BioEnergy Research

, Volume 9, Issue 3, pp 969–979 | Cite as

Eucalyptus Cell Wall Architecture: Clues for Lignocellulosic Biomass Deconstruction

  • Marcela Mendes Salazar
  • Adriana Grandis
  • Sivakumar Pattathil
  • Jorge Lepikson Neto
  • Eduardo Leal Oliveira Camargo
  • Ana Alves
  • José Carlos Rodrigues
  • Fabio Squina
  • João Paulo Franco Cairo
  • Marcos S. Buckeridge
  • Michael G. Hahn
  • Gonçalo Amarante Guimarães Pereira


The architecture, composition, and chemical properties of wood cell walls have a direct influence on the process that occurs prior to fermentation in second-generation biofuel production. The understanding of the construction patterns of cell wall types is the key to the new era of second-generation biofuels. Eucalyptus species are great candidates for this purpose since these species are among the fastest growing hardwood trees in the world and they have been improved for biomass production. We applied the glycome profiling and other combined techniques to study xylem cell walls of three economically important species (Eucalyptus globulus, Eucalyptus grandis, and Eucalyptus urophylla). Glycome profiling analyses revealed that species differ in the same key aspects of cell wall polymer linkages, with E. globulus and E. urophylla presenting contrasting phenotypes, and E. grandis with intermediate characteristics. E. urophylla is known for high recalcitrance, that is probably determined by the strong associations between lignin and cell wall polymers, and also lignin content. On the other hand, E. globulus cell wall polymers are loosely linked, so its cell wall can be easily deconstructed. We have shown in this work that the composition of cell walls differs in quantity and quality among the Eucalyptus species and such variations in composition influence the process of lignocellulosic feedstock assessment. However, the greatest influence relies on the amount and type of associations between cell wall polymers. A high yield of cellulose, from any biomass source, directly depends on the cell wall architecture.


Bioethanol Cell wall architecture Glycome profiling Eucalyptus Wood 


1 M

1 Molar

4 M

4 Molar


Alcohol-insoluble residues


Dimethyl sulfoxide






Fucosylated xyloglucan


Galacturonic acid










Lignin-carbohydrate complex





Non-fuc XG

Non-fucosylated xyloglucan


Post chlorite


Rhamnogalacturonan backbone




Rhamnogalacturonan I


Rhamnogalacturonan II











The authors would like to thank International Paper-Brazil for kindly providing plant materials and Espaço da Escrita/Coordenadoria Geral-UNICAMP for English revision. This work was supported by research funding of FAPESP (process number 2007/54877-0) and grants from International Paper do Brasil (IP/IB/Gene Discovery: 3972).


  1. 1.
    Buckeridge MS, Goldman GH (2011) Routes to cellulosic ethanol. Springer, New YorkCrossRefGoogle Scholar
  2. 2.
    Hochman G, Zilberman D (2014) Algae farming and its bio-products. In: Edited by McCann MC, Carpita NC, Buckeridge MS, editors. New York: Springer, 40–66Google Scholar
  3. 3.
    Meyer MM and Salatino A (2014) Perspectives in Brazil of the contribution of palm trees to biodiesel production. In: McCann, MC, Carpita, NC, Buckeridge, MS, editors. New York: Springer, 141–152Google Scholar
  4. 4.
    Ragauskas AJ et al (2006) The path forward for biofuels and biomaterials. Science 311:484–489CrossRefPubMedGoogle Scholar
  5. 5.
    Jørgensen H, Kristensen JB, Felby C (2007) Enzymatic conversion of lignocellulose into fermentable sugars: challenges and opportunities. Biofuels, Bioproducts and Biorefining 1(2):119–134CrossRefGoogle Scholar
  6. 6.
    Salisbury FB, Ross CW (1991) Plant physiology, 4th edn. Wassworth Publishing Company, BelmontGoogle Scholar
  7. 7.
    Li L, Lu S, Chiang V (2006) A genomic and molecular view of wood formation. Crit Rev Plant Sci 25:215–233CrossRefGoogle Scholar
  8. 8.
    Carpita NC, Campbell M, Tierney M (2001) Plant cell walls. Springer Science + Business Media, DordrechtCrossRefGoogle Scholar
  9. 9.
    Wilson SM et al (2012) Pattern of deposition of cell wall polysaccharides and transcript abundance of related cell wall synthesis genes during differentiation in barley endosperm. Plant Physiol 159:655–670CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Hamelinck CN, Hooijdonk G, Faaij APC (2005) Ethanol from lignocellulosic biomass: techno-economic performance in short-, middle- and long-term. Biomass and Bioenergy 28:384–410CrossRefGoogle Scholar
  11. 11.
    Simmons BA, Loque D, Blanch HW (2008) Next-generation biomass feedstocks for biofuel production. Genome Biol 9:242CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Naik SN, Goud VV, Rout PK, Dalai AK (2010) Production of first and second generation biofuels: a comprehensive review. Renew Sustain Energy Rev 14:578–597CrossRefGoogle Scholar
  13. 13.
    Li M, Pattathil S, Hahn MG, Hodge DB (2014) Identification of features associated with plant cell wall recalcitrance to pretreatment by alkaline hydrogen peroxide in diverse bioenergy feedstocks using glycome profiling. RSC Advances 4:17282CrossRefGoogle Scholar
  14. 14.
    Turnbull JW (2001) Economic and social importance of eucalyptus. In: Keane PJ, Kile GA, Podger FD, Brown BN, editors. Collingwood: CSIRO Publishing, 1–9Google Scholar
  15. 15.
    González-García S, Moreira MT, Feijoo G (2012) Environmental aspects of eucalyptus based ethanol production and use. Sci Total Environ 438:1–8CrossRefPubMedGoogle Scholar
  16. 16.
    Potts BM and Pederick LA (2000) Morphology, phylogeny, origin, distribution and genetic diversity of eucalyptus. In Keane PJ, Kile GA, Podger FD, Brown BN, editors. Collingwood:CSIRO Publishing. 11–34Google Scholar
  17. 17.
    Foekel C (2009) Papermaking properties of eucalyptus trees, woods, and pulp fibers. [,] Accessed in 13 Sep 2014
  18. 18.
    Grattapaglia D (2008) Genomics of Eucalyptus, a global tree for energy, paper, and wood. In Moore PH, Ming R, editors. New York: Springer, 259 – 297Google Scholar
  19. 19.
    Grattapaglia D (2004) Integrating genomics into Eucalyptus breeding. Genet Mol Res 369–379Google Scholar
  20. 20.
    Bison O, Ramalho MAP, Rezende GDSP, Aguiar AM, De Resende MDV (2007) Combining ability of elite clones of Eucalyptus grandis and Eucalyptus urophylla with Eucalyptus globulus. Genet Mol Biol 30(2):417–422CrossRefGoogle Scholar
  21. 21.
    Silveira RL, Stayanov SR, Gusarov S, Skaf MS, Kovalenko A (2013) Plant biomass recalcitrance: effect of hemicellulose composition on nanoscale forces that control cell wall strength. J Am Chem Soc 135:19048–19051CrossRefPubMedGoogle Scholar
  22. 22.
    Zeng J, Singh D, Gao D, Chen S (2014) Effects of lignin modification on wheat staw cell wall deconstruction by Phanerochaete chrysosporium. Biotechnology for Biofuels 7:161CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    DeMartini JD et al (2011) Application of monoclonal antibodies to investigate plant cell wall deconstruction for biofuels production. Energy Environ Sci 4(4332)Google Scholar
  24. 24.
    De Souza AP, Leite DCC, Pattathil S, Hahn MG, Buckeridge MS (2013) Composition and structure of sugarcane cell wall polysaccharides: implications for second-generation bioethanol production. Bioenergy Research 6:564–579CrossRefGoogle Scholar
  25. 25.
    Camargo ELO et al (2014) Contrasting nitrogen fertilization treatments impact xylem gene expression and secondary cell wall lignification in Eucalyptus. BMC Plant Biol 14:256CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    De Souza AP et al (2015) J Exp Bot. doi: 10.1093/jxb/erv183
  27. 27.
    Pattathil S, Saffold T, Gallego-Giraldo L, O’Neill M, York WS, Dixon RA, Hahn MG et al (2012) Changes in cell wall carbohydrate extractability are correlated with reduced recalcitrance of HCT downregulated alfalfa biomass. Ind Biotechnol 8(4)Google Scholar
  28. 28.
    Pattathil S, Avci U, Miller JS, Hahn MG (2012) Immunological approaches to plant cell wall and biomass characterization: glycome profiling. In: Himmel M (ed). New York: Humana Press, 61-72Google Scholar
  29. 29.
    McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96:323–334Google Scholar
  30. 30.
    Brett C, Waldron KN (1996) Physiology and biochemistry of plant cell walls, 1st edn. Champ and Hall, LondonGoogle Scholar
  31. 31.
    Popper ZA, Fry SC (2008) Xyloglucan-pectin linkages are formed intra-protoplasmically, contribute to wall-assembly, and remain stable in the cell wall. Planta 227(4):781–794CrossRefPubMedGoogle Scholar
  32. 32.
    Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2011) Plant cell walls—from chemistry to biology. Garland Science, New YorkGoogle Scholar
  33. 33.
    Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing wall. Plant Cell Physiology 56(2):180–194CrossRefPubMedGoogle Scholar
  34. 34.
    Cetinkol OP et al (2012) Structural and chemical characterization of hardwood from tree species with applications as bioenergy feedstocks. PLoS One 7(12):e52820CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277CrossRefPubMedGoogle Scholar
  36. 36.
    Abramson M, Shoseyov O, Shani Z (2010) Plant cell wall reconstruction toward improved lignocellulosec production and processability. Plant Sci 178(2):61–72CrossRefGoogle Scholar
  37. 37.
    Liners F, Letesson J, Didembourg C, Cutsem PV (1989) Monoclonal antibodies against pectin recognition of a conformation induced by calcium. Plant Physiol 91:1419–1424CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Carpita NC (1984) Fractionation of hemicelluloses from maize cell walls with increasing concentrations of alkali. Phytochemistry 23(5):1089–1093CrossRefGoogle Scholar
  39. 39.
    Salazar MM et al (2013) Xylem transcription profiles indicate potential metabolic responses for economically relevant characteristics of Eucalyptus species. BMC Genomics 14:201CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Sheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289CrossRefGoogle Scholar
  41. 41.
    Melton LD, Smith BG (2005) Isolation of plant cell walls and fractionation of cell wall polysaccharides. In: Wrolstad RE, Acree TE, Decker EA, Penner MH, Reid DS, Schwartz SJ, Shoemaker CF, Smith D, Sporns P. New York: Wiley-Interscience, 697–719Google Scholar
  42. 42.
    Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546CrossRefPubMedGoogle Scholar
  43. 43.
    Shi R, Sun Y-H, Li Q, Heber S, Sederoff R, Chiang VL (2010) Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol 51(10):144–163CrossRefPubMedGoogle Scholar
  44. 44.
    Lepikson-Neto J et al (2013) Flavonoid supplementation reduces the extractive content and increases the syringyl/guaiacyl ration in Eucalyptus grandis X Eucalyptus urophylla hybrid species. Bioresources 8(2):1747–1757CrossRefGoogle Scholar
  45. 45.
    Lepikson-Neto J et al (2014) Flavonoid supplementation affects the expression of genes involved in cell wall formation and lignification metabolism and increases sugar content and saccharification in the fast-growing eucalyptus hybrid E. urophylla x E. grandis. BMC Plant Biol 14:301CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Carpita NC (1983) Hemicellulosic polymers of cell-walls of Zea coleoptiles. Plant Physiol 72:512–521CrossRefGoogle Scholar
  47. 47.
    Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method determination of sugars and related substances. Anal Chem 28(3):350–356CrossRefGoogle Scholar
  48. 48.
    Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S-I, Lee YC (2005) Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal Biochem 339(1):69–72CrossRefPubMedGoogle Scholar
  49. 49.
    Pattathil S et al (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153:514–525CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Saeman JF, Harris EE, Kline AA (1945) Quantitative saccharification of wood and cellulose. Anal Chem 17:35–37Google Scholar
  51. 51.
    Buckeridge MS, Dietrich SMC (1996) Mobilisation of the raffinose family oligosaccharides and galactomannan in germinating seeds of Sesbania marginata Benth (Leguminosae-Faboideae). Plant Sci 117:33–43CrossRefGoogle Scholar
  52. 52.
    Dos Santos HP, Purgatto E, Mercier H, Buckeridge MS (2004) The control of storage xyloglucan mobilization in cotyledons of Hymenaea courbaril. Plant Physiol 135:287–299CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Amaral LIV, Gaspar M, Costa PMF, Aidar MPM, Buckeridge MS (2007) A new rapid and sensitive enzymatic method for extraction and quantification of starch in plant material. Hoehnea. 34Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Marcela Mendes Salazar
    • 1
    • 2
  • Adriana Grandis
    • 3
  • Sivakumar Pattathil
    • 4
  • Jorge Lepikson Neto
    • 1
    • 2
  • Eduardo Leal Oliveira Camargo
    • 1
  • Ana Alves
    • 5
  • José Carlos Rodrigues
    • 5
  • Fabio Squina
    • 6
  • João Paulo Franco Cairo
    • 1
    • 6
  • Marcos S. Buckeridge
    • 3
  • Michael G. Hahn
    • 4
  • Gonçalo Amarante Guimarães Pereira
    • 1
  1. 1.Genomic and Expression Laboratory, Department of Evolution Genetics and Bioagents, Institute of BiologyUniversity of CampinasCampinasBrazil
  2. 2.Senai Innovation Institute for BiomassTrês LagoasBrazil
  3. 3.Department of Botany, Institute of BiosciencesUniversity of São PauloSão PauloBrazil
  4. 4.BioEnergy Science Center, Complex Carbohydrate Research CenterUniversity of GeorgiaAthensUSA
  5. 5.Tropical Research Institute of Portugal (IICT), Forestry and Forest Products GroupLisbonPortugal
  6. 6.Brazilian Bioethanol Science and Technology Laboratory (CTBE)CampinasBrazil

Personalised recommendations