Challenges and advances in the heterologous expression of cellulolytic enzymes: a review

Biotechnology for Biofuels

Camilla Lambertz²  Megan Garvey¹  Johannes Klinger²  Dirk Heesel²  Holger Klose⁴  Rainer Fischer³  Ulrich Commandeur² 

[1] Present address: School of Medicine, Deakin University, CSIRO Australian Animal Health Laboratory, 5 Portarlington Rd, Newcomb 3219, VIC, Australia

[2] Institute for Molecular Biotechnology, RWTH Aachen University, Worringerweg 1, Aachen, 52074, Germany

[3] Fraunhofer Institute for Molecular Biology and Applied Ecology, Forckenbeckstrasse 6, Aachen, 52074, Germany

[4] Present address: Institute for Botany and Molecular Genetics, RWTH Aachen University, Worringerweg 3, Aachen, 52074, Germany

关键词: Industrial processing;    Consolidated bioprocessing;    Cellulosome;    Heterologous expression;    Cellulase;   

Others  :  1084341
DOI  :  10.1186/s13068-014-0135-5

 received in 2014-06-05, accepted in 2014-09-03,  发布年份 2014

【 摘 要 】

Second generation biofuel development is increasingly reliant on the recombinant expression of cellulases. Designing or identifying successful expression systems is thus of preeminent importance to industrial progress in the field. Recombinant production of cellulases has been performed using a wide range of expression systems in bacteria, yeasts and plants. In a number of these systems, particularly when using bacteria and plants, significant challenges have been experienced in expressing full-length proteins or proteins at high yield. Further difficulties have been encountered in designing recombinant systems for surface-display of cellulases and for use in consolidated bioprocessing in bacteria and yeast. For establishing cellulase expression in plants, various strategies are utilized to overcome problems, such as the auto-hydrolysis of developing plant cell walls. In this review, we investigate the major challenges, as well as the major advances made to date in the recombinant expression of cellulases across the commonly used bacterial, plant and yeast systems. We review some of the critical aspects to be considered for industrial-scale cellulase production.

【 授权许可】

   
2014 Lambertz et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Bhat MK: Cellulases and related enzymes in biotechnology. Biotechnol Adv 2000, 18:355-383.
• [2]Phitsuwan P, Laohakunjit N, Kerdchoechuen O, Kyu KL, Ratanakhanokchai K: Present and potential applications of cellulases in agriculture, biotechnology, and bioenergy. Folia Microbiol (Praha) 2013, 58:163-176.
• [3]Wilson DB: Cellulases and biofuels. Curr Opin Biotechnol 2009, 20:295-299.
• [4]Van Dyk JS, Pletschke BI: A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes-factors affecting enzymes, conversion and synergy. Biotechnol Adv 2012, 30:1458-1480.
• [5]Teeri TT: Crystalline cellulose degradation: new insights into the function of cellobiohydrolases. Trends Biotechnol 1997, 15:160-167.
• [6]Medve J, Karlsson J, Lee D, Tjerneld F: Hydrolysis of microcrystalline cellulose by cellobiohydrolase I and endoglucanase II from Trichoderma reesei: adsorption, sugar production pattern, and synergism of the enzymes. Biotechnol Bioeng 1998, 59:621-634.
• [7]Zhang YHP, Himmel ME, Mielenz JR: Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv 2006, 24:452-481.
• [8]Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS: Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 2002, 66:506-577.
• [9]Watanabe H, Tokuda G: Cellulolytic systems in insects. Annu Rev Entomol 2010, 55:609-632.
• [10]Fischer R, Ostafe R, Twyman RM: Cellulases from insects. Adv Biochem Eng Biotechnol 2013, 136:51-64.
• [11]Duan CJ, Feng JX: Mining metagenomes for novel cellulase genes. Biotechnol Lett 2010, 32:1765-1775.
• [12]Bayer EA, Lamed R, Himmel ME: The potential of cellulases and cellulosomes for cellulosic waste management. Curr Opin Biotechnol 2007, 18:237-245.
• [13]Peterson R, Nevalainen H: Trichoderma reesei RUT-C30 - thirty years of strain improvement. Microbiology 2012, 158:58-68.
• [14]Gusakov AV: Alternatives to Trichoderma reesei in biofuel production. Trends Biotechnol 2011, 29:419-425.
• [15]Chundawat SP, Beckham GT, Himmel ME, Dale BE: Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu Rev Chem Biomol Eng 2011, 2:121-145.
• [16]Blouzard JC, Coutinho PM, Fierobe HP, Henrissat B, Lignon S, Tardif C, Pages S, de Philip P: Modulation of cellulosome composition in Clostridium cellulolyticum: adaptation to the polysaccharide environment revealed by proteomic and carbohydrate-active enzyme analyses. Proteomics 2010, 10:541-554.
• [17]Mazzoli R, Lamberti C, Pessione E: Engineering new metabolic capabilities in bacteria: lessons from recombinant cellulolytic strategies. Trends Biotechnol 2012, 30:111-119.
• [18]Tsai SL, Oh J, Singh S, Chen R, Chen W: Functional assembly of minicellulosomes on the Saccharomyces cerevisiae cell surface for cellulose hydrolysis and ethanol production. Appl Environ Microbiol 2009, 75:6087-6093.
• [19]Desvaux M, Hebraud M, Talon R, Henderson IR: Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol 2009, 17:139-145.
• [20]Yan S, Wu G: Secretory pathway of cellulase: a mini-review. Biotechnol Biofuels 2013, 6:177.
• [21]Jung SK, Parisutham V, Jeong SH, Lee SK: Heterologous expression of plant cell wall degrading enzymes for effective production of cellulosic biofuels. J Biomed Biotechnol 2012, 2012:405842.
• [22]Osumi M: The ultrastructure of yeast: cell wall structure and formation. Micron 1998, 29:207-233.
• [23]Bonawitz ND, Chapple C: The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 2010, 44:337-363.
• [24]Twyman RM, Stoger E, Schillberg S, Christou P, Fischer R: Molecular farming in plants: host systems and expression technology. Trends Biotechnol 2003, 21:570-578.
• [25]Stutzenberger FJ: Cellulolytic activity of Thermomonospora curvata: nutritional requirements for cellulase production. Appl Microbiol 1972, 24:77-82.
• [26]Wilson DB: Biochemistry and genetics of actinomycete cellulases. Crit Rev Biotechnol 1992, 12:45-63.
• [27]Lin E, Wilson DB: Regulation of β-1, 4-endoglucanase synthesis in Thermomonospora fusca. Appl Environ Microbiol 1987, 53:1352-1357.
• [28]Kotchoni O, Shonukan O, Gachomo W: Bacillus pumilus BpCRI 6, a promising candidate for cellulase production under conditions of catabolite repression. Afr J Biotechnol 2003, 2:140-146.
• [29]Garcia-Martinez D, Shinmyo A, Madia A, Demain A: Studies on cellulase production by Clostridium thermocellum. Eur J Appl Microbiol 1980, 9:189-197.
• [30]Liu SL, Du K: Enhanced expression of an endoglucanase in Bacillus subtilis by using the sucrose-inducible sacB promoter and improved properties of the recombinant enzyme. Protein Expres Purif 2012, 83:164-168.
• [31]Lee SJ, Pan JG, Park SH, Choi SK: Development of a stationary phase-specific autoinducible expression system in Bacillus subtilis. J Biotechnol 2010, 149:16-20.
• [32]Jakob F, Lehmann C, Martinez R, Schwaneberg U: Increasing protein production by directed vector backbone evolution. AMB Express 2013, 3:39.
• [33]Bill RM: Playing catch-up with Escherichia coli: using yeast to increase success rates in recombinant protein production experiments. Front Microbiol 2014, 5:85.
• [34]Chang JJ, Ho CY, Ho FJ, Tsai TY, Ke HM, Wang CH, Chen HL, Shih MC, Huang CC, Li WH: PGASO: A synthetic biology tool for engineering a cellulolytic yeast. Biotechnol Biofuels 2012, 5:53.
• [35]Mittendorf V, Thomson JA: Cloning of an endo-(1 → 4)-β-glucanase gene, celA, from the rumen bacterium Clostridium sp. (‘C. longisporum’) and characterization of its product, CelA, in Escherichia coli. J Gen Microbiol 1993, 139:3233-3242.
• [36]Meinke A, Gilkes N, Kilburn D, Miller R, Warren R: Multiple domains in endoglucanase B (CenB) from Cellulomonas fimi: functions and relatedness to domains in other polypeptides. J Bacteriol 1991, 173:7126-7135.
• [37]Fierobe HP, Gaudin C, Belaich A, Loutfi M, Faure E, Bagnara C, Baty D, Belaich JP: Characterization of endoglucanase A from Clostridium cellulolyticum. J Bacteriol 1991, 173:7956-7962.
• [38]Jamaluddin MJA, Salleh HM: On-column refolding of recombinant fungal endoglucanase. Aust J Basic and Appl Sci 2012, 6:128-133.
• [39]Murashima K, Kosugi A, Doi RH: Solubilization of cellulosomal cellulases by fusion with cellulose-binding domain of noncellulosomal cellulase engd from Clostridium cellulovorans. Proteins 2003, 50:620-628.
• [40]Abdeljabbar DM, Song HJ, Link AJ: Trichoderma reesei cellobiohydrolase II is associated with the outer membrane when overexpressed in Escherichia coli. Biotechnol Lett 2012, 34:91-96.
• [41]Zhang XZ, Zhang Z, Zhu Z, Sathitsuksanoh N, Yang Y, Zhang YH: The noncellulosomal family 48 cellobiohydrolase from Clostridium phytofermentans ISDg: heterologous expression, characterization, and processivity. Appl Microbiol Biotechnol 2010, 86:525-533.
• [42]Koukiekolo R, Cho HY, Kosugi A, Inui M, Yukawa H, Doi RH: Degradation of corn fiber by Clostridium cellulovorans cellulases and hemicellulases and contribution of scaffolding protein CbpA. Appl Environ Microbiol 2005, 71:3504-3511.
• [43]Mingardon F, Chanal A, Lopez-Contreras AM, Dray C, Bayer EA, Fierobe HP: Incorporation of fungal cellulases in bacterial minicellulosomes yields viable, synergistically acting cellulolytic complexes. Appl Environ Microbiol 2007, 73:3822-3832.
• [44]Song JM, An YJ, Kang MH, Lee YH, Cha SS: Cultivation at 6–10 degrees C is an effective strategy to overcome the insolubility of recombinant proteins in Escherichia coli. Protein Expres Purif 2012, 82:297-301.
• [45]Liu SL, Du K, Chen WZ, Liu G, Xing M: Effective approach to greatly enhancing selective secretion and expression of three cytoplasmic enzymes in Escherichia coli through synergistic effect of EDTA and lysozyme. J Ind Microbiol Biotechnol 2012, 39:1301-1307.
• [46]Gupta S, Adlakha N, Yazdani SS: Efficient extracellular secretion of an endoglucanase and a β-glucosidase in E. coli. Protein Expres Purif 2013, 88:20-25.
• [47]Shen B, Sun X, Zuo X, Shilling T, Apgar J, Ross M, Bougri O, Samoylov V, Parker M, Hancock E, Lucero H, Gray B, Ekborg NA, Zhang D, Johnson JC, Lazar G, Raab RM: Engineering a thermoregulated intein-modified xylanase into maize for consolidated lignocellulosic biomass processing. Nat Biotechnol 2012, 30:1131-1136.
• [48]Zhou S, Yomano LP, Saleh AZ, Davis FC, Aldrich HC, Ingram LO: Enhancement of expression and apparent secretion of Erwinia chrysanthemi endoglucanase (encoded by celZ) in Escherichia coli B. Appl Environ Microbiol 1999, 65:2439-2445.
• [49]Zhou S, Davis FC, Ingram LO: Gene integration and expression and extracellular secretion of Erwinia chrysanthemi endoglucanase CelY (celY) and CelZ (celZ) in ethanologenic Klebsiella oxytoca P2. Appl Environ Microbiol 2001, 67:6-14.
• [50]Shin HD, Chen RR: Extracellular recombinant protein production from an Escherichia coli lpp deletion mutant. Biotechnol Bioeng 2008, 101:1288-1296.
• [51]Girfoglio M, Rossi M, Cannio R: Cellulose degradation by Sulfolobus solfataricus requires a cell-anchored endo-beta-1-4-glucanase. J Bacteriol 2012, 194:5091-5100.
• [52]Wacker M, Linton D, Hitchen PG, Nita-Lazar M, Haslam SM, North SJ, Panico M, Morris HR, Dell A, Wren BW, Aebi M: N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 2002, 298:1790-1793.
• [53]Receveur V, Czjzek M, Schulein M, Panine P, Henrissat B: Dimension, shape, and conformational flexibility of a two domain fungal cellulase in solution probed by small angle X-ray scattering. J Biol Chem 2002, 277:40887-40892.
• [54]Harrison MJ, Nouwens AS, Jardine DR, Zachara NE, Gooley AA, Nevalainen H, Packer NH: Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei. Eur J Biochem 1998, 256:119-127.
• [55]Adlakha N, Rajagopal R, Kumar S, Reddy VS, Yazdani SS: Synthesis and characterization of chimeric proteins based on cellulase and xylanase from an insect gut bacterium. Appl Environ Microbiol 2011, 77:4859-4866.
• [56]Adlakha N, Sawant S, Anil A, Lali A, Yazdani SS: Specific fusion of beta-1,4-endoglucanase and beta-1,4-glucosidase enhances cellulolytic activity and helps in channeling of intermediates. Appl Environ Microbiol 2012, 78:7447-7454.
• [57]Fierobe HP, Bayer EA, Tardif C, Czjzek M, Mechaly A, Belaich A, Lamed R, Shoham Y, Belaich JP: Degradation of cellulose substrates by cellulosome chimeras - substrate targeting versus proximity of enzyme components. J Biol Chem 2002, 277:49621-49630.
• [58]Morais S, Barak Y, Lamed R, Wilson DB, Xu Q, Himmel ME, Bayer EA: Paradigmatic status of an endo- and exoglucanase and its effect on crystalline cellulose degradation. Biotechnol Biofuels 2012, 5:78.
• [59]Fontes C, Gilbert HJ: Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 2010, 79:655-681.
• [60]Xu Q, Ding SY, Brunecky R, Bomble YJ, Himmel ME, Baker JO: Improving activity of minicellulosomes by integration of intra- and intermolecular synergies. Biotechnol Biofuels 2013, 6:126.
• [61]Huang GL, Anderson TD, Clubb RT: Engineering microbial surfaces to degrade lignocellulosic biomass. Bioengineered 2014, 5:96-106.
• [62]Cha J, Matsuoka S, Chan H, Yukawa H, Inui M, Doi RH: Effect of multiple copies of cohesins on cellulase and hemicellulase activities of Clostridium cellulovorans mini-cellulosomes. J Microbiol Biotechnol 2007, 17:1782-1788.
• [63]Do-Myoung K, Umetsu M, Takai K, Matsuyama T, Ishida N, Takahashi H, Asano R, Kumagai I: Enhancement of cellulolytic enzyme activity by clustering cellulose binding domains on nanoscaffolds. Small 2011, 7:656-664.
• [64]Kim DM, Nakazawa H, Umetsu M, Matsuyama T, Ishida N, Ikeuchi A, Takahashi H, Asano R, Kumagai I: A nanocluster design for the construction of artificial cellulosomes. Catal Sci Technol 2012, 2:499-503.
• [65]Elkins JG, Raman B, Keller M: Engineered microbial systems for enhanced conversion of lignocellulosic biomass. Curr Opin Biotechnol 2010, 21:657-662.
• [66]Caspi J, Barak Y, Haimovitz R, Irwin D, Lamed R, Wilson DB, Bayer EA: Effect of linker length and dockerin position on conversion of a Thermobifida fusca endoglucanase to the cellulosomal mode. Appl Environ Microbiol 2009, 75:7335-7342.
• [67]Caspi J, Irwin D, Lamed R, Li Y, Fierobe HP, Wilson DB, Bayer EA: Conversion of Thermobifida fusca free exoglucanases into cellulosomal components: comparative impact on cellulose-degrading activity. J Biotechnol 2008, 135:351-357.
• [68]Anderson TD, Miller JI, Fierobe HP, Clubb RT: Recombinant Bacillus subtilis that grows on untreated plant biomass. Appl Environ Microbiol 2013, 79:867-876.
• [69]Anderson TD, Robson SA, Jiang XW, Malmirchegini GR, Fierobe HP, Lazazzera BA, Clubb RT: Assembly of minicellulosomes on the surface of Bacillus subtilis. Appl Environ Microbiol 2011, 77:4849-4858.
• [70]Matsuoka S, Yukawa H, Inui M, Doi RH: Synergistic interaction of Clostridium cellulovorans cellulosomal cellulases and HbpA. J Bacteriol 2007, 189:7190-7194.
• [71]Mingardon F, Chanal A, Tardif C, Fierobe HP: The issue of secretion in heterologous expression of Clostridium cellulolyticum cellulase-encoding genes in Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 2011, 77:2831-2838.
• [72]Wieczorek AS, Martin VJJ: Engineering the cell surface display of cohesins for assembly of cellulosome-inspired enzyme complexes on Lactococcus lactis. Microb Cell Fact 2010, 9:89.
• [73]Hyeon JE, Jeon WJ, Whang SY, Han SO: Production of minicellulosomes for the enhanced hydrolysis of cellulosic substrates by recombinant Corynebacterium glutamicum. Enzyme Microb Technol 2011, 48:371-377.
• [74]Fierobe HP, Mechaly A, Tardif C, Belaich A, Lamed R, Shoham Y, Belaich JP, Bayer EA: Design and production of active cellulosome chimeras. Selective incorporation of dockerin-containing enzymes into defined functional complexes. J Biol Chem 2001, 276:21257-21261.
• [75]Mitsuzawa S, Kagawa H, Li Y, Chan SL, Paavola CD, Trent JD: The rosettazyme: a synthetic cellulosome. J Biotechnol 2009, 143:139-144.
• [76]Morais S, Heyman A, Barak Y, Caspi J, Wilson DB, Lamed R, Shoseyov O, Bayer EA: Enhanced cellulose degradation by nano-complexed enzymes: synergism between a scaffold-linked exoglucanase and a free endoglucanase. J Biotechnol 2010, 147:205-211.
• [77]Francisco JA, Stathopoulos C, Warren RA, Kilburn DG, Georgiou G: Specific adhesion and hydrolysis of cellulose by intact Escherichia coli expressing surface anchored cellulase or cellulose binding domains. Biotechnol 1993, 11:491-495.
• [78]Kim YS, Jung HC, Pan JG: Bacterial cell surface display of an enzyme library for selective screening of improved cellulase variants. Appl Environ Microbiol 2000, 66:788-793.
• [79]Garvey M, Klose H, Fischer R, Lambertz C, Commandeur U: Cellulases for biomass degradation: comparing recombinant cellulase expression platforms. Trends Biotechnol 2013, 31:581-593.
• [80]Manabe K, Kageyama Y, Morimoto T, Shimizu E, Takahashi H, Kanaya S, Ara K, Ozaki K, Ogasawara N: Improved production of secreted heterologous enzyme in Bacillus subtilis strain MGB874 via modification of glutamate metabolism and growth conditions. Microb Cell Fact 2013, 12:18.
• [81]Liu JM, Xin XJ, Li CX, Xu JH, Bao J: Cloning of thermostable cellulase genes of Clostridium thermocellum and their secretive expression in Bacillus subtilis. Appl Biochem Biotechnol 2012, 166:652-662.
• [82]Yamada R, Hasunuma T, Kondo A: Endowing non-cellulolytic microorganisms with cellulolytic activity aiming for consolidated bioprocessing. Biotechnol Adv 2013, 31:754-763.
• [83]Bokinsky G, Peralta-Yahya PP, George A, Holmes BM, Steen EJ, Dietrich J, Soon Lee T, Tullman-Ercek D, Voigt CA, Simmons BA, Keasling JD: Synthesis of three advanced biofuels from ionic liquid-pretreated switchgrass using engineered Escherichia coli. Proc Natl Acad Sci U S A 2011, 108:19949-19954.
• [84]Liu J-R, Yu B, Liu F-H, Cheng K-J, Zhao X: Expression of rumen microbial fibrolytic enzyme genes in probiotic Lactobacillus reuteri. Appl Environ Microbiol 2005, 71:6769-6775.
• [85]Lee EJ, Lee BH, Kim BK, Lee JW: Enhanced production of carboxymethylcellulase of a marine microorganism, Bacillus subtilis subsp. subtilis A-53 in a pilot-scaled bioreactor by a recombinant Escherichia coli JM109/A-53 from rice bran. Mol Biol Rep 2013, 40:3609-3621.
• [86]la Grange DC, den Haan R, van Zyl WH: Engineering cellulolytic ability into bioprocessing organisms. Appl Microbiol Biotechnol 2010, 87:1195-1208.
• [87]Young CL, Robinson AS: Protein folding and secretion: mechanistic insights advancing recombinant protein production in S. cerevisiae. Curr Opin Biotechnol 2014, 30C:168-177.
• [88]Varnai A, Tang C, Bengtsson O, Atterton A, Mathiesen G, Eijsink VG: Expression of endoglucanases in Pichia pastoris under control of the GAP promoter. Microb Cell Fact 2014, 13:57.
• [89]Jeoh T, Michener W, Himmel ME, Decker SR, Adney WS: Implications of cellobiohydrolase glycosylation for use in biomass conversion. Biotechnol Biofuels 2008, 1:10.
• [90]Shen H, Schmuck M, Pilz I, Gilkes NR, Kilburn DG, Miller RC Jr, Warren RA: Deletion of the linker connecting the catalytic and cellulose-binding domains of endoglucanase A (CenA) of Cellulomonas fimi alters its conformation and catalytic activity. J Biol Chem 1991, 266:11335-11340.
• [91]Payne CM, Resch MG, Chen L, Crowley MF, Himmel ME, Taylor LE 2nd, Sandgren M, Stahlberg J, Stals I, Tan Z, Beckham GT: Glycosylated linkers in multimodular lignocellulose-degrading enzymes dynamically bind to cellulose. Proc Natl Acad Sci U S A 2013, 110:14646-14651.
• [92]Bommarius AS, Sohn M, Kang Y, Lee JH, Realff MJ: Protein engineering of cellulases. Curr Opin Biotechnol 2014, 29C:139-145.
• [93]Trudeau DL, Lee TM, Arnold FH: Engineered thermostable fungal cellulases exhibit efficient synergistic cellulose hydrolysis at elevated temperatures.Biotechnol Bioeng 2014. doi:10.1002/bit.25308.
• [94]Ostafe R, Prodanovic R, Commandeur U, Fischer R: Flow cytometry-based ultra-high-throughput screening assay for cellulase activity. Anal Biochem 2013, 435:93-98.
• [95]Haan RD, Mcbride JE, la Grange DC, Lynd LR, van Zyl JM: Functional expression of cellobiohydrolases in Saccharomyces cerevisiae. Enzyme Microb Technol 2007, 40:1291-1299.
• [96]Fitzpatrick J, Kricka W, James TC, Bond U: Expression of three Trichoderma reesei cellulase genes in Saccharomyces pastorianus for the development of a two-step process of hydrolysis and fermentation of cellulose. J Appl Microbiol 2014, 117:96-108.
• [97]Banerjee G, Car S, Scott-Craig JS, Borrusch MS, Aslam N, Walton JD: Synthetic enzyme mixtures for biomass deconstruction: production and optimization of a core set. Biotechnol Bioeng 2010, 106:707-720.
• [98]Chen P, Fu X, Ng TB, Ye XY: Expression of a secretory beta-glucosidase from Trichoderma reesei in Pichia pastoris and its characterization. Biotechnol Lett 2011, 33:2475-2479.
• [99]Chang JJ, Ho FJ, Ho CY, Wu YC, Hou YH, Huang CC, Shih MC, Li WH: Assembling a cellulase cocktail and a cellodextrin transporter into a yeast host for CBP ethanol production. Biotechnol Biofuels 2013, 6:19.
• [100]Ito J, Kosugi A, Tanaka T, Kuroda K, Shibasaki S, Ogino C, Ueda M, Fukuda H, Doi RH, Kondo A: Regulation of the display ratio of enzymes on the Saccharomyces cerevisiae cell surface by the immunoglobulin G and cellulosomal enzyme binding domains. Appl Environ Microbiol 2009, 75:4149-4154.
• [101]Apiwatanapiwat W, Murata Y, Kosugi A, Yamada R, Kondo A, Arai T, Rugthaworn P, Mori Y: Direct ethanol production from cassava pulp using a surface-engineered yeast strain co-displaying two amylases, two cellulases, and beta-glucosidase. Appl Microbiol Biotechnol 2011, 90:377-384.
• [102]den Haan R, Kroukamp H, van Zyl JHD, van Zyl WH: Cellobiohydrolase secretion by yeast: current state and prospects for improvement. Process Biochem 2013, 48:1-12.
• [103]Arima K, Oshima T, Kubota I, Nakamura N, Mizunaga T, Toh-e A: The nucleotide sequence of the yeast PHO5 gene: a putative precursor of repressible acid phosphatase contains a signal peptide. Nucleic Acids Res 1983, 11:1657-1672.
• [104]Perlman D, Halvorson HO, Cannon LE: Presecretory and cytoplasmic invertase polypeptides encoded by distinct mRNAs derived from the same structural gene differ by a signal sequence. Proc Natl Acad Sci U S A 1982, 79:781-785.
• [105]Van Zyl JH, Den Haan R, Van Zyl WH: Over-expression of native Saccharomyces cerevisiae exocytic SNARE genes increased heterologous cellulase secretion. Appl Microbiol Biotechnol 2014, 98:5567-5578.
• [106]du Plessis L, Rose SH, van Zyl WH: Exploring improved endoglucanase expression in Saccharomyces cerevisiae strains. Appl Microbiol Biotechnol 2010, 86:1503-1511.
• [107]Heinzelman P, Snow CD, Wu I, Nguyen C, Villalobos A, Govindarajan S, Minshull J, Arnold FH: A family of thermostable fungal cellulases created by structure-guided recombination. Proc Natl Acad Sci U S A 2009, 106:5610-5615.
• [108]Kroukamp H, den Haan R, van Wyk N, van Zyl WH: Overexpression of native PSE1 and SOD1 in Saccharomyces cerevisiae improved heterologous cellulase secretion. Appl Energ 2013, 102:150-156.
• [109]Sakai A, Shimizu Y, Hishinuma F: Integration of heterologous genes into the chromosome of Saccharomyces cerevisiae using a delta sequence of yeast retrotransposon Ty. Appl Microbiol Biotechnol 1990, 33:302-306.
• [110]Liu L, Liu C, Zou S, Yang H, Hong J, Ma Y, Zhang M: Expression of cellulase genes in Saccharomyces cerevisiae via delta-integration subject to auxotrophic markers. Biotechnol Lett 2013, 35:1303-1307.
• [111]Blazeck J, Alper HS: Promoter engineering: recent advances in controlling transcription at the most fundamental level. Biotechnol J 2013, 8:46-58.
• [112]Yamanishi M, Ito Y, Kintaka R, Imamura C, Katahira S, Ikeuchi A, Moriya H, Matsuyama T: A genome-wide activity assessment of terminator regions in Saccharomyces cerevisiae provides a “terminatome” toolbox. ACS Synth Biol 2013, 2:337-347.
• [113]Ito Y, Yamanishi M, Ikeuchi A, Matsuyama T: A highly tunable system for the simultaneous expression of multiple enzymes inSaccharomyces cerevisiae.ACS Synth Biol 2014. doi:10.1021/sb500096y.
• [114]Akcapinar GB, Gul O, Sezerman U: Effect of codon optimization on the expression of Trichoderma reesei endoglucanase 1 in Pichia pastoris. Biotechnol Prog 2011, 27:1257-1263.
• [115]Bey M, Berrin JG, Poidevin L, Sigoillot JC: Heterologous expression of Pycnoporus cinnabarinus cellobiose dehydrogenase in Pichia pastoris and involvement in saccharification processes. Microb Cell Fact 2011, 10:113.
• [116]Akbarzadeh A, Ranaei Siadat SO, Motallebi M, Zamani MR, Barshan Tashnizi M, Moshtaghi S: Characterization and high level expression of acidic endoglucanase in Pichia pastoris. Appl Biochem Biotechnol 2014, 172:2253-2265.
• [117]Jager G, Girfoglio M, Dollo F, Rinaldi R, Bongard H, Commandeur U, Fischer R, Spiess AC, Buchs J: How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels 2011, 4:33.
• [118]Tsai SL, Goyal G, Chen W: Surface display of a functional minicellulosome by intracellular complementation using a synthetic yeast consortium and its application to cellulose hydrolysis and ethanol production. Appl Environ Microbiol 2010, 76:7514-7520.
• [119]Kim S, Baek SH, Lee K, Hahn JS: Cellulosic ethanol production using a yeast consortium displaying a minicellulosome and beta-glucosidase. Microb Cell Fact 2013, 12:14.
• [120]Hyeon JE, Yu KO, Suh DJ, Suh YW, Lee SE, Lee J, Han SO: Production of minicellulosomes from Clostridium cellulovorans for the fermentation of cellulosic ethanol using engineered recombinant Saccharomyces cerevisiae. FEMS Microbiol Lett 2010, 310:39-47.
• [121]Ilmen M, den Haan R, Brevnova E, McBride J, Wiswall E, Froehlich A, Koivula A, Voutilainen SP, Siika-Aho M, la Grange DC, Thorngren N, Ahlgren S, Mellon M, Deleault K, Rajgarhia V, van Zyl WH, Penttila M: High level secretion of cellobiohydrolases by Saccharomyces cerevisiae. Biotechnol Biofuels 2011, 4:30.
• [122]Romanos MA, Scorer CA, Clare JJ: Foreign gene expression in yeast: a review. Yeast 1992, 8:423-488.
• [123]Boer H, Teeri TT, Koivula A: Characterization of Trichoderma reesei cellobiohydrolase Cel7A secreted from Pichia pastoris using two different promoters. Biotechnol Bioeng 2000, 69:486-494.
• [124]Li YL, Li H, Li AN, Li DC: Cloning of a gene encoding thermostable cellobiohydrolase from the thermophilic fungus Chaetomium thermophilum and its expression in Pichia pastoris. J Appl Microbiol 2009, 106:1867-1875.
• [125]Sadie CJ, Rose SH, den Haan R, van Zyl WH: Co-expression of a cellobiose phosphorylase and lactose permease enables intracellular cellobiose utilisation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 2011, 90:1373-1380.
• [126]Yamada R, Taniguchi N, Tanaka T, Ogino C, Fukuda H, Kondo A: Cocktail delta-integration: a novel method to construct cellulolytic enzyme expression ratio-optimized yeast strains. Microb Cell Fact 2010, 9:32.
• [127]Khramtsov N, McDade L, Amerik A, Yu E, Divatia K, Tikhonov A, Minto M, Kabongo-Mubalamate G, Markovic Z, Ruiz-Martinez M, Henck S: Industrial yeast strain engineered to ferment ethanol from lignocellulosic biomass. Bioresour Technol 2011, 102:8310-8313.
• [128]Olson DG, McBride JE, Shaw AJ, Lynd LR: Recent progress in consolidated bioprocessing. Curr Opin Biotechnol 2012, 23:396-405.
• [129]Kricka W, Fitzpatrick J, Bond U: Metabolic engineering of yeasts by heterologous enzyme production for degradation of cellulose and hemicellulose from biomass: a perspective. Front Microbiol 2014, 5:174.
• [130]Yamada R, Nakatani Y, Ogino C, Kondo A: Efficient direct ethanol production from cellulose by cellulase- and cellodextrin transporter-co-expressing Saccharomyces cerevisiae. AMB Express 2013, 3:34.
• [131]Merico A, Capitanio D, Vigentini I, Ranzi BM, Compagno C: How physiological and cultural conditions influence heterologous protein production in Kluyveromyces lactis. J Biotechnol 2004, 109:139-146.
• [132]Liu B, Gong X, Chang S, Yang Y, Song M, Duan D, Wang L, Ma Q, Wu J: Disruption of the OCH1 and MNN1 genes decrease N-glycosylation on glycoprotein expressed in Kluyveromyces lactis. J Biotechnol 2009, 143:95-102.
• [133]Aden A, Ruth M, Ibsen K, Jechura J, Neeves K, Sheehan J, Wallace B, Montague L, Slayton A, Lukas J: Lignocellulosic biomass to ethanol process design and economics utilizing co-current dilute acid prehydrolysis and enzymatic hydrolysis for corn stover. In DTIC Document. NREL; 2002.
• [134]Ziegelhoffer T, Raasch JA, Austin-Phillips S: Dramatic effects of truncation and sub-cellular targeting on the accumulation of recombinant microbial cellulase in tobacco. Mol Breeding 2001, 8:147-158.
• [135]Dai Z, Hooker BS, Quesenberry RD, Thomas SR: Optimization of Acidothermus cellulolyticus endoglucanase (E1) production in transgenic tobacco plants by transcriptional, post-transcription and post-translational modification. Transgenic Res 2005, 14:627-643.
• [136]Hood EE, Love R, Lane J, Bray J, Clough R, Pappu K, Drees C, Hood KR, Yoon S, Ahmad A: Subcellular targeting is a key condition for high‐level accumulation of cellulase protein in transgenic maize seed. Plant Biotechnol J 2007, 5:709-719.
• [137]Oraby H, Venkatesh B, Dale B, Ahmad R, Ransom C, Oehmke J, Sticklen M: Enhanced conversion of plant biomass into glucose using transgenic rice-produced endoglucanase for cellulosic ethanol. Trangenic Res 2007, 16:739-749.
• [138]Mei C, Park SH, Sabzikar R, Ransom C, Qi C, Sticklen M: Green tissue specific production of a microbial endo cellulase in maize (Zea mays L.) endoplasmic reticulum and mitochondria converts cellulose into fermentable sugars. J Chem Technol Biotechnol 2009, 84:689-695.
• [139]Mahadevan SA, Wi SG, Kim YO, Lee KH, Bae H-J: In planta differential targeting analysis of Thermotoga maritima Cel5A and CBM6-engineered Cel5A for autohydrolysis. Transgenic Res 2011, 20:877-886.
• [140]Jung S, Lee DS, Kim YO, Joshi CP, Bae HJ: Improved recombinant cellulase expression in chloroplast of tobacco through promoter engineering and 5′ amplification promoting sequence. Plant Mol Biol 2013, 83:317-328.
• [141]Caspi J, Barak Y, Haimovitz R, Gilary H, Irwin DC, Lamed R, Wilson DB, Bayer EA: Thermobifida fusca exoglucanase Cel6B is incompatible with the cellulosomal mode in contrast to endoglucanase Cel6A. Syst Synth Biol 2010, 4:193-201.
• [142]Klose H, Röder J, Girfoglio M, Fischer R, Commandeur U: Hyperthermophilic endoglucanase for in planta lignocellulose conversion. Biotechnol Biofuels 2012, 5:63.
• [143]Oey M, Lohse M, Kreikemeyer B, Bock R: Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 2009, 57:436-445.
• [144]Ziegelhoffer T, Raasch JA, Austin-Phillips S: Expression of Acidothermus cellulolyticus E1 endo-β-1,4-glucanase catalytic domain in transplastomic tobacco. Plant Biotechnol J 2009, 7:527-536.
• [145]Yu L-X, Gray BN, Rutzke CJ, Walker LP, Wilson DB, Hanson MR: Expression of thermostable microbial cellulases in the chloroplasts of nicotine-free tobacco. J Biotechnol 2007, 131:362-369.
• [146]Gray B, Yang H, Ahner B, Hanson M: An efficient downstream box fusion allows high-level accumulation of active bacterial beta-glucosidase in tobacco chloroplasts. Plant Mol Biol 2011, 76:345-355.
• [147]Gray BN, Ahner BA, Hanson MR: High-level bacterial cellulase accumulation in chloroplast-transformed tobacco mediated by downstream box fusions. Biotechnol Bioeng 2009, 102:1045-1054.
• [148]Petersen K, Bock R: High-level expression of a suite of thermostable cell wall-degrading enzymes from the chloroplast genome. Plant Mol Biol 2011, 76:311-321.
• [149]Krichevsky A, Meyers B, Vainstein A, Maliga P, Citovsky V: Autoluminescent plants. PLoS One 2010, 5:e15461.
• [150]Bock R: Genetic engineering of the chloroplast: novel tools and new applications. Curr Opin Biotechnol 2014, 26:7-13.
• [151]Ruf S, Karcher D, Bock R: Determining the transgene containment level provided by chloroplast transformation. Proc Natl Acad Sci U S A 2007, 104:6998-7002.
• [152]Nuttall J, Vine N, Hadlington JL, Drake P, Frigerio L, Ma JK: ER-resident chaperone interactions with recombinant antibodies in transgenic plants. Eur J Biochem 2002, 269:6042-6051.
• [153]Klose H, Günl M, Usadel B, Fischer R, Commandeur U: Ethanol inducible expression of a mesophilic cellulase avoids adverse effects on plant development. Biotechnol Biofuels 2013, 6:53.
• [154]Hartati S, Sudarmonowati E, Park YW, Kaku T, Kaida R, Baba K, Hayashi T: Overexpression of poplar cellulase accelerates growth and disturbs the closing movements of leaves in sengon. Plant Physiol 2008, 147:552-561.
• [155]Ransom C, Balan V, Biswas G, Dale B, Crockett E, Sticklen M: Heterologous Acidothermus cellulolyticus 1,4-beta-endoglucanase E1 produced within the corn biomass converts corn stover into glucose. Appl Biochem Biotechnol 2007, 137–140:207-219.
• [156]Zhang Q, Zhang W, Lin C, Xu X, Shen Z: Expression of an Acidothermus cellulolyticus endoglucanase in transgenic rice seeds. Protein Expres Purif 2012, 82:279-283.
• [157]Maloney VJ, Mansfield SD: Characterization and varied expression of a membrane-bound endo-beta-1,4-glucanase in hybrid poplar. Plant Biotechnol J 2010, 8:294-307.
• [158][http://www.syngenta.com/country/us/en/enogen/Pages/Home.asp] webcite Syngenta. []
• [159]Hood EE, Devaiah SP, Fake G, Egelkrout E, Teoh K, Requesens DV, Hayden C, Hood KR, Pappu KM, Carroll J, Howard JA: Manipulating corn germplasm to increase recombinant protein accumulation. Plant Biotechnol J 2012, 10:20-30.
• [160]Harrison MD, Geijskes J, Coleman HD, Shand K, Kinkema M, Palupe A, Hassall R, Sainz M, Lloyd R, Miles S, Dale JL: Accumulation of recombinant cellobiohydrolase and endoglucanase in the leaves of mature transgenic sugar cane. Plant Biotechnol J 2011, 9:884-896.
• [161]Harrison MD, Geijskes RJ, Lloyd R, Miles S, Palupe A, Sainz MB, Dale JL: Recombinant cellulase accumulation in the leaves of mature, vegetatively propagated transgenic sugarcane. Mol Biotechnol 2014, 56:795-802.
• [162]Kaida R, Kaku T, Baba K, Oyadomari M, Watanabe T, Nishida K, Kanaya T, Shani Z, Shoseyov O, Hayashi T: Loosening xyloglucan accelerates the enzymatic degradation of cellulose in wood. Mol Plant 2009, 2:904-909.
• [163]Taylor Ii LE, Dai Z, Decker SR, Brunecky R, Adney WS, Ding S-Y, Himmel ME: Heterologous expression of glycosyl hydrolases in planta: a new departure for biofuels. Trends Biotechnol 2008, 26:413-424.
• [164]Sainz M: Commercial cellulosic ethanol: rhe role of plant-expressed enzymes. In Vitro Cell Dev-Pl 2009, 45:314-329.
• [165]Brunecky R, Selig M, Vinzant T, Himmel M, Lee D, Blaylock M, Decker S: In planta expression of A. cellulolyticus Cel5A endocellulase reduces cell wall recalcitrance in tobacco and maize. Biotechnol Biofuels 2011, 4:1.
• [166]Zhang D, VanFossen A, Pagano R, Johnson J, Parker M, Pan S, Gray B, Hancock E, Hagen D, Lucero H, Shen B, Lessard P, Ely C, Moriarty M, Ekborg N, Bougri O, Samoylov V, Lazar G, Raab RM: Consolidated pretreatment and hydrolysis of plant biomass expressing cell wall degrading enzymes. Bioenerg Res 2011, 4:276-286.
• [167]de O Buanafina MM, Fescemyer H: Modification of esterified cell wall phenolics increases vulnerability of tall fescue to herbivory by the fall armyworm. Planta 2012, 236:513-523.