Advertisement

Planta

, Volume 244, Issue 3, pp 589–606 | Cite as

Structural diversity of xylans in the cell walls of monocots

  • Maria J. Peña
  • Ameya R. Kulkarni
  • Jason Backe
  • Michael Boyd
  • Malcolm A. O’Neill
  • William S. York
Original Article

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.

Keywords

Monocot Cell wall Glucuronoarabinoxylan Glucuronoxylan 

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

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest

Supplementary material

425_2016_2527_MOESM1_ESM.pptx (1.3 mb)
Supplementary material 1 (PPTX 1340 kb)

References

  1. 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 297–371CrossRefGoogle Scholar
  2. 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 230:229–238CrossRefPubMedGoogle Scholar
  3. 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 161:105–121CrossRefGoogle Scholar
  4. Buanafina M (2009) Feruloylation in grasses: current and future perspectives. Mol Plant 2:861–872CrossRefGoogle Scholar
  5. Carnachan SM, Harris PJ (2000) Polysaccharide compositions of primary cell walls of the palms Phoenix canariensis and Rhopalostylis sapida. Plant Physiol Biochem 38:699–708CrossRefGoogle Scholar
  6. Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Biol 47:445–476CrossRefGoogle Scholar
  7. 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 3:1–30CrossRefPubMedGoogle Scholar
  8. 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 80:528–580CrossRefGoogle Scholar
  9. 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 22:63–75Google Scholar
  10. 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 79:807–812CrossRefPubMedGoogle Scholar
  11. 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 66:1135–1141CrossRefPubMedPubMedCentralGoogle Scholar
  12. Domon B, Costello C (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconjug J 5:397–409CrossRefGoogle Scholar
  13. Ebringerova A, Hromadkova Z, Heinze T (2005) Hemicellulose. Adv Polym Sci 186:1–67CrossRefGoogle Scholar
  14. Fangel J, Ulvskov P, Knox JP, Mikklelsen M, Harholt J, Popper Z, Willats W (2012) Cell wall evolution and diversity. Front Plant Sci 3:1–8CrossRefGoogle Scholar
  15. Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738CrossRefPubMedGoogle Scholar
  16. 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 97:584–616CrossRefGoogle Scholar
  17. 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 338:341–352CrossRefPubMedGoogle Scholar
  18. Harris P (2006) Primary and secondary plant cell walls: a comparative overview. N Zeal J For Sci 36:36–53Google Scholar
  19. Harris PJ, Hartley R (1980) Phenolic constituents of the cell walls of monocotyledons. Biochem Syst Ecol 8:153–160CrossRefGoogle Scholar
  20. Harris PJ, Trethewey J (2010) The distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochem Rev 9:19–33CrossRefGoogle Scholar
  21. 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 25:167–179CrossRefGoogle Scholar
  22. 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 58:413–422CrossRefPubMedGoogle Scholar
  23. Hsieh YSY, Harris PJ (2009) Xyloglucans of monocotyledons have diverse structures. Mol Plant 2:943–965CrossRefPubMedGoogle Scholar
  24. 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 74:579–589CrossRefGoogle Scholar
  25. Johansson M, Samuelson O (1977) Reducing end groups in brich xylan and their alkaline degradation. Wood Sci Technol 11:251–263CrossRefGoogle Scholar
  26. Kulkarni AR, Pattathil S, Hahn M, York W, O’Neill MA (2012a) Comparison of arabinoxylan structure in bioenergy and model grasses. Ind Biotechnol 8:222–229CrossRefGoogle Scholar
  27. 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 22:439–451CrossRefPubMedGoogle Scholar
  28. 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:e77140CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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, ZürichGoogle Scholar
  30. Liu L, Paulitz J, Pauly M (2015) The presence of fucogalactoxyloglucan and its synthesis in rice indicates conserved functional importance in plants. Plant Physiol 168:549–560CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mazumder K, York W (2010) Structural analysis of arabinoxylans isolated from ball milled switchgrass biomass. Carbohydr Res 345:2183–2193CrossRefPubMedGoogle Scholar
  32. 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 83:413–426CrossRefPubMedPubMedCentralGoogle Scholar
  33. Packer NH, Lawson MA, Jardine DR, Redmond JW (1998) A general approach to desalting oligosaccharides released from glycoproteins. Glycoconjug J 15:737–747CrossRefGoogle Scholar
  34. 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 19:549–563CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 18:891–899CrossRefPubMedGoogle Scholar
  36. 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 24:4511–4524CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ratnayake S, Beahan CT, Callahan DL, Bacic A (2014) The reducing end sequence of wheat endosperm cell wall arabinoxylans. Carbohydr Res 386:23–32CrossRefPubMedGoogle Scholar
  38. 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 19:3589–3599CrossRefGoogle Scholar
  39. Saulnier L, Vigouroux J, Thibault J-F (1995) Isolation and partial characterization of feruloylated oligosaccharides from maize bran. Carbohydr Res 272:241–253CrossRefPubMedGoogle Scholar
  40. 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 320:93–99CrossRefPubMedGoogle Scholar
  41. Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89CrossRefPubMedGoogle Scholar
  42. Smith B, Harris P (1999) The polysaccharide composition of Poales cell walls: Poaceae cell walls are not unique. Biochem Syst Ecol 27:33–53CrossRefGoogle Scholar
  43. Togashi H, Kato A, Shimizu K (2009) Enzymatically derived aldouronic acids from Eucalyptus globulus glucuronoxylan. Carbohydr Polym 78:247–252CrossRefGoogle Scholar
  44. 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 109:14253–14258CrossRefPubMedPubMedCentralGoogle Scholar
  45. York WS, O’Neill MA (2008) Biochemical control of xylan biosynthesis—which end is up? Curr Opin Plant Biol 11:258–265CrossRefPubMedGoogle Scholar
  46. Zablackis E, Huang J, Muller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107:1129–1138CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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:e27933CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Maria J. Peña
    • 1
  • Ameya R. Kulkarni
    • 1
    • 4
  • Jason Backe
    • 1
  • Michael Boyd
    • 2
  • Malcolm A. O’Neill
    • 1
  • William S. York
    • 1
    • 3
  1. 1.Complex Carbohydrate Research Center and US Department of Energy Bioenergy Science CenterUniversity of GeorgiaAthensUSA
  2. 2.Department of Plant BiologyUniversity of GeorgiaAthensUSA
  3. 3.Department of Biochemistry and Molecular BiologyUniversity of GeorgiaAthensUSA
  4. 4.Incyte CorporationWilmingtonUSA

Personalised recommendations