M, McNeal J, McKain MR, Steele PR, dePamphilis CW, Graham SW, Pires JC, Stevenson D, Zomlefer W (2010) Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Ann Mo Bot Garden 97:584–616

    Article  Google Scholar 

  • Glushka JN, Terrell M, York WS, O’Neill MA, Gucwa A, Darvill AG, Albersheim P, Prestegard JH (2003) Primary structure of the 2-O-methyl-α-fucose-containing side chain of the pectic polysaccharide, rhamnogalacturonan II. Carbohydr Res 338:341–352

    Article  CAS  PubMed  Google Scholar 

  • Harris P (2006) Primary and secondary plant cell walls: a comparative overview. N Zeal J For Sci 36:36–53

    CAS  Google Scholar 

  • Harris PJ, Hartley R (1980) Phenolic constituents of the cell walls of monocotyledons. Biochem Syst Ecol 8:153–160

    Article  CAS  Google Scholar 

  • Harris PJ, Trethewey J (2010) The distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochem Rev 9:19–33

    Article  CAS  Google Scholar 

  • Harris PJ, Kelderman MR, Kendon MF, McKenzie RJ (1997) Monosaccharide compositions of unlignified cell walls of monocotyledons in relation to the occurrence of wall-bound ferulic acid. Biochem Syst Ecol 25:167–179

    Article  CAS  Google Scholar 

  • Hervé C, Rogowski A, Gilbert HJ, Knox JP (2009) Enzymatic treatments reveal differential capacities for xylan recognition and degradation in primary and secondary plant cell walls. Plant J 58:413–422

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ishii T, Konishi T, Ono H, Ohnishi-Kameyama M, Togashi H, Shimizu K (2008) Assignment of the 1H and 13C NMR spectra of 2-aminobenzamide-labeled xylo-oligosaccharides. Carbohydr Polym 74:579–589

    Article  CAS  Google Scholar 

  • Johansson M, Samuelson O (1977) Reducing end groups in brich xylan and their alkaline degradation. Wood Sci Technol 11:251–263

    Article  CAS  Google Scholar 

  • Kulkarni AR, Pattathil S, Hahn M, York W, O’Neill MA (2012a) Comparison of arabinoxylan structure in bioenergy and model grasses. Ind Biotechnol 8:222–229

    Article  CAS  Google Scholar 

  • Kulkarni AR, Peña MJ, Avci U, Mazumder K, Urbanowicz B, Pattathil S, Yin Y, O’Neill MA, Roberts AW, Hahn MG (2012b) The ability of land plants to synthesize glucuronoxylans predates the evolution of tracheophytes. Glycobiology 22:439–451

    Article  CAS  PubMed  Google Scholar 

  • Lampugnani E, Moller I, Cassin A, Jones D, Koh PL, Ratnayake S, Beahan C, Wilson SM, Bacic A, Newbigin E (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 

  • Landolt E (1986) Biosystematic investigation in the family of duckweeds (“Lemnaceae”). The family of “Lemnaceae”: a monographic study, vol 2. Veröffentlichungen des Geobotanischen Institutes der ETH, Zürich

    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 

  • Mazumder K, York W (2010) Structural analysis of arabinoxylans isolated from ball milled switchgrass biomass. Carbohydr Res 345:2183–2193

    Article  CAS  PubMed  Google Scholar 

  • Mortimer JC, Faria-Blanc N, Yu X, Tryfona T, Sorieul M, Ng YZ, Zhang Z, Stott K, Anders N, Dupree P (2015) An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. Plant J 83:413–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Packer NH, Lawson MA, Jardine DR, Redmond JW (1998) A general approach to desalting oligosaccharides released from glycoproteins. Glycoconjug J 15:737–747

    Article  CAS  Google Scholar 

  • Peña MJ, Zhong R, Zhou GK, Richardson EA, O’Neill MA, Darvill AG, York WS, Ye ZH (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19:549–563

    Article  PubMed  PubMed Central  Google Scholar 

  • Peña MJ, Darvill AG, Eberhard S, York WS, O’Neill MA (2008) Moss and liverwort xyloglucans contain galacturonic acid and are structurally distinct from the xyloglucans synthesized by hornworts and vascular plants. Glycobiology 18:891–899

    Article  PubMed  Google Scholar 

  • Peña MJ, Kong Y, York WS, O’Neill MA (2012) A galacturonic acid-containing xyloglucan is involved in Arabidopsis root hair tip growth. Plant Cell 24:4511–4524

    Article  PubMed  PubMed Central  Google Scholar 

  • Ratnayake S, Beahan CT, Callahan DL, Bacic A (2014) The reducing end sequence of wheat endosperm cell wall arabinoxylans. Carbohydr Res 386:23–32

    Article  CAS  PubMed  Google Scholar 

  • Reis A, Pinto P, Evtuguin D, Neto CP, Domingues P, Ferrer-Correia A, Domingues MRM (2005) Electrospray tandem mass spectrometry of underivatised acetylated xylo-oligosaccharides. Rapid Comm Mass Spectrom 19:3589–3599

    Article  CAS  Google Scholar 

  • Saulnier L, Vigouroux J, Thibault J-F (1995) Isolation and partial characterization of feruloylated oligosaccharides from maize bran. Carbohydr Res 272:241–253

    Article  CAS  PubMed  Google Scholar 

  • Shatalov AA, Evtuguin DV, Pascoal Neto C (1999) (2-O-α-d-Galactopyranosyl-4-O-methyl-α-d-glucurono)-d-xylan from Eucalyptus globulus Labill. Carbohydr Res 320:93–99

    Article  CAS  PubMed  Google Scholar 

  • Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89

    Article  CAS  PubMed  Google Scholar 

  • Smith B, Harris P (1999) The polysaccharide composition of Poales cell walls: Poaceae cell walls are not unique. Biochem Syst Ecol 27:33–53

    Article  CAS  Google Scholar 

  • Togashi H, Kato A, Shimizu K (2009) Enzymatically derived aldouronic acids from Eucalyptus globulus glucuronoxylan. Carbohydr Polym 78:247–252

    Article  CAS  Google Scholar 

  • Urbanowicz BR, Peña MJ, Ratnaparkhe S, Avci U, Backe J, Steet HF, Foston M, Li H, O’Neill MA, Ragauskas AJ, Darvill AG, Wyman C, Gilbert HJ, York WS (2012) 4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Proc Nat Acad Sci USA 109:14253–14258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • York WS, O’Neill MA (2008) Biochemical control of xylan biosynthesis—which end is up? Curr Opin Plant Biol 11:258–265

    Article  CAS  PubMed  Google Scholar 

  • Zablackis E, Huang J, Muller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107:1129–1138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Teng Q, Lee C, Ye Z-H (2014) Identification of a disaccharide side chain 2-O-α-d-galactopyranosyl-α-d-glucuronic acid in Arabidopsis xylan. Plant Signal Behav 9:e27933

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was funded by the BioEnergy Science Center (BESC). BESC is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. We also acknowledge the U.S. Department of Energy-funded Center for Plant and Microbial Complex Carbohydrates (Grant DE-FG02-93ER20097) for equipment support.

Author information

Author notes

  1. Ameya R. Kulkarni

    Present address: Incyte Corporation, Wilmington, DE, 19803, USA

Authors and Affiliations

  1. Complex Carbohydrate Research Center and US Department of Energy Bioenergy Science Center, University of Georgia, Athens, GA, 30602, USA

    Maria J. Peña, Ameya R. Kulkarni, Jason Backe, Malcolm A. O’Neill & William S. York

  2. Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA

    Michael Boyd

  3. Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, 30602, USA

    William S. York

Authors
  1. Maria J. Peña
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ameya R. Kulkarni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jason Backe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Boyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Malcolm A. O’Neill
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. William S. York
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to William S. York.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest

Additional information

M. J. Peña and A. R. Kulkarni contributed equally to this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 1340 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peña, M.J., Kulkarni, A.R., Backe, J. et al. Structural diversity of xylans in the cell walls of monocots. Planta 244, 589–606 (2016). https://doi.org/10.1007/s00425-016-2527-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2527-1

Keywords

Search

Navigation