Lignin Depletion Enhances the Digestibility of Cellulose in Cultured Xylem Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Lacayo, Catherine I ^a   Hwang, Mona S ^a   Ding, Shi You ^b   Thelen, Michael P ^a  

^a LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^b NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFUEL; CELLULOSE; LIGNIN; LIGNOCELLULOSE;

ANGIOSPERM; ARTICLE; BIODEGRADATION; BIOGENESIS; BIOSYNTHESIS; CELL WALL; CONTROLLED STUDY; ENZYME INHIBITION; FLUORESCENCE; LIGNIFICATION; NONHUMAN; PLANT CELL; PROTEIN BINDING; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; XYLEM CELL; ZINNIA ELEGANS;

ASTERACEAE; BIOSYNTHETIC PATHWAYS; CELL CULTURE TECHNIQUES; CELL WALL; CELLULASE; CELLULOSE; DIGESTION; FLUORESCENCE; LIGNIN; TIME-LAPSE IMAGING; XYLEM;

EID: 84880414041     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068266     Document Type: Article

References (58)

1. Wei H, Xu Q, Taylor LE, Baker JO, Tucker MP, et al. (2009) Natural paradigms of plant cell wall degradation. Curr Opin Biotechnol 20: 330-338. doi:10.1016/j.copbio.2009.05.008. PubMed: 19523812.
2. Pérez J, Muñoz-Dorado J, de la Rubia T, Martínez J, (2002) Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol 5: 53-63. doi:10.1007/s10123-002-0062-3. PubMed: 12180781.
3. Klein-Marcuschamer D, Simmons BA, Blanch HW, (2011) Techno-economic analysis of a lignocellulosic ethanol biorefinery with ionic liquid pre-treatment. Biofuel Bioprod Bior 5: 562-569. doi:10.1002/bbb.303.
4. Van Dyk JS, Pletschke BI, (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes-Factors affecting enzymes, conversion and synergy. Biotechnol Adv 30: 1458-1480. doi:10.1016/j.biotechadv.2012.03.002. PubMed: 22445788.
5. Hendriks ATWM, Zeeman G, (2009) Pretreatments to enhance the digestibility of lignocellulosic biomass. Bioresour Technol 100: 10-18. doi:10.1016/j.biortech.2008.05.027. PubMed: 18599291.
6. Grethlein HE, Allen DC, Converse AO, (1984) A comparative study of the enzymatic hydrolysis of acid-pretreated white pine and mixed hardwood. Biotechnol Bioeng 26: 1498-1505. doi:10.1002/bit.260261215. PubMed: 18551682.
7. Hubbell CA, Ragauskas AJ, (2010) Effect of acid-chlorite delignification on cellulose degree of polymerization. Bioresour Technol 101: 7410-7415. doi:10.1016/j.biortech.2010.04.029. PubMed: 20471250.
8. Kumar L, Arantes V, Chandra R, Saddler J, (2012) The lignin present in steam pretreated softwood binds enzymes and limits cellulose accessibility. Bioresour Technol 103: 201-208. doi:10.1016/j.biortech.2011.09.091. PubMed: 22047660.
9. Palonen H, Tjerneld F, Zacchi G, Tenkanen M, (2004) Adsorption of Trichoderma reesei CBH I and EG II and their catalytic domains on steam pretreated softwood and isolated lignin. J Biotechnol 107: 65-72. doi:10.1016/j.jbiotec.2003.09.011. PubMed: 14687972.
10. Henmi K, Demura T, Tsuboi S, Fukuda H, Iwabuchi M, et al. (2005) Change in the redox state of glutathione regulates differentiation of tracheary elements in Zinnia cells and Arabidopsis roots. Plant Cell Physiol 46: 1757-1765. doi:10.1093/pcp/pci198. PubMed: 16301210.
11. Karlsson M, Melzer M, Prokhorenko I, Johansson T, Wingsle G, (2005) Hydrogen peroxide and expression of hipI-superoxide dismutase are associated with the development of secondary cell walls in Zinnia elegans. J Exp Bot 56: 2085-2093. doi:10.1093/jxb/eri207. PubMed: 15955789.
12. Ros Barceló A, (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207: 207-216. doi:10.1007/s004250050474.
13. Mansfield SD, Mooney C, Saddler JN, (1999) Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol Prog 15: 804-816. doi:10.1021/bp9900864. PubMed: 10514250.
14. Burton RA, Gidley MJ, Fincher GB, (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6: 724-732. doi:10.1038/nchembio.439. PubMed: 20852610.
15. Fukuda H, (1996) Xylogenesis: Initiation, progression, and cell death. Annu Rev Plant Physiol 47: 299-325. doi:10.1146/annurev.arplant.47.1.299. PubMed: 15012291.
16. Fukuda H, Komamine A, (1982) Lignin synthesis and its related enzymes as markers of tracheary element differentiation in single cells isolated from the mesophyll of Zinnia elegans. Planta 155: 423-430. doi:10.1007/BF00394471.
17. Falconer MM, Seagull RW, (1985) Immunofluorescent and calcofluor white staining of developing tracheary elements in Zinnia elegans L. suspension cultures. Protoplasma 125: 190-198. doi:10.1007/BF01281237.
18. Lacayo CI, Malkin AJ, Holman HY, Chen L, Ding SY, et al. (2010) Imaging cell wall architecture in single Zinnia elegans tracheary elements. Plant Physiol 154: 121-133. doi:10.1104/pp.110.155242. PubMed: 20592039.
19. Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W, (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47: 239-274. doi:10.1023/A:1010699919325. PubMed: 11554475.
20. Turner S, Gallois P, Brown D, (2007) Tracheary element differentiation. Annu Rev Plant Biol 58: 407-433. doi:10.1146/annurev.arplant.57.032905.105236. PubMed: 17472568.
21. Medie FM, Davies GJ, Drancourt M, Henrissat B, (2012) Genome analyses highlight the different biological roles of cellulases. Nat Rev Microbiol 10: 227-234. doi:10.1038/nrmicro2729. PubMed: 22266780.
22. Ding SY, Himmel ME, (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. Agric Food Chem 54: 597-606. doi:10.1021/jf051851z. PubMed: 16448156.
23. Eudes A, George A, Mukerjee P, Kim JS, Pollet B, et al. (2012) Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification. Plant Biotechnol J 10: 609-620. doi:10.1111/j.1467-7652.2012.00692.x. PubMed: 22458713.
24. Fu CX, Mielenz JR, Xiao XR, Ge YX, Hamilton CY, et al. (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci U S A 108: 3803-3808. doi:10.1073/pnas.1100310108. PubMed: 21321194.
25. Reddy MSS, Chen F, Shadle G, Jackson L, Aljoe H, et al. (2005) Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.). Proc Natl Acad Sci U S A 102: 16573-16578. doi:10.1073/pnas.0505749102. PubMed: 16263933.
26. Leavitt SW, Danzer SR, (1993) Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 65: 87-89. doi:10.1021/ac00051a703.
27. Ding SY, Xu Q, Ali MK, Baker JO, Bayer EA, et al. (2006) Versatile derivatives of carbohydrate-binding modules for imaging of complex carbohydrates approaching the molecular level of resolution. BioTechniques 41: 435-442. doi:10.2144/000112244. PubMed: 17068959.
28. Clarke ND, (2010) Protein engineering for bioenergy and biomass-based chemicals. Curr Opin Struct Biol 20: 527-532. doi:10.1016/j.sbi.2010.06.001. PubMed: 20591648.
29. Ding SY, Liu YS, Zeng Y, Himmel ME, Baker JO, et al. (2012) How does plant cell wall nanoscale architecture correlate with enzymatic digestibility? Science 338: 1055-1060. doi:10.1126/science.1227491. PubMed: 23180856.
30. Jung HJG, Jorgensen MA, Linn JG, Engels FM, (2000) Impact of accessibility and chemical composition on cell wall polysaccharide degradability of maize and lucerne stems. J Sci Food Agric 80: 419-427. doi:10.1002/1097-0010(200002)80:3.
31. Mooney CA, Mansfield SD, Touhy MG, Saddler JN, (1998) The effect of initial pore volume and lignin content on the enzymatic hydrolysis of softwoods. Bioresour Technol 64: 113-119. doi:10.1016/S0960-8524(97)00181-8.
32. Cosgrove DJ, (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850-861. doi:10.1038/nrm1746. PubMed: 16261190.
33. Bura R, Chandra R, Saddler J, (2009) Influence of xylan on the enzymatic hydrolysis of steam-pretreated corn stover and hybrid poplar. Biotechnol Prog 25: 315-322. doi:10.1002/btpr.98. PubMed: 19266561.
34. Yang B, Wyman CE, (2004) Effect of xylan and lignin removal by batch and flowthrough pretreatment on the enzymatic digestibility of corn stover cellulose. Biotechnol Bioeng 86: 88-95. doi:10.1002/bit.20043. PubMed: 15007845.
35. Ahlgren PA, Goring DAI, (1971) Removal of wood components during chlorite delignification of black spruce. Can J Chem 49: 1272-1275. doi:10.1139/v71-207.
36. Yoshida M, Liu Y, Uchida S, Kawarada K, Ukagami Y, et al. (2008) Effects of cellulose crystallinity, hemicellulose, and lignin on the enzymatic hydrolysis of Miscanthus sinensis to monosaccharides. Biosci Biotechnol Biochem 72: 805-810. doi:10.1271/bbb.70689. PubMed: 18323635.
37. Puri VP, (1984) Effect of crystallinity and degree of polymerization of cellulose on enzymatic saccharification. Biotechnol Bioeng 26: 1219-1222. doi:10.1002/bit.260261010. PubMed: 18551639.
38. Hong J, Ye XH, Zhang YHP, (2007) Quantitative determination of cellulose accessibility to cellulase based on adsorption of a nonhydrolytic fusion protein containing CBM and GFP with its applications. Langmuir 23: 12535-12540. doi:10.1021/la7025686. PubMed: 17988165.
39. Jeoh T, Ishizawa CI, Davis MF, Himmel ME, Adney WS, et al. (2007) Cellulase digestibility of pretreated biomass is limited by cellulose accessibility. Biotechnol Bioeng 98: 112-122. doi:10.1002/bit.21408. PubMed: 17335064.
40. Zhu ZG, Sathitsuksanoh N, Vinzant T, Schell DJ, McMillan JD, et al. (2009) Comparative study of corn stover pretreated by dilute acid and cellulose solvent-based lignocellulose fractionation: enzymatic hydrolysis, supramolecular structure, and substrate accessibility. Biotechnol Bioeng 103: 715-724. doi:10.1002/bit.22307. PubMed: 19337984.
41. Rollin JA, Zhu ZG, 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: 22-30. doi:10.1002/bit.22919. PubMed: 20812260.
42. Grabber JH, (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci 45: 820-831. doi:10.2135/cropsci2004.0191.
43. Piquemal J, Lapierre C, Myton K, O'Connell A, Schuch W, et al. (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J 13: 71-83.
44. Ralph J, Hatfield RD, Piquemal J, Yahiaoui N, Pean M, et al. (1998) NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamyl-alcohol dehydrogenase and cinnamoyl-CoA reductase. Proc Natl Acad Sci U S A 95: 12803-12808. doi:10.1073/pnas.95.22.12803. PubMed: 9788995.
45. Grabber JH, Ralph J, Hatfield RD, (1998) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J Agr Foods Chem 46: 2609-2614. doi:10.1021/jf9800099.
46. Kumar L, Chandra R, Saddler J, (2011) Influence of steam pretreatment severity on post-treatments used to enhance the enzymatic hydrolysis of pretreated softwoods at low enzyme loadings. Biotechnol Bioeng 108: 2300-2311. doi:10.1002/bit.23185. PubMed: 21520024.
47. Knox JP, (2008) Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol 11: 308-313. doi:10.1016/j.pbi.2008.03.001. PubMed: 18424171.
48. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ, (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382: 769-781. doi:10.1042/BJ20040892. PubMed: 15214846.
49. Boraston AB, Nurizzo D, Notenboom V, Ducros V, Rose DR, et al. (2002) Differential oligosaccharide recognition by evolutionarily-related β-1,4 and β-1,3 glucan-binding modules. J Mol Biol 319: 1143-1156. doi:10.1016/S0022-2836(02)00374-1. PubMed: 12079353.
50. McCartney L, Gilbert HJ, Bolam DN, Boraston AB, Knox JP, (2004) Glycoside hydrolase carbohydrate-binding modules as molecular probes for the analysis of plant cell wall polymers. Anal Biochem 326: 49-54. doi:10.1016/j.ab.2003.11.011. PubMed: 14769335.
51. Linder M, Winiecka-Krusnell J, Linder E, (2002) Use of recombinant cellulose-binding domains of Trichoderma reesei cellulase as a selective immunocytochemical marker for cellulose in protozoa. Appl Environ Microbiol 68: 2503-2508. doi:10.1128/AEM.68.5.2503-2508.2002. PubMed: 11976127.
52. Blake AW, Marcus SE, Copeland JE, Blackburn RS, Knox JP, (2008) In situ analysis of cell wall polymers associated with phloem fibre cells in stems of hemp, Cannabis sativa L. Planta 228: 1-13. doi:10.1007/s00425-008-0713-5. PubMed: 18299887.
53. Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA, et al. (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153: 514-525. doi:10.1104/pp.109.151985. PubMed: 20363856.
54. Ishizawa CI, Jeoh T, Adney WS, Himmel ME, Johnson DK, et al. (2009) Can delignification decrease cellulose digestibility in acid pretreated corn stover? Cellulose 16: 677-686. doi:10.1007/s10570-009-9313-1.
55. Wood PJ, Fulcher RG, Stone BA, (1983) Studies on the specificity of interaction of cereal cell wall components with Congo Red and Calcofluor. Specific Detect Histochemistry of: pp. 1-3,(1-4),-β-D-glucan. J Cereal Sci 1: 95-110.
56. Roberts AW, Koonce LT, Haigler CH, (1992) A simplified medium for in vitro tracheary element differentiation in mesophyll suspension cultures from Zinnia elegans L. Plants Cell Tiss Org 28: 27-35. doi:10.1007/BF00039912.
57. Blanchette C, Lacayo CI, Fischer, Hwang M, Thelen MP, (2012) Enhanced cellulose degradation using cellulase-nanosphere complexes. PLOS ONE 7(8):: e42116. doi:10.1371/journal.pone.0042116. PubMed: 22870287.
58. Porter SE, Donohoe BS, Beery KE, Xu Q, Ding SY, et al. (2007) Microscopic analysis of corn fiber using starch- and cellulose-specific molecular probes. Biotechnol Bioeng 98: 123-131. doi:10.1002/bit.21409. PubMed: 17335065.