Biomass recalcitrance: a multi-scale, multi-factor, and conversion-specific property.

Recalcitrance of plant biomass to enzymatic hydrolysis for biofuel production is thought to be a property conferred by lignin or lignin-carbohydrate complexes. However, chemical catalytic and thermochemical conversion pathways, either alone or in combination with biochemical and fermentative pathways, now provide avenues to utilize lignin and to expand the product range beyond ethanol or butanol. To capture all of the carbon in renewable biomass, both lignin-derived aromatics and polysaccharide-derived sugars need to be transformed by catalysts to liquid hydrocarbons and high-value co-products. We offer a new definition of recalcitrance as those features of biomass which disproportionately increase energy requirements in conversion processes, increase the cost and complexity of operations in the biorefinery, and/or reduce the recovery of biomass carbon into desired products. The application of novel processing technologies applied to biomass reveal new determinants of recalcitrance that comprise a broad range of molecular, nanoscale, and macroscale factors. Sampling natural genetic diversity within a species, transgenic approaches, and synthetic biology approaches are all strategies that can be used to select biomass for reduced recalcitrance in various pretreatments and conversion pathways.

[1]  John Ralph,et al.  The Effects on Lignin Structure of Overexpression of Ferulate 5-Hydroxylase in Hybrid Poplar1[W] , 2009, Plant Physiology.

[2]  C. Wyman,et al.  Features of promising technologies for pretreatment of lignocellulosic biomass. , 2005, Bioresource technology.

[3]  H. Höfte,et al.  Novel receptor kinases involved in growth regulation. , 2008, Current opinion in plant biology.

[4]  Rakesh Agrawal,et al.  High-pressure fast-pyrolysis, fast-hydropyrolysis and catalytic hydrodeoxygenation of cellulose: production of liquid fuel from biomass , 2014 .

[5]  Hengfu Yin,et al.  Systems and synthetic biology approaches to alter plant cell walls and reduce biomass recalcitrance , 2014, Plant biotechnology journal.

[6]  C. Chapple,et al.  The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. , 2002, The Plant journal : for cell and molecular biology.

[7]  Michael R. Ladisch,et al.  Molecular breeding to enhance ethanol production from corn and sorghum stover. , 2007 .

[8]  R. Zhong,et al.  The Arabidopsis DUF231 domain-containing protein ESK1 mediates 2-O- and 3-O-acetylation of xylosyl residues in xylan. , 2013, Plant & cell physiology.

[9]  N. Carpita,et al.  Maize and sorghum: genetic resources for bioenergy grasses. , 2008, Trends in plant science.

[10]  Joseph J. Bozell,et al.  Connecting Biomass and Petroleum Processing with a Chemical Bridge , 2010, Science.

[11]  G. Eggink,et al.  Disruption of the acetate kinase (ack) gene of Clostridium acetobutylicum results in delayed acetate production , 2012, Applied Microbiology and Biotechnology.

[12]  D. Mohan,et al.  Pyrolysis of Wood/Biomass for Bio-oil: A Critical Review , 2006 .

[13]  J. Keasling,et al.  From fields to fuels: recent advances in the microbial production of biofuels. , 2012, ACS synthetic biology.

[14]  R. Zhong,et al.  Arabidopsis irregular xylem8 and irregular xylem9: Implications for the Complexity of Glucuronoxylan Biosynthesis[W] , 2007, The Plant Cell Online.

[15]  F. Ribeiro,et al.  Cleavage and hydrodeoxygenation (HDO) of C–O bonds relevant to lignin conversion using Pd/Zn synergistic catalysis , 2013 .

[16]  V. T. Forsyth,et al.  Nanostructure of cellulose microfibrils in spruce wood , 2011, Proceedings of the National Academy of Sciences.

[17]  R. Newman,et al.  Conformational features of crystal-surface cellulose from higher plants. , 2002, The Plant journal : for cell and molecular biology.

[18]  C. Wilkerson,et al.  Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone , 2014, Science.

[19]  T. Ezeji,et al.  Bioproduction of butanol from biomass: from genes to bioreactors. , 2007, Current opinion in biotechnology.

[20]  Maureen C. McCann,et al.  Direct visualization of cross-links in the primary plant cell wall , 1990 .

[21]  David M Brown,et al.  GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. , 2013, The Plant journal : for cell and molecular biology.

[22]  N. Carpita.  STRUCTURE AND BIOGENESIS OF THE CELL WALLS OF GRASSES. , 1996, Annual review of plant physiology and plant molecular biology.

[23]  M. Defernez,et al.  Cell wall architecture of the elongating maize coleoptile. , 2001, Plant physiology.

[24]  J. O. Baker,et al.  How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility? , 2012, Science.

[25]  Gerald A. Tuskan,et al.  Lignin Valorization: Improving Lignin Processing in the Biorefinery , 2014, Science.

[26]  Mark F. Davis,et al.  Lignin content in natural Populus variants affects sugar release , 2011, Proceedings of the National Academy of Sciences.

[27]  Sang Yup Lee,et al.  Metabolic Engineering of Clostridium acetobutylicum ATCC 824 for Isopropanol-Butanol-Ethanol Fermentation , 2011, Applied and Environmental Microbiology.

[28]  C. Lloyd.  The Cytoskeletal basis of plant growth and form , 1991 .

[29]  M. Himmel,et al.  Visualizing lignin coalescence and migration through maize cell walls following thermochemical pretreatment , 2008, Biotechnology and bioengineering.

[30]  K. Seffen,et al.  Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass , 2010, Proceedings of the National Academy of Sciences.

[31]  M. Romero,et al.  Chloride channels in stellate cells are essential for uniquely high secretion rates in neuropeptide-stimulated Drosophila diuresis , 2014, Proceedings of the National Academy of Sciences.

[32]  J. Dumesic,et al.  Hydrogen from catalytic reforming of biomass-derived hydrocarbons in liquid water , 2002, Nature.

[33]  Judith Gurney.  BP Statistical Review of World Energy , 1985 .

[34]  V. T. Forsyth,et al.  Structure and spacing of cellulose microfibrils in woody cell walls of dicots , 2014, Cellulose.

[35]  Jay D Keasling,et al.  Advanced biofuel production in microbes , 2010, Biotechnology journal.

[36]  Paul Dupree,et al.  The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana , 2014, The Plant journal : for cell and molecular biology.

[37]  Lee Makowski,et al.  Tissue specific specialization of the nanoscale architecture of Arabidopsis. , 2013, Journal of structural biology.

[38]  R. Dixon,et al.  A polymer of caffeyl alcohol in plant seeds , 2012, Proceedings of the National Academy of Sciences.

[39]  Marilyn F. Slininger,et al.  Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment , 2010, Biotechnology for biofuels.

[40]  J. Estevez,et al.  Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase , 2012, Proceedings of the National Academy of Sciences.

[41]  S. Hill,et al.  Wide-Angle X-Ray Scattering and Solid-State Nuclear Magnetic Resonance Data Combined to Test Models for Cellulose Microfibrils in Mung Bean Cell Walls1 , 2013, Plant Physiology.

[42]  C. Chapple,et al.  Significant increases in pulping efficiency in C4H-F5H-transformed poplars: improved chemical savings and reduced environmental toxins. , 2003, Journal of agricultural and food chemistry.

[43]  Henrik Vibe Scheller,et al.  Reduced Wall Acetylation Proteins Play Vital and Distinct Roles in Cell Wall O-Acetylation in Arabidopsis1[C][W][OPEN] , 2013, Plant Physiology.

[44]  J. Pedersen,et al.  Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues , 2010 .

[45]  Mark F. Davis,et al.  Genetic Determinants for Enzymatic Digestion of Lignocellulosic Biomass Are Independent of Those for Lignin Abundance in a Maize Recombinant Inbred Population1[W][OPEN] , 2014, Plant Physiology.

[46]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[47]  J. Pronk,et al.  The Ehrlich Pathway for Fusel Alcohol Production: a Century of Research on Saccharomyces cerevisiae Metabolism , 2008, Applied and Environmental Microbiology.

[48]  John Ralph,et al.  Lignin Biosynthesis and Structure1 , 2010, Plant Physiology.

[49]  M. Auer,et al.  Plant cell walls throughout evolution: towards a molecular understanding of their design principles. , 2009, Journal of experimental botany.

[50]  Emre Gençer,et al.  A synergistic biorefinery based on catalytic conversion of lignin prior to cellulose starting from lignocellulosic biomass , 2015 .

[51]  J. Houghton,et al.  Breaking the Biological Barriers to Cellulosic Ethanol: A Joint Research Agenda , 2006 .

[52]  James C Liao,et al.  Next generation biofuel engineering in prokaryotes. , 2013, Current opinion in chemical biology.

[53]  R. Zhong,et al.  Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. , 2010, Trends in plant science.

[54]  Linan Yang,et al.  From furfural to fuel: synthesis of furoins by organocatalysis and their hydrodeoxygenation by cascade catalysis. , 2014, ChemSusChem.

[55]  J. Keasling,et al.  Microbial production of fatty-acid-derived fuels and chemicals from plant biomass , 2010, Nature.

[56]  R. Zhong,et al.  The four Arabidopsis reduced wall acetylation genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. , 2011, Plant & cell physiology.

[57]  A deep transcriptomic analysis of pod development in the vanilla orchid (Vanilla planifolia) , 2014, BMC Genomics.

[58]  Sandra Pelletier,et al.  A Receptor-like Kinase Mediates the Response of Arabidopsis Cells to the Inhibition of Cellulose Synthesis , 2007, Current Biology.

[59]  Peter J. Bradbury,et al.  Genome-wide association study of leaf architecture in the maize nested association mapping population , 2011, Nature Genetics.

[60]  L. Donaldson.  Cellulose microfibril aggregates and their size variation with cell wall type , 2007, Wood Science and Technology.

[61]  V. T. Forsyth,et al.  Structure of Cellulose Microfibrils in Primary Cell Walls from Collenchyma1[C][W][OA] , 2012, Plant Physiology.

[62]  N. Mosier,et al.  Selective Conversion of Biomass Hemicellulose to Furfural Using Maleic Acid with Microwave Heating , 2012 .

[63]  Peter N. Ciesielski,et al.  Engineering Plant Cell Walls: Tuning Lignin Monomer Composition for Deconstructable Biofuel Feedstocks or Resilient Biomaterials , 2014 .

[64]  Johnathan E. Holladay,et al.  Top Value Added Chemicals From Biomass. Volume 1 - Results of Screening for Potential Candidates From Sugars and Synthesis Gas , 2004 .

[65]  P. Marriott,et al.  Range of cell-wall alterations enhance saccharification in Brachypodium distachyon mutants , 2014, Proceedings of the National Academy of Sciences.

[66]  Philip J. Harris,et al.  The polysaccharide composition of Poales cell walls: Poaceae cell walls are not unique , 1999 .

[67]  Rodrigo L. Silveira,et al.  Plant biomass recalcitrance: effect of hemicellulose composition on nanoscale forces that control cell wall strength. , 2013, Journal of the American Chemical Society.

[68]  Johnathan E. Holladay,et al.  Studying cellulose fiber structure by SEM, XRD, NMR and acid hydrolysis , 2007 .

[69]  W. Vermerris,et al.  Allelic Association, Chemical Characterization and Saccharification Properties of brown midrib Mutants of Sorghum (Sorghum bicolor (L.) Moench) , 2008, BioEnergy Research.

[70]  K. Wilkie.  The Hemicelluloses of Grasses and Cereals , 1979 .

[71]  Cheng-Ting Yeh,et al.  Genic and nongenic contributions to natural variation of quantitative traits in maize , 2012, Genome research.

[72]  N. Carpita,et al.  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. , 1993, The Plant journal : for cell and molecular biology.

[73]  T. Demura,et al.  Regulation of plant biomass production. , 2010, Current opinion in plant biology.

[74]  Michael Ladisch,et al.  Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant , 2014, Nature.

[75]  M. Auer,et al.  Engineering secondary cell wall deposition in plants , 2012, Plant biotechnology journal.

[76]  Changwei Hu,et al.  Conversion of glucose into furans in the presence of AlCl3 in an ethanol-water solvent system. , 2012, Bioresource technology.

[77]  Helmut Lieth,et al.  Primary Production of the Major Vegetation Units of the World , 1975 .

[78]  Peter N. Ciesielski,et al.  Transgenic ferritin overproduction enhances thermochemical pretreatments in Arabidopsis , 2015 .

[79]  Charles E. Wyman,et al.  Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass , 2013 .

[80]  Vincenzo Lionetti,et al.  Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion , 2009, Proceedings of the National Academy of Sciences.

[81]  Rakesh Agrawal,et al.  Sustainable fuel for the transportation sector , 2007, Proceedings of the National Academy of Sciences.

[82]  John Ralph,et al.  Advances in modifying lignin for enhanced biofuel production. , 2010, Current opinion in plant biology.

[83]  William S York,et al.  Biochemical control of xylan biosynthesis - which end is up? , 2008, Current opinion in plant biology.

[84]  C. Chapple,et al.  The genetics of lignin biosynthesis: connecting genotype to phenotype. , 2010, Annual review of genetics.

[85]  N. Carpita,et al.  Maize Brittle stalk2 Encodes a COBRA-Like Protein Expressed in Early Organ Development But Required for Tissue Flexibility at Maturity1[C][OA] , 2007, Plant Physiology.

[86]  G. Tuskan,et al.  Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. , 2013, The New phytologist.

[87]  R. Dixon,et al.  Transcriptional networks for lignin biosynthesis: more complex than we thought? , 2011, Trends in plant science.

[88]  Ying Zhang,et al.  Targeted mutagenesis of the Clostridium acetobutylicum acetone-butanol-ethanol fermentation pathway. , 2012, Metabolic engineering.

[89]  David K. Johnson,et al.  Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production , 2007, Science.

[90]  M. Van Montagu,et al.  Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase , 2013, Proceedings of the National Academy of Sciences.