Linking Plant Biology and Pretreatment: Understanding the Structure and Organization of the Plant Cell Wall and Interactions with Cellulosic Biofuel Production

  • Rebecca Garlock Ong
  • Shishir P. S. Chundawat
  • David B. Hodge
  • Sai Keskar
  • Bruce E. Dale
Chapter
Part of the Advances in Plant Biology book series (AIPB, volume 4)

Abstract

In order to more economically process cellulosic feedstocks using a biochemical pathway for fuel production, it is necessary to develop a detailed understanding of plant cell wall characteristics, pretreatment reaction chemistry, and their complex interactions. However given the large number of thermochemical pretreatment methods that are currently being researched and the extreme diversity of plant cell wall structure and composition, this prospect is extremely challenging. Here we present the current state of research at the interface between plant biology and pretreatment chemistry. The first two sections discuss the chemistry of the secondary plant cell wall and how different pretreatment methods alter the overall cell wall structure. The third section addresses how the characteristics of the cell wall and pretreatment efficacy are impacted by different factors such as plant maturity, classification, and plant fraction. The fourth section summarizes current directions in the development of novel plant materials for improved biochemical conversion. And the final section discusses the use of chemical pretreatments as a screening and analysis tool for rapid identification of amenable plant materials, and for expansion of the fundamental understanding of plant cell walls.

Keywords

Enzymatic digestibility Lignocellulose Plant breeding and transgenesis Plant cell wall Pretreatment chemistry Screening tools 

Abbreviations

AFEX™

Ammonia fiber expansion

BMIMCl

1-butyl-3-methylimidazolium chloride

CBM

Carbohydrate binding module

EMIMAc

1-ethyl-3-methylimidazolium acetate

EMIMCl

1-ethyl-3-methylimidazolium chloride

G

Guaiacyl

GAX

Glucuronoarabinoxylan

H

p-hydroxyphenyl

IL

Ionic liquid

S

Syringyl

TAGs

Triacylglycerols

References

  1. Abe K, Yano H (2009) Comparison of the characteristics of cellulose microfibril aggregates of wood, rice straw and potato tuber. Cellulose 16:1017–1023Google Scholar
  2. Abramson M, Shoseyov O, Hirsch S, Shani Z (2013) Genetic modifications of plant cell walls to increase biomass and bioethanol production. In: Lee JW (ed) Advanced biofuels and bioproducts. Springer, New York, pp 315–338Google Scholar
  3. Adler PR, Sanderson MA, Boateng AA, Weimer PJ, Jung H-JG (2006) Biomass yield and biofuel quality of switchgrass harvested in fall or spring. Agron J 98:1518–1525Google Scholar
  4. Åkerholm M, Salmén L (2001) Interactions between wood polymers studied by dynamic ft-ir spectroscopy. Polym 42:963–969Google Scholar
  5. Åkerholm M, Salmén L (2004) Softening of wood polymers induced by moisture studied by dynamic FTIR spectroscopy. J Appl Polym Sci 94:2032–2040Google Scholar
  6. Alonso-Simón A, Kristensen JB, Øbro J, Felby C, Willats WGT, Jørgensen H (2010) High-throughput microarray profiling of cell wall polymers during hydrothermal pre-treatment of wheat straw. Biotechnol Bioeng 105:509–514PubMedGoogle Scholar
  7. Altaner CM, Jarvis MC (2008) Modelling polymer interactions of the `molecular velcro’ type in wood under mechanical stress. J Theor Biol 253:434–445PubMedGoogle Scholar
  8. Arantes V, Saddler J (2011) Cellulose accessibility limits the effectiveness of minimum cellulase loading on the efficient hydrolysis of pretreated lignocellulosic substrates. Biotechnol Biofuel 4(3):1–16Google Scholar
  9. Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285PubMedGoogle Scholar
  10. Awal A, Sain M (2011) Spectroscopic studies and evaluation of thermorheological properties of softwood and hardwood lignin. J Appl Polym Sci 122:956–963Google Scholar
  11. Azarpira A, Lu F, Ralph J (2011) Reactions of dehydrodiferulates with ammonia. Org Biomol Chem 9:6779–6787PubMedGoogle Scholar
  12. Bals B, Rogers C, Jin MJ, Balan V, Dale B (2010) Evaluation of ammonia fibre expansion (AFEX) pretreatment for enzymatic hydrolysis of switchgrass harvested in different seasons and locations. Biotechnol Biofuel 3(1):1–11Google Scholar
  13. Banerjee G, Car S, Scott-Craig J, Borrusch M, Walton J (2010) Rapid optimization of enzyme mixtures for deconstruction of diverse pretreatment/biomass feedstock combinations. Biotechnol Biofuel 3:22Google Scholar
  14. Barrière Y, Ralph J, Méchin V, Guillaumie S, Grabber JH, Argillier O et al (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. C R Biol 327:847–860PubMedGoogle Scholar
  15. Buanafina MMdO, Langdon T, Hauck B, Dalton S, Morris P (2008) Expression of a fungal ferulic acid esterase increases cell wall digestibility of tall fescue (Festuca arundinacea). Plant Biotechnol J 6:264–280PubMedGoogle Scholar
  16. Carpita NC (2012) Progress in the biological synthesis of the plant cell wall: New ideas for improving biomass for bioenergy. Curr Opin Biotechnol 23:330–337PubMedGoogle Scholar
  17. 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 3:1–30PubMedGoogle Scholar
  18. Casler MD, Buxton DR, Vogel KP (2002) Genetic modification of lignin concentration affects fitness of perennial herbaceous plants. Theor Appl Genet 104:127–131PubMedGoogle Scholar
  19. Chandrasekaran A, Bharadwaj R, Park JI, Sapra R, Adams PD, Singh AK (2010) A microscale platform for integrated cell-free expression and activity screening of cellulases. J Proteome Res 9:5677–5683PubMedGoogle Scholar
  20. Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761PubMedGoogle Scholar
  21. Chen L, Auh C, Chen F, Cheng XF, Aljoe H, Dixon RA et al (2002) Lignin deposition and associated changes in anatomy, enzyme activity, gene expression, and ruminal degradability in stems of tall fescue at different developmental stages. J Agric Food Chem 50:5558–5565PubMedGoogle Scholar
  22. Chiniquy D, Sharma V, Schultink A, Baidoo EE, Rautengarten C, Cheng K et al (2012) XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. PNAS 109:17117–17122PubMedGoogle Scholar
  23. Chuck GS, Tobias C, Sun L, Kraemer F, Li C, Dibble D, et al (2011) Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass. PNAS, http://www.pnas.org/content/early/2011/10/04/1113971108.abstract. (Ahead of Print)
  24. Chundawat SPS, Balan V, Dale BE (2008) High-throughput microplate technique for enzymatic hydrolysis of lignocellulosic biomass. Biotechnol Bioeng 99:1281–1294PubMedGoogle Scholar
  25. Chundawat SPS, Donohoe BS, Sousa L, Elder T, Agarwal UP, Lu F et al (2011) Multi-scale visualization and characterization of plant cell wall deconstruction during thermochemical pretreatment. Energ Environ Sci 4:973–984Google Scholar
  26. Chundawat SPS, Vismeh R, Sharma LN, Humpula JF, da Costa Sousa L, Chambliss CK et al (2010) Multifaceted characterization of cell wall decomposition products formed during ammonia fiber expansion (AFEX) and dilute acid based pretreatments. Bioresour Technol 101:8429–8438PubMedGoogle Scholar
  27. Clayton DW, Phelps GR (1965) The sorption of glucomannan and xylan on α-cellulose wood fibers. J Polym Sci: Part C 11:197–220Google Scholar
  28. Coleman HD, Ellis DD, Gilbert M, Mansfield SD (2006) Up-regulation of sucrose synthase and udp-glucose pyrophosphorylase impacts plant growth and metabolism. Plant Biotechnol J 4:87–101PubMedGoogle Scholar
  29. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedGoogle Scholar
  30. da Costa Sousa L, Chundawat SPS, Balan V, Dale BE (2009) `Cradle-to-grave’ assessment of existing lignocellulose pretreatment technologies. Curr Opin Biotechnol 20:339–347Google Scholar
  31. Dammström S, Salmén L, Gatenholm P (2009) On the interactions between cellulose and xylan, a biomimetic simulation of the hardwood cell wall. BioResources 4:3–14Google Scholar
  32. Davison BH, Drescher SR, Tuskan GA, Davis MF, Nghiem NP (2006) Variation of S/G ratio and lignin content in a Populus family influences the release of xylose by dilute acid hydrolysis. Appl Biochem Biotechnol 129–132:427–435PubMedGoogle Scholar
  33. de Lima DU, Buckeridge MS (2001) Interaction between cellulose and storage xyloglucans: the influence of the degree of galactosylation. Carbohydr Polym 46:157–163Google Scholar
  34. DeMartini J, Wyman C (2011a) Composition and hydrothermal pretreatment and enzymatic saccharification performance of grasses and legumes from a mixed-species prairie. Biotechnol Biofuel 4(52):1–10Google Scholar
  35. DeMartini JD, Pattathil S, Avci U, Szekalski K, Mazumder K, Hahn MG et al (2011a) Application of monoclonal antibodies to investigate plant cell wall deconstruction for biofuels production. Energ Environ Sci 4:4332–4339Google Scholar
  36. DeMartini JD, Studer MH, Wyman CE (2011b) Small-scale and automatable high-throughput compositional analysis of biomass. Biotechnol Bioeng 108:306–312PubMedGoogle Scholar
  37. DeMartini JD, Wyman CE (2011b) Changes in composition and sugar release across the annual rings of Populus wood and implications on recalcitrance. Bioresour Technol 102:1352–1358PubMedGoogle Scholar
  38. Dien BS, Jung H-JG, Vogel KP, Casler MD, Lamb JFS, Iten L et al (2006) Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass. Biomass Bioenerg 30:880–891Google Scholar
  39. Donaldson L (2007) Cellulose microfibril aggregates and their size variation with cell wall type. Wood Sci Technol 41:443–460Google Scholar
  40. Donohoe B, Decker S, Tucker M, Himmel M, Vinzant T (2008) Visualizing lignin coalescence and migration through maize cell walls following thermochemical pretreatment. Biotechnol Bioeng 101:913–925PubMedGoogle Scholar
  41. Donohoe BS, Selig MJ, Viamajala S, Vinzant TB, Adney WS, Himmel ME (2009) Detecting cellulase penetration into corn stover cell walls by immuno-electron microscopy. Biotechnol Bioeng 103:480–489PubMedGoogle Scholar
  42. Donohoe BS, Vinzant TB, Elander RT, Pallapolu VR, Lee YY, Garlock RJ et al (2011) Surface and ultrastructural characterization of raw and pretreated switchgrass. Bioresour Technol 102:11097–11104PubMedGoogle Scholar
  43. Du BW, Sharma LN, Becker C, Chen S-F, Mowery RA, van Walsum GP et al (2010) Effect of varying feedstock–pretreatment chemistry combinations on the formation and accumulation of potentially inhibitory degradation products in biomass hydrolysates. Biotechnol Bioeng 107:430–440PubMedGoogle Scholar
  44. Duguid KB, Montross MD, Radtke CW, Crofcheck CL, Shearer SA, Hoskinson RL (2007) Screening for sugar and ethanol processing characteristics from anatomical fractions of wheat stover. Biomass Bioenerg 31:585–592Google Scholar
  45. Duguid KB, Montross MD, Radtke CW, Crofcheck CL, Wendt LM, Shearer SA (2009) Effect of anatomical fractionation on the enzymatic hydrolysis of acid and alkaline pretreated corn stover. Bioresour Technol 100:5189–5195PubMedGoogle Scholar
  46. Durrett TP, Benning C, Ohlrogge J (2008) Plant triacylglycerols as feedstocks for the production of biofuels. Plant J 54:593–607PubMedGoogle Scholar
  47. Engels FM, Jung HG (1998) Alfalfa stem tissues: cell-wall development and lignification. Ann Bot 82:561–568Google Scholar
  48. Eudes A, George A, Mukerjee P, Kim JS, Pollet B, Benke PI et al (2012) Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification. Plant Biotechnol J 10:609–620PubMedGoogle Scholar
  49. Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M, et al (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. PNAS, http://www.pnas.org/content/early/2011/02/04/1100310108.abstract. (Ahead of Print)
  50. Fu D, Mazza G (2011) Aqueous ionic liquid pretreatment of straw. Bioresour Technol 102:7008–7011PubMedGoogle Scholar
  51. Funke M, Buchenauer A, Mokwa W, Kluge S, Hein L, Muller C et al (2010) Bioprocess control in microscale: scalable fermentations in disposable and user-friendly microfluidic systems. Microb Cell Fact 9(86):1–13Google Scholar
  52. Garlock R, Chundawat S, Balan V, Dale B (2009) Optimizing harvest of corn stover fractions based on overall sugar yields following ammonia fiber expansion pretreatment and enzymatic hydrolysis. Biotechnol Biofuel 2(29):1–14Google Scholar
  53. Garlock RJ, Balan V, Dale BE (2012a) Optimization of AFEX™ pretreatment conditions and enzyme mixtures to maximize sugar release from upland and lowland switchgrass. Bioresour Technol 104:757–768PubMedGoogle Scholar
  54. Garlock RJ, Balan V, Dale BE, Ramesh Pallapolu V, Lee YY, Kim Y et al (2011) Comparative material balances around pretreatment technologies for the conversion of switchgrass to soluble sugars. Bioresour Technol 102:11063–11071PubMedGoogle Scholar
  55. Garlock RJ, Bals B, Jasrotia P, Balan V, Dale BE (2012b) Influence of variable species composition on the saccharification of AFEX™ pretreated biomass from unmanaged fields in comparison to corn stover. Biomass Bioenerg 37:49–59Google Scholar
  56. Garrote G, Domínguez H, Parajó JC (1999) Hydrothermal processing of lignocellulosic materials. Eur J Wood Wood Prod 57:191–202Google Scholar
  57. Gericke M, Fardim P, Heinze T (2012) Ionic liquids—promising but challenging solvents for homogeneous derivatization of cellulose. Molecules 17:7458–7502PubMedGoogle Scholar
  58. Gille S, Pauly M (2012) O-acetylation of plant cell wall polysaccharides. Front Plant Sci 3(12):1–7Google Scholar
  59. Gomez L, Whitehead C, Barakate A, Halpin C, McQueen-Mason S (2010) Automated saccharification assay for determination of digestibility in plant materials. Biotechnol Biofuel 3(23):1–12Google Scholar
  60. Grabber JH, Hatfield RD, Lu FC, Ralph J (2008) Coniferyl ferulate incorporation into lignin enhances the alkaline delignification and enzymatic degradation of cell walls. Biomacromolecules 9:2510–2516PubMedGoogle Scholar
  61. Grabber JH, Ralph J, Hatfield RD (1998) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J Agric Food Chem 46:2609–2614Google Scholar
  62. Harris D, Stork J, Debolt S (2009) Genetic modification in cellulose-synthase reduces crystallinity and improves biochemical conversion to fermentable sugar. GCB Bioenergy 1:51–61Google Scholar
  63. Harris P, Trethewey J (2010) The distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochem Rev 9:19–33Google Scholar
  64. Hartati S, Sudarmonowati E, Park YW, Kaku T, Kaida R, Baba Ki et al (2008) Overexpression of poplar cellulase accelerates growth and disturbs the closing movements of leaves in sengon. Plant Physiol 147:552–561PubMedGoogle Scholar
  65. Iiyama K, Lam TBT, Stone BA (1990) Phenolic acid bridges between polysaccharides and lignin in wheat internodes. Phytochem 29:733–737Google Scholar
  66. Imamura T, Watanabe T, Kuwahara M, Koshijima T (1994) Ester linkages between lignin and glucuronic acid in lignin-carbohydrate complexes from Fagus crenata. Phytochem 37:1165–1173Google Scholar
  67. Ishizawa CI, Davis MF, Schell DF, Johnson DK (2007) Porosity and its effect on the digestibility of dilute sulfuric acid pretreated corn stover. J Agric Food Chem 55:2575–2581PubMedGoogle Scholar
  68. Ivakov A, Persson S (2012) Plant cell walls. eLS. Wiley, pp 1–17 doi:  10.1002/9780470015902.a0001682.pub2
  69. Jäger G, Wulfhorst H, Zeithammel EU, Elinidou E, Spiess AC, Büchs J (2011) Screening of cellulases for biofuel production: online monitoring of the enzymatic hydrolysis of insoluble cellulose using high-throughput scattered light detection. Biotechnol J 6:74–85PubMedGoogle Scholar
  70. Jarvis MC (2012) Sclerenchyma. eLS. Wiley, pp 1–3 doi:  10.1002/9780470015902.a0002082.pub2
  71. Jeoh T, Ishizawa CI, Davis MF, Himmel ME, Adney WS, Johnson DK (2007) Cellulase digestibility of pretreated biomass is limited by cellulose accessibility. Biotechnol Bioeng 98:112–122PubMedGoogle Scholar
  72. Jung H-JG, Samac DA, Sarath G (2012) Modifying crops to increase cell wall digestibility. Plant Sci 185–186:65–77PubMedGoogle Scholar
  73. Kabel MA, van den Borne H, Vincken J-P, Voragen AGJ, Schols HA (2007) Structural differences of xylans affect their interaction with cellulose. Carbohydr Polym 69:94–105Google Scholar
  74. Karlsson O, Ikeda T, Kishimoto T, Magara K, Matsumoto Y, Hosoya S (2004) Isolation of lignin–carbohydrate bonds in wood. Model experiments and preliminary application to pine wood. J Wood Sci 50:141–150Google Scholar
  75. Karlsson O, Lundquist K, Meuller S, Westlid K (1988) On the acidolytic cleavage of arylglycerol β-aryl ethers. Acta Chem Scand B 42:48–51Google Scholar
  76. Keskar SS, Edye LA, Doherty WOS, Bartley JP (2011) The chemistry of acid catalyzed delignification of sugarcane bagasse in the ionic liquid trihexyl tetradecyl phosphonium chloride. J Wood Chem Technol 32:71–81Google Scholar
  77. Kim H, Ralph J (2010) Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5. Org Biomol Chem 8:576–591PubMedGoogle Scholar
  78. Kim Y, Mosier NS, Ladisch MR, Ramesh Pallapolu V, Lee YY, Garlock R et al (2011) Comparative study on enzymatic digestibility of switchgrass varieties and harvests processed by leading pretreatment technologies. Bioresour Technol 102:11089–11096PubMedGoogle Scholar
  79. Kimon KS, Leslie Alan E, William Orlando Sinclair D (2011) Enhanced saccharification kinetics of sugarcane bagasse pretreated in 1-butyl-3-methylimidazolium chloride at high temperature and without complete dissolution. Bioresour Technol 102:9325–9329PubMedGoogle Scholar
  80. King AWT, Parviainen A, Karhunen P, Matikainen J, Hauru LKJ, Sixta H et al (2012) Relative and inherent reactivities of imidazolium-based ionic liquids: the implications for lignocellulose processing applications. RSC Adv 2:8020–8026Google Scholar
  81. Kishimoto T, Chiba W, Saito K, Fukushima K, Uraki Y, Ubukata M (2009) Influence of syringyl to guaiacyl ratio on the structure of natural and synthetic lignins. J Agric Food Chem 58:895–901Google Scholar
  82. Knill CJ, Kennedy JF (2003) Degradation of cellulose under alkaline conditions. Carbohydr Polym 51:281–300Google Scholar
  83. Koo B-W, Min B-C, Gwak K-S, Lee S-M, Choi J-W, Yeo H et al (2012) Structural changes in lignin during organosolv pretreatment of Liriodendron tulipifera and the effect on enzymatic hydrolysis. Biomass Bioenerg 42:24–32Google Scholar
  84. Kumar R, Mago G, Balan V, Wyman CE (2009) Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies. Bioresour Technol 100:3948–3962PubMedGoogle Scholar
  85. Larsen SU, Bruun S, Lindedam J (2012) Straw yield and saccharification potential for ethanol in cereal species and wheat cultivars. Biomass Bioenerg 45:239–250Google Scholar
  86. Lawoko M, Henriksson G, Gellerstedt G (2006) Characterisation of lignin-carbohydrate complexes (LCCs) of spruce wood (Picea abies L.) isolated with two methods. Holzforschung 60:156–161Google Scholar
  87. Le Ngoc Huyen T, Rémond C, Dheilly RM, Chabbert B (2010) Effect of harvesting date on the composition and saccharification of Miscanthus x giganteus. Bioresour Technol 101:8224–8231Google Scholar
  88. Lee C, Teng Q, Huang W, Zhong R, Ye Z-H (2009) Down-regulation of PoGT47C expression in poplar results in a reduced glucuronoxylan content and an increased wood digestibility by cellulase. Plant Cell Physiol 50:1075–1089PubMedGoogle Scholar
  89. Li W, Sun N, Stoner B, Jiang X, Lu X, Rogers RD (2011) Rapid dissolution of lignocellulosic biomass in ionic liquids using temperatures above the glass transition of lignin. Green Chem 13:2038–2047Google Scholar
  90. Li X, Ximenes E, Kim Y, Slininger M, Meilan R, Ladisch M et al (2010) Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment. Biotechnol Biofuel 3(27):1–7Google Scholar
  91. Liang H, Frost CJ, Wei X, Brown NR, Carlson JE, Tien M (2008) Improved sugar release from lignocellulosic material by introducing a tyrosine-rich cell wall peptide gene in poplar. CLEAN–Soil, Air, Water 36:662–668Google Scholar
  92. Lindedam J, Andersen SB, DeMartini J, Bruun S, Jørgensen H, Felby C et al (2012) Cultivar variation and selection potential relevant to the production of cellulosic ethanol from wheat straw. Biomass Bioenerg 37:221–228Google Scholar
  93. Lindedam J, Bruun S, Jorgensen H, Felby C, Magid J (2010) Cellulosic ethanol: Interactions between cultivar and enzyme loading in wheat straw processing. Biotechnol Biofuel 3(25):1–10Google Scholar
  94. Lionetti V, Francocci F, Ferrari S, Volpi C, Bellincampi D, Galletti R et al (2010) Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. PNAS 107:616–621PubMedGoogle Scholar
  95. Lundquist K (1973) Acid degradation of lignin. Part VIII. Low molecular weight phenols from acidolysis of birch lignin. Acta Chem Scand 27:2597–2606Google Scholar
  96. Lundquist K, Lundgren R (1972) Acid degradation of lignin. Part VII. The cleavage of ether bonds. Acta Chem Scand 26:2005–2023Google Scholar
  97. MacFarlane DR, Pringle JM, Johansson KM, Forsyth SA, Forsyth M (2006) Lewis base ionic liquids. Chem Commun, 1905–1917, doi:  10.1039/B516961P
  98. Maloney MT, Chapman TW, Baker AJ (1985) Dilute acid hydrolysis of paper birch: kinetics studies of xylan and acetyl-group hydrolysis. Biotechnol Bioeng 27:355–361PubMedGoogle Scholar
  99. Maloney VJ, Mansfield SD (2010) Characterization and varied expression of a membrane-bound endo-β-1,4-glucanase in hybrid poplar. Plant Biotechnol J 8:294–307PubMedGoogle Scholar
  100. McGee JK, April GC (1982) Chemicals from renewable resources: hemicellulose behavior during organosolv delignification of southern yellow pine. Chem Eng Commun 19:49–56Google Scholar
  101. Mechin V, Argillier O, Rocher F, Hebert Y, Mila I, Pollet B et al (2005) In search of a maize ideotype for cell wall enzymatic degradability using histological and biochemical lignin characterization. J Agric Food Chem 53:5872–5881PubMedGoogle Scholar
  102. Moller I, Sørensen I, Bernal AJ, Blaukopf C, Lee K, Øbro J et al (2007) High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J 50:1118–1128PubMedGoogle Scholar
  103. Morreel K, Dima O, Kim H, Lu F, Niculaes C, Vanholme R et al (2010) Mass spectrometry-based sequencing of lignin oligomers. Plant Physiol 153:1464–1478PubMedGoogle Scholar
  104. Muhammad N, Omar WN, Man Z, Bustam MA, Rafiq S, Uemura Y (2012) Effect of ionic liquid treatment on pyrolysis products from bamboo. Ind Eng Chem Res 51:2280–2289Google Scholar
  105. Ong RG (2011) Interactions between biomass feedstock characteristics and bioenergy production: from the landscape to the molecular scale, PhD., Michigan State University, USAGoogle Scholar
  106. Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA, Popper Z et al (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153:514–525PubMedGoogle Scholar
  107. Pauly M, Hake S, Kraemer FJ (2011) Maize variety and method of production. US Patent 13/152,219, Filed 2 Jun 2011Google Scholar
  108. Pedersen M, Meyer AS (2010) Lignocellulose pretreatment severity—relating pH to biomatrix opening. New Biotechnol 27:739–750Google Scholar
  109. Pordesimo LO, Hames BR, Sokhansanj S, Edens WC (2005) Variation in corn stover composition and energy content with crop maturity. Biomass Bioenerg 28:366–374Google Scholar
  110. Ralph J, Brunow G, Boerjan W (2007) Lignins. eLS. Wiley, pp 1–10, doi:  10.1002/9780470015902.a0020104
  111. Rencoret J, Gutiérrez A, Nieto L, Jiménez-Barbero J, Faulds CB, Kim H et al (2011) Lignin composition and structure in young versus adult Eucalyptus globulus plants. Plant Physiol 155:667–682PubMedGoogle Scholar
  112. Riedlberger P, Weuster-Botz D (2012) New miniature stirred-tank bioreactors for parallel study of enzymatic biomass hydrolysis. Bioresour Technol 106:138–146PubMedGoogle Scholar
  113. Rock K, Thelemann R, Jung H-J, Tschirner U, Sheaffer C, Johnson G (2009) Variation due to growth environment in alfalfa yield, cellulosic ethanol traits, and paper pulp characteristics. Bioenerg Res 2:79–89Google Scholar
  114. Rollin JA, Zhu Z, Sathitsuksanoh N, Zhang YHP (2011) Increasing cellulose accessibility is more important than removing lignin: a comparison of cellulose solvent-based lignocellulose fractionation and soaking in aqueous ammonia. Biotechnol Bioeng 108:22–30PubMedGoogle Scholar
  115. Saake B, Lehnen R (2007) Lignin. In: Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH, doi:10.1002/14356007.a15_305.pub3 Google Scholar
  116. Sanjaya Durrett TP, Weise SE, Benning C (2011) Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol J 9:874–883PubMedGoogle Scholar
  117. Sannigrahi P, Ragauskas AJ, Miller SJ (2009) Lignin structural modifications resulting from ethanol organosolv treatment of loblolly pine. Energ Fuel 24:683–689Google Scholar
  118. Santoro N, Cantu S, Tornqvist C-E, Falbel T, Bolivar J, Patterson S et al (2010) A high-throughput platform for screening milligram quantities of plant biomass for lignocellulose digestibility. Bioenerg Res 3:93–102Google Scholar
  119. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedGoogle Scholar
  120. Selig M, Tucker M, Law C, Doeppke C, Himmel M, Decker S (2011) High throughput determination of glucan and xylan fractions in lignocelluloses. Biotechnol Lett 33:961–967PubMedGoogle Scholar
  121. Selig MJ, Tucker MP, Sykes RW, Reichel KL, Brunecky R, Himmel ME et al (2010) Lignocellulose recalcitrance screening by integrated high-throughput hydrothermal pretreatment and enzymatic saccharification. Ind Biotechnol 6:104–111Google Scholar
  122. Sewalt VJH, Fontenot JP, Allen VG, Glasser WG (1996) Fiber composition and in vitro digestibility of corn stover fractions in response to ammonia treatment. J Agric Food Chem 44:3136–3142Google Scholar
  123. Shen H, He X, Poovaiah CR, Wuddineh WA, Ma J, Mann DGJ et al (2012) Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks. New Phytol 193:121–136PubMedGoogle Scholar
  124. Shi J, Ebrik MA, Yang B, Garlock RJ, Balan V, Dale BE et al (2011) Application of cellulase and hemicellulase to pure xylan, pure cellulose, and switchgrass solids from leading pretreatments. Bioresour Technol 102:11080–11088PubMedGoogle Scholar
  125. Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol R 70:283–295Google Scholar
  126. Simmons BA, Loqué D, Ralph J (2010) Advances in modifying lignin for enhanced biofuel production. Curr Opin Plant Biol 13:312–319Google Scholar
  127. Singh S, Simmons BA, Vogel KP (2009) Visualization of biomass solubilization and cellulose regeneration during ionic liquid pretreatment of switchgrass. Biotechnol Bioeng 104:68–75PubMedGoogle Scholar
  128. Siqueira G, Milagres A, Carvalho W, Koch G, Ferraz A (2011) Topochemical distribution of lignin and hydroxycinnamic acids in sugar-cane cell walls and its correlation with the enzymatic hydrolysis of polysaccharides. Biotechnol Biofuel 4:7Google Scholar
  129. Slocombe SP, Cornah J, Pinfield-Wells H, Soady K, Zhang Q, Gilday A et al (2009) Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol J 7:694–703PubMedGoogle Scholar
  130. Stewart JJ, Akiyama T, Chapple C, Ralph J, Mansfield SD (2009) The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol 150:621–635PubMedGoogle Scholar
  131. Sticklen M (2006) Plant genetic engineering to improve biomass characteristics for biofuels. Curr Opin Biotechnol 17:315–319PubMedGoogle Scholar
  132. Stone B (2005) Cellulose: Structure and distribution. eLS. Wiley, pp 1–8, doi:  10.1038/npg.els.0003892
  133. Studer M, Brethauer S, DeMartini J, McKenzie H, Wyman C (2011a) Co-hydrolysis of hydrothermal and dilute acid pretreated populus slurries to support development of a high-throughput pretreatment system. Biotechnol Biofuel 4(19):1–10Google Scholar
  134. Studer MH, DeMartini JD, Brethauer S, McKenzie HL, Wyman CE (2010) Engineering of a high-throughput screening system to identify cellulosic biomass, pretreatments, and enzyme formulations that enhance sugar release. Biotechnol Bioeng 105:231–238PubMedGoogle Scholar
  135. Studer MH, DeMartini JD, Davis MF, Sykes RW, Davison B, Keller M et al (2011b) Lignin content in natural Populus variants affects sugar release. PNAS 108:6300–6305PubMedGoogle Scholar
  136. Sun L, Simmons BA, Singh S (2011) Understanding tissue specific compositions of bioenergy feedstocks through hyperspectral raman imaging. Biotechnol Bioeng 108:286–295PubMedGoogle Scholar
  137. Sun Y, Cheng JJ (2005) Dilute acid pretreatment of rye straw and bermudagrass for ethanol production. Bioresour Technol 96:1599–1606PubMedGoogle Scholar
  138. Tadesse H, Luque R (2011) Advances on biomass pretreatment using ionic liquids: an overview. Energ Environ Sci 4:3913–3929Google Scholar
  139. Tarkow H, Feist WC (1969) A mechanism for improving the digestibility of lignocellulosic materials with dilute alkali and liquid ammonia. In: Hajny GJ, Reese ET (eds) Cellulases and their applications. American Chemical Society, Washington, D. C., pp 197–218Google Scholar
  140. Teymouri F, Alizadeh H, Laureano-Pérez L, Dale B, Sticklen M (2004) Effects of ammonia fiber explosion treatment on activity of endoglucanase from acidothermus cellulolyticus in transgenic plant. Appl Biochem Biotechnol 116:1183–1191Google Scholar
  141. Tunc MS, van Heiningen ARP (2008) Hemicellulose extraction of mixed southern hardwood with water at 150°C: effect of time. Ind Eng Chem Res 47:7031–7037Google Scholar
  142. Várnai A, Siika-aho M, Viikari L (2010) Restriction of the enzymatic hydrolysis of steam-pretreated spruce by lignin and hemicellulose. Enzym Microb Technol 46:185–193Google Scholar
  143. Verma D, Kanagaraj A, Jin S, Singh ND, Kolattukudy PE, Daniell H (2010) Chloroplast-derived enzyme cocktails hydrolyse lignocellulosic biomass and release fermentable sugars. Plant Biotechnol J 8:332–350PubMedGoogle Scholar
  144. Vitz J, Erdmenger T, Haensch C, Schubert US (2009) Extended dissolution studies of cellulose in imidazolium based ionic liquids. Green Chem 11:417–424Google Scholar
  145. Voelker SL, Lachenbruch B, Meinzer FC, Kitin P, Strauss SH (2011) Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival. Plant, Cell Environ 34:655–668Google Scholar
  146. Wallace G, Russell WR, Lomax JA, Jarvis MC, Lapierre C, Chesson A (1995) Extraction of phenolic-carbohydrate complexes from graminaceous cell walls. Carbohydr Res 272:41–53Google Scholar
  147. Wang PY, Bolker HI, Purves CB (1964) Ammonolysis of uronic ester groups in birch xylan. Can J Chem 42:2434–2439Google Scholar
  148. Whitney SEC, Brigham JE, Darke AH, Reid JSG, Gidley MJ (1998) Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose. Carbohydr Res 307:299–309Google Scholar
  149. Willför S, Sundberg A, Hemming J, Holborn B (2005a) Polysaccharides in selected industrially important softwood species. In: 59th appita annual conference and exhibition. Auckland, New Zealand, pp 415–422Google Scholar
  150. Willför S, Sundberg A, Pranovich A, Holborn B (2005b) Polysaccharides in some industrially important hardwood species. Wood Sci Technol 39:601–617Google Scholar
  151. Wilson JR, Hatfield RD (1997) Structural and chemical changes of cell wall types during stem development: consequences for fibre degradation by rumen microflora. Aust J Agric Res 48:165–180Google Scholar
  152. Wiman M, Dienes D, Hansen MAT, van der Meulen T, Zacchi G, Lidén G (2012) Cellulose accessibility determines the rate of enzymatic hydrolysis of steam-pretreated spruce. Bioresour Technol 126:208–215PubMedGoogle Scholar
  153. Wu H, Mora-Pale M, Miao J, Doherty TV, Linhardt RJ, Dordick JS (2011) Facile pretreatment of lignocellulosic biomass at high loadings in room temperature ionic liquids. Biotechnol Bioeng 108:2865–2875PubMedGoogle Scholar
  154. Wyman CE, Dale BE, Balan V, Elander RT, Holtzapple MT, Ramirez RS, et al (2013) Comparative performance of leading pretreatment technologies for biological conversion of corn stover, poplar wood, and switchgrass to sugars, 1st edn. In: Wyman CE (ed) Aqueous Pretreatment of Plant Biomass for Biological and Chemical Conversion to Fuels and Chemicals. Wiley, London, pp 245–265Google Scholar
  155. Xiao L-P, Shi Z-J, Xu F, Sun R-C (2013) Characterization of lignins isolated with alkaline ethanol from the hydrothermal pretreated Tamarix ramosissima. Bioenerg Res 6:1–14Google Scholar
  156. Xu H, Pan W, Wang R, Zhang D, Liu C (2012) Understanding the mechanism of cellulose dissolution in 1-butyl-3-methylimidazolium chloride ionic liquid via quantum chemistry calculations and molecular dynamics simulations. J Comput Aided Mol Des 26:329–337PubMedGoogle Scholar
  157. Zeng M, Ximenes E, Ladisch MR, Mosier NS, Vermerris W, Huang C-P et al (2012) Tissue-specific biomass recalcitrance in corn stover pretreated with liquid hot-water: enzymatic hydrolysis (Part 1). Biotechnol Bioeng 109:390–397PubMedGoogle Scholar
  158. Zhang H, Fangel JU, Willats WGT, Selig MJ, Lindedam J, Jørgensen H, et al (2013a) Assessment of leaf/stem ratio in wheat straw feedstock and impact on enzymatic conversion. GCB Bioenergy, doi:  10.1111/gcbb.12060, (Ahead of Print)
  159. Zhang H, Wu J, Zhang J, He J (2005) 1-allyl-3-methylimidazolium chloride room temperature ionic liquid: a new and powerful nonderivatizing solvent for cellulose. Macromolecules 38:8272–8277Google Scholar
  160. Zhang X, Yang W, Blasiak W (2011a) Modeling study of woody biomass: interactions of cellulose, hemicellulose, and lignin. Energ Fuel 25:4786–4795Google Scholar
  161. Zhang Y, Culhaoglu T, Pollet B, Melin C, Denoue D, Barrière Y et al (2011b) Impact of lignin structure and cell wall reticulation on maize cell wall degradability. J Agric Food Chem 59:10129–10135PubMedGoogle Scholar
  162. Zhang Z, O’Hara IM, Doherty WOS (2013b) Effects of pH on pretreatment of sugarcane bagasse using aqueous imidazolium ionic liquids. Green Chem 15:431–438Google Scholar
  163. Zhao X, Zhang L, Liu D (2012) Biomass recalcitrance. Part II: Fundamentals of different pre-treatments to increase the enzymatic digestibility of lignocellulose. Biofuel Bioprod Biorefin 6:561–579Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Rebecca Garlock Ong
    • 1
    • 2
  • Shishir P. S. Chundawat
    • 1
    • 2
    • 3
  • David B. Hodge
    • 1
    • 2
    • 4
    • 5
  • Sai Keskar
    • 1
    • 2
  • Bruce E. Dale
    • 1
    • 2
  1. 1.Department of Chemical Engineering and Materials ScienceMichigan State UniversityLansingUSA
  2. 2.DOE Great Lakes Bioenergy Research CenterMadisonUSA
  3. 3.Department of BiochemistryUniversity of Wisconsin–MadisonMadisonUSA
  4. 4.Department of Biosystems and Agricultural EngineeringMichigan State UniversityXXXXXX
  5. 5.Department of Civil, Environmental and Natural Resources EngineeringLuleå University of TechnologyXXXXXX

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