Skip to main content

Advertisement

SpringerLink
Log in

Cell Wall Engineering by Heterologous Expression of Cell Wall-Degrading Enzymes for Better Conversion of Lignocellulosic Biomass into Biofuels

  • Published:
BioEnergy Research Aims and scope Submit manuscript

Abstract

Huge energy demand with increasing population is addressing renewable and sustainable energy sources. A solution to energy demand problem is to replace our current fossil fuel-based economy with alternative strategies that do not emit carbon dioxide. Plant biomass is one of the best candidates for this issue. Plants use solar power to convert carbon dioxide and water into sugars, which can be used in fermentation reactions to produce both energy and materials. However, the desired sugars are trapped in the highly recalcitrant cell wall as building blocks of cellulose chains. Moreover, the complexity of the plant cell wall structure hinders the hydrolysis of cellulose into fermentable sugar monomers. Although pretreatments are used to change the physical and chemical properties of the lignocellulosic biomass and improve hydrolysis rates, these pretreatments often use harsh and polluting chemicals and severely increase the cost of biofuel production. The goal of the review is to summarize recent researches, which describe generating plants with a modified cell wall and improve hydrolysis of cellulose without applying any or less pretreatment methods. Since pretreatment of lignocellulosic biomass is the most cost effective step in biofuel production, generating autodigestible plants could reduce the production cost of biofuels and bio-based biomaterials. One of the strategies to improve biomass conversion efficiency is the modification of the cell wall by heterologous expression of cell wall-modifying proteins. These cell wall-modifying proteins could alter the cell wall structure and reduce cell wall recalcitrance. The use of such transgenic technologies would consume less energy and chemicals when cellulose is more accessible for enzymatic hydrolysis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. IEA (2013) World energy outlook 2013. IEA Publications. www.worldenergyoutlook.org

  2. De Jong E, Langeveld H, Van Ree R. (2009) IEA bioenergy task 42 on biorefinery

  3. McKendry P (2002) Energy production from biomass (part 1): overview of biomass. Bioresour Technol 83:37–46

    CAS  PubMed  Google Scholar 

  4. Gray KA, Zhao L, Emptage M (2006) Bioethanol. Curr Opin Chem Biol 10(2):141–6

    CAS  PubMed  Google Scholar 

  5. Young AL (2009) Finding the balance between food and biofuels. Environ Sci Pollut Res Int 16(2):117–9

    PubMed  Google Scholar 

  6. Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci U S A 103(30):11206–10

    PubMed Central  CAS  PubMed  Google Scholar 

  7. Ford C, Runge BS (2007) Biofuel: corn isn’t the king of this growing domain. Nature 450:478

    Google Scholar 

  8. Gomez LD, Steele-King CG, McQueen-Mason SJ (2008) Sustainable liquid biofuels from biomass: the writings on the walls. New Phytol 178(3):473–85

    CAS  PubMed  Google Scholar 

  9. Tilman D, Hill J, Lehman C (2006) Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314(5805):1598–600

    CAS  PubMed  Google Scholar 

  10. Davis J (2008) Genetic improvement of poplar (Populus spp.) as a bioenergy crop. In: Vermerris W (ed) Genetic improvement of bioenergy crops. Springer, New York, pp 397–419

    Google Scholar 

  11. Gordon JC (2001) Poplars: trees of the people, trees of the future. For Chron 77(2):217–9

    Google Scholar 

  12. Wingren A, Galbe M, Zacchi G (2003) Techno-economic evaluation of producing ethanol from softwood: comparison of SSF and SHF and identification of bottlenecks. Biotechnol Prog 19(4):1109–17

    CAS  PubMed  Google Scholar 

  13. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25(3):294–306

    CAS  PubMed  Google Scholar 

  14. Antizar-Ladislao B, Turrion-Gomez JL (2008) Second-generation biofuels and local bioenergy systems. Biofuels Bioprod Bioref 2(5):455–69

    CAS  Google Scholar 

  15. Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171–201

    CAS  PubMed  Google Scholar 

  16. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6(11):850

    CAS  PubMed  Google Scholar 

  17. Peng L, Kawagoe Y, Hogan P, Delmer D (2002) Sitosterol-beta-glucoside as primer for cellulose synthesis in plants. Science 295(5552):147–50

    CAS  PubMed  Google Scholar 

  18. Brett CT (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161

    CAS  PubMed  Google Scholar 

  19. Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17(8):2281–95

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Ha MA, Apperley DC, Evans BW, Huxham IM, Jardine WG, Viëtor RJ et al (1998) Fine structure in cellulose microfibrils: NMR evidence from onion and quince. Plant J 16:183–90

    CAS  PubMed  Google Scholar 

  21. Herth W (1983) Arrays of plasma-membrane rosettes involved in cellulose microfibril formation of spirogyra. Planta 159(4):347–56

    CAS  PubMed  Google Scholar 

  22. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–89

    CAS  PubMed  Google Scholar 

  23. Ebringerová A, Hromádková Z, Heinze T (2005) Hemicellulose 186:1–67

    Google Scholar 

  24. Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–77

    CAS  PubMed  Google Scholar 

  25. Harholt J, Suttangkakul A, Vibe SH (2010) Biosynthesis of pectin. Plant Physiol 153(2):384–95

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Wiethölter N, Graeßner B, Mierau M, Mort AJ, Moerschbacher BM (2003) Differences in the methyl ester distribution of homogalacturonans from near-isogenic wheat lines resistant and susceptible to the wheat stem rust fungus. Mol Plant Microbe Interact 16(10):945–54

    PubMed  Google Scholar 

  27. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344(14):1879–900

    CAS  PubMed  Google Scholar 

  28. Xiao C, Anderson CT (2013) Roles of pectin in biomass yield and processing for biofuels. Front Plant Sci 4:67

    PubMed Central  PubMed  Google Scholar 

  29. O’Neill M, Albersheim P, Darvill A (1990) The pectic polysaccharides of primary cell walls. In: Carbohydrates PMD, Harborne JB (eds) Methods in plant biochemistry. Academic, London, pp 415–41

    Google Scholar 

  30. Albersheim P, Darvill A, O’Neill M, Schols H, Voragen A (1996) An hypothesis; the same six polysaccharides are components of the primary cell walls of all higher plants. In: Visser J, Voragen AGJ (eds) Pectins and pectinases. Elsevier Science BV, Amsterdam, pp 47–55

    Google Scholar 

  31. O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–39

    PubMed  Google Scholar 

  32. Ishii T, Matsunaga T (1996) Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydr Res 284(1):1–9

    CAS  Google Scholar 

  33. Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193(1–2):121–48

    CAS  Google Scholar 

  34. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–46

    CAS  PubMed  Google Scholar 

  35. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153(3):895–905

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Shafizadeh F, Chin P (1977) Thermal degradation of wood. In IS Goldstein (ed), Wood technology: chemical aspects American chemical society symposium series, Washington DC, 57–81

  37. White RH (1987) Effect of lignin content and extractives on the higher heating value of wood. Wood Fiber Sci 19:446–52

    CAS  Google Scholar 

  38. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz P et al (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev 3:29–60

    CAS  Google Scholar 

  39. Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11(3):301–7

    CAS  PubMed  Google Scholar 

  40. Jordan DB, Bowman MJ, Braker JD, Dien BS, Hector RE, Lee CC et al (2012) Plant cell walls to ethanol. Biochem J 442:241–52

    CAS  PubMed  Google Scholar 

  41. Mood SH, Golfeshan AH, Tabatabaei M, Abbasalizadeh S, Ardjmand M (2013) Comparison of different ionic liquids pretreatment for barley straw enzymatic saccharification. Biotech 3(5):399–406

    Google Scholar 

  42. Zhang D, VanFossen AL, Pagano RM, Johnson JS, Parker MH, Pan S et al (2011) Consolidated pretreatment and hydrolysis of plant biomass expressing cell wall degrading enzymes. BioEnergy Res 4(4):276–86

    Google Scholar 

  43. Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66:10–26

    CAS  PubMed  Google Scholar 

  44. Palmqvist E, Hahn-Hagerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33

    CAS  Google Scholar 

  45. Klein-Marcuschamer D, Oleskowicz-Popiel P, Simmons BA, Blanch HW (2012) The challenge of enyzme cost in the production of lignocellulosic biomass. Biotechnol Bioeng 109(4):1083–7

    CAS  PubMed  Google Scholar 

  46. Merino ST, Cherry J (2007) Progress and challenges in enzyme development for biomass utilization. Biofuels 108:95–120

    CAS  Google Scholar 

  47. Aden A, Foust T (2009) Technoeconomic analysis of the dilute sulfuric acid and enzymatic hydrolysis process for the conversion of corn stover to ethanol. Cellulose 16:535–45

    CAS  Google Scholar 

  48. Lynd LR, Laser MS, Bransby D, Dale BE, Davison B, Hamilton R et al (2008) How biotech can transform biofuels. Nat Biotechnol 26:169–72

    CAS  PubMed  Google Scholar 

  49. Dutta A, Dowe N, Ibsen KN, Schell DJ, Aden A (2010) An economic comparison of different fermentation configurations to convert corn stover to ethanol using Z. mobilis and Saccharomyces. Biotechnol Prog 26:64–72

    CAS  PubMed  Google Scholar 

  50. Kazi FK, Fortman JA, Anex RP, Hsu DD, Aden A, Dutta A et al (2010) Techno-economic comparison of process technologies for biochemical ethanol production from corn stover. Fuel 89:20–8

    Google Scholar 

  51. Levine SE, Fox JM, Clark DS, Blanch HW (2011) A mechanistic model for rational design of optimal cellulase mixtures. Biotechnol Bioeng 108:2561–70

    CAS  PubMed  Google Scholar 

  52. Peterson R, Nevalainen H (2012) Trichoderma reesei RUT-C30—thirty years of strain improvement. Microbiology 158(Pt 1):58–68

    CAS  PubMed  Google Scholar 

  53. Alvira P, Tomas-Pejo E, Ballesteros M, Negro MJ (2010) Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: a review. Bioresour Technol 101(13):4851–61

    CAS  PubMed  Google Scholar 

  54. Haghighi Mood S, Hossein Golfeshan A, Tabatabaei M, Salehi Jouzani G, Najafi GH, Gholami M et al (2013) Lignocellulosic biomass to bioethanol, a comprehensive review with a focus on pretreatment. Renew Sust Energ Rev 27:77–93

    CAS  Google Scholar 

  55. Gille S, Pauly M (2012) O-acetylation of plant cell wall polysaccharides. Front Plant Sci 3:12

    PubMed Central  CAS  PubMed  Google Scholar 

  56. Lin Y, Tanaka S (2006) Ethanol fermentation from biomass resources: current state and prospects. Appl Microbiol Biotechnol 69(6):627–42

    CAS  PubMed  Google Scholar 

  57. Hector R, Qureshi N, Hughes S, Cotta M (2008) Expression of a heterologous xylose transporter in a Saccharomyces cerevisiae strain engineered to utilize xylose improves aerobic xylose consumption. Appl Microbiol Biotechnol 80(4):675–84

    CAS  PubMed  Google Scholar 

  58. Demeke MM, Dietz H, Li Y, Foulquié-Moreno MR, Mutturi S, Deprez S et al (2013) Development of a D-xylose fermenting and inhibitor tolerant industrial Saccharomyces cerevisiae strain with high performance in lignocellulose hydrolysates using metabolic and evolutionary engineering. Biotechnol Biofuels 6:89

    PubMed Central  CAS  PubMed  Google Scholar 

  59. Abramson M, Shoseyov O, Shani Z (2010) Plant cell wall reconstruction toward improved lignocellulosic production and processability. Plant Sci 178(2):61–72

    CAS  Google Scholar 

  60. Eudes A, Liang Y, Mitra P, Loqué D (2014) Lignin bioengineering. Curr Opin Biotechnol 26:189–98

    CAS  PubMed  Google Scholar 

  61. Petersen PD, Lau J, Ebert B, Yang F, Verhertbruggen Y, Kim JS et al (2012) Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants. Biotechnol Biofuels 5:84

    PubMed Central  CAS  PubMed  Google Scholar 

  62. Garvey M, Klose H, Fischer R, Lambertz C, Commandeur U (2013) Cellulases for biomass degradation: comparing recombinant cellulase expression platforms. Trends Biotechnol 31(10):581–93

    CAS  PubMed  Google Scholar 

  63. Mahadevan SA, Wi SG, Kim YO, Lee KH, Bae HJ (2011) In planta differential targeting analysis of Thermotoga maritima Cel5A and CBM6-engineered Cel5A for autohydrolysis. Transgenic Res 20:877–86

    CAS  PubMed  Google Scholar 

  64. Chou HL, Dai Z, Hsieh CW, Ku MS (2011) High level expression of Acidothermus cellulolyticus beta-1, 4-endoglucanase in transgenic rice enhances the hydrolysis of its straw by cultured cow gastric fluid. Biotechnol Biofuels 4:58

    PubMed Central  CAS  PubMed  Google Scholar 

  65. Maloney VJ, Mansfield SD (2010) Characterization and varied expression of a membrane-bound endo-beta-1,4-glucanase in hybrid poplar. Plant Biotechnol J 8:294–307

    CAS  PubMed  Google Scholar 

  66. Kawazu T, Sun JL, Shibata M, Kimura T, Sakka K, Ohmiya K (1999) Expression of a Bacterial Endoglucanase Gene in Tobacco Increases Digestibility of Its Cell Wall Fibers. J Biosci Bioeng 88(4):421–425

    CAS  PubMed  Google Scholar 

  67. Ziegelhoffer T, Raasch JA, Austin-Phillips S (2001) Dramatic effects of truncation and sub-cellular targeting on the accumulation of recombinant microbial cellulase in tobacco. Mol Breed 8(2):147–58

    CAS  Google Scholar 

  68. Dai Z, Hooker BS, Anderson DB, Thomas SR (2000) Expression of Acidothermus cellulolyticus endoglucanase E1 in transgenic tobacco: biochemical characteristics and physiological effects. Transgenic Res 9(1):43–54

    CAS  PubMed  Google Scholar 

  69. Dai Y, Hooker BS, Anderson DB, Thomas SR (2000) Improved plant-based production of E1 endoglucanase using potato: expression optimization and tissue targeting. Mol Breed 6:277–85

    CAS  Google Scholar 

  70. Ziegler MT, Thomas SR, Danna KJ (2000) Accumulation of a thermostable endo-1, 4-β-D-glucanase in the apoplast of Arabidopsis thaliana leaves. Mol Breed 6(1):37–46

    CAS  Google Scholar 

  71. Jin R, Richter S, Zhong R, Lamppa GK (2003) Expression and import of an active cellulase from a thermophilic bacterium into the chloroplast both in vitro and in vivo. Plant Mol Biol 51:493–507

    CAS  PubMed  Google Scholar 

  72. Xue GP, Patel M, Johnson JS, Smyth DJ, Vickers CE (2003) Selectable marker-free transgenic barley producing a high level of cellulase (1,4-β-glucanase) in developing grains. Plant Cell Rep 21:1088–94

    CAS  PubMed  Google Scholar 

  73. Dai Z, Hooker BS, Quesenberry RD, Thomas SR (2005) Optimization of Acidothermus cellulolyticus endoglucanase (E1) production in transgenic tobacco plants by transcriptional, post-transcription and post-translational modification. Transgenic Res 14:627–43

    CAS  PubMed  Google Scholar 

  74. Biswas GCG, Ransom C, Sticklen M (2006) Expression of biologically active acidothermus cellulolyticus endoglucanase in transgenic maize plants. Plant Sci 171(5):617–23

    CAS  Google Scholar 

  75. Sun Y, Cheng JJ, Himmel ME, Skory CD, Adney WS, Thomas SR et al (2007) Expression and characterization of Acidothermus cellulolyticus E1 endoglucanase in transgenic duckweed Lemna minor 8627. Bioresour Technol 98:2866–2872

    CAS  PubMed  Google Scholar 

  76. Oraby H, Venkatesh B, Dale B, Ahmad R, Ransom C, Oehmke J et al (2007) Enhanced conversion of plant biomass into glucose using transgenic rice-produced endoglucanase for cellulosic ethanol. Transgenic Res 16(6):739–49

    CAS  PubMed  Google Scholar 

  77. Ransom C, Balan V, Biswas G, Dale B, Crockett E, Sticklen M (2007) Heterologous Acidothermus cellulolyticus 1, 4-β-endoglucanase E1 produced within the corn biomass converts corn stover into glucose. Appl Biochem Biotechnol 137(140):207–19

    PubMed  Google Scholar 

  78. Yu LX, Gray BN, Rutzke CJ, Walker LP, Wilson DB, Hanson MR (2007) Expression of thermostable microbial cellulases in the chloroplasts of nicotine-free tobacco. J Biotechnol 131(3):362–9

    CAS  PubMed  Google Scholar 

  79. Liu JH, Selinger LB, Cheng KJ, Beauchemin KA, Moloney MM (1997) Plant seed oil-bodies as an immobilization matrix for a recombinant xylanase from the rumen fungus Neocallimastix patriciarum. Mol Breed 3(6):463–470

    CAS  Google Scholar 

  80. Patel M, Johnson JS, Brettell RIS, Jacobsen J, Xue GP (2000) Transgenic barley expressing a fungal xylanase gene in the endosperm of the developing grains. Mol Breed 6(1):113–124

    CAS  Google Scholar 

  81. Kimura T, Mizutani T, Tanaka T, Koyama T, Sakka K, Ohmiya K (2003) Molecular breeding of transgenic rice expressing a xylanase domain of the xynA gene from Clostridium thermocellum. Appl Microbiol Biotechnol 62(4):374–379

    CAS  PubMed  Google Scholar 

  82. Hyunjong B, Lee DS, Hwang I (2006) Dual targeting of xylanase to chloroplasts and peroxisomes as a means to increase protein accumulation in plant cells. J Exp Bot 57(1):161–169

    CAS  PubMed  Google Scholar 

  83. Pogorelko G, Fursova O, Lin M, Pyle E, Jass J, Zabotina OA (2011) Post-synthetic modification of plant cell walls by expression of microbial hydrolases in the apoplast. Plant Mol Biol 77(4–5):433–45

    CAS  PubMed  Google Scholar 

  84. Buanafina MM, Langdon T, Dalton S, Morris P (2012) Expression of a Trichoderma reesei beta-1,4 endo-xylanase in tall fescue modifies cell wall structure and digestibility and elicits pathogen defence responses. Planta 236(6):1757–74

    CAS  PubMed  Google Scholar 

  85. Tsai AY, Canam T, Gorzsas A, Mellerowicz EJ, Campbell MM, Master ER (2012) Constitutive expression of a fungal glucuronoyl esterase in Arabidopsis reveals altered cell wall composition and structure. Plant Biotechnol J 10(9):1077–87

    CAS  PubMed  Google Scholar 

  86. Borkhardt B, Harholt J, Ulvskov P, Ahring BK, Jorgensen B, Brinch-Pedersen H (2010) Autohydrolysis of plant xylans by apoplastic expression of thermophilic bacterial endo-xylanases. Plant Biotechnol J 8(3):363–74

    CAS  PubMed  Google Scholar 

  87. Chatterjee A, Das NC, Raha S, Babbit R, Huang Q, Zaitlin D et al (2010) Production of xylanase in transgenic tobacco for industrial use in bioenergy and biofuel applications. In Vitro Cellular and Developmental Biology Plant 46(2):198–209

    CAS  Google Scholar 

  88. Herbers K, Wilke I, Sonnewald U (1995) A thermostable xylanase from Closteridium thermocellum expressed at high levels in the apoplast of transgenic tobacco has no detrimental effects and is easily purified. Biotechnology 13:63–66

    CAS  Google Scholar 

  89. 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. Proc Natl Acad Sci U S A 107(2):616–21

    PubMed Central  CAS  PubMed  Google Scholar 

  90. Gou JY, Miller LM, Hou G, Yu XH, Chen XY, Liu CJ (2012) Acetylesterase-mediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell 24(1):50–65

    PubMed Central  CAS  PubMed  Google Scholar 

  91. Orfila C, Dal Degan F, Jorgensen B, Scheller HV, Ray PM, Ulvskov P (2012) Expression of mung bean pectin acetyl esterase in potato tubers: effect on acetylation of cell wall polymers and tuber mechanical properties. Planta 236:185–196

    CAS  PubMed  Google Scholar 

  92. Biswal AK, Soeno K, Gandla ML, Immerzeel P, Pattathil S, Lucenius J et al (2014) Aspen pectate lyase PtxtPL1-27 mobilizes matrix polysaccharides from woody tissues and improves saccharification yield. Biotechnol Biofuels 7:11

    PubMed Central  PubMed  Google Scholar 

  93. Osteryoung KW, Toenjes K, Hall B, Winkler V, Bennett AB (1990) Analysis of Tomato Polygalacturonase Expression in Transgenic Tobacco. Plant Cell 2:1239–1248

    PubMed Central  CAS  PubMed  Google Scholar 

  94. Atkinson RG, Schroder R, Hallett IC, Cohen D, MacRae EA (2002) Overexpression of polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involving changes in cell adhesion. Plant Physiol 129(1):122–133

    PubMed Central  CAS  PubMed  Google Scholar 

  95. Musialak M, Wróbel-Kwiatkowska M, Kulma A, Starzycka E, Szopa J (2008) Improving retting of fibre through genetic modification of flax to express pectinases. Transgenic Res 17:133–147

    CAS  PubMed  Google Scholar 

  96. Obro J, Borkhardt B, Harholt J, Skjot M, Willats WGT, Ulvskov P (2009) Simultaneous in vivo truncation of pectic side chains. Transgenic Res 18:961–9

    CAS  PubMed  Google Scholar 

  97. Prieto-Alcedo M, Veiga-Crespo P, Poza M, Coronado C, Zarra I, Villa TG (2011) Expression of a yeast polygalacturonase gene in Arabidopsis thaliana. Biol Plant 55(2):349–352

    CAS  Google Scholar 

  98. Capodicasa C, Vairo D, Zabotina O, McCartney L, Caprari C, Mattei B et al (2004) Targeted modification of homogalacturonan by transgenic expression of a fungal polygalacturonase alters plant growth. Plant Physiol 135(3):1294–1304

    PubMed Central  CAS  PubMed  Google Scholar 

  99. Oxenboll Sorensen S, Pauly M, Bush M, Skjot M, McCann MC, Borkhardt B et al (2000) Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-beta-D-galactanase. Proc Natl Acad Sci U S A 97(13):7639–7644

    PubMed Central  CAS  PubMed  Google Scholar 

  100. Skjøt M, Kauppinen S, Kofod LV, Fuglsang C, Pauly M, Dalbøge H et al (2001) Functional cloning of an endoarabinanase from Aspergillus aculeatus and its heterologous expression in A. or oryzae and tobacco. Mol Gen Genomics 265(5):913–921

    Google Scholar 

  101. Oomen RJ, Doeswijk-Voragen CH, Bush MS, Vincken JP, Borkhardt B, van den Broek LAM et al (2002) In muro fragmentation of the rhamnogalacturonan I backbone in potato (Solanum tuberosum L.) results in a reduction and altered location of the galactan and arabinan side-chains and abnormal periderm development. Plant J 30:403–413

    CAS  PubMed  Google Scholar 

  102. Boudart G, Charpentier M, Lafitte C, Martinez Y, Jauneau A, Gaulin E et al (2003) Elicitor activity of a fungal endopolygalacturonase in tobacco requires a functional catalytic site and cell wall localization. Plant Physiol 131:93–101

    PubMed Central  CAS  PubMed  Google Scholar 

  103. Hasunuma T, Fukusaki E, Kobayashi A (2003) Methanol production is enhanced by expression of an Aspergillus niger pectin methylesterase in tobacco cells. J Biotechnol 106:45–52

    CAS  PubMed  Google Scholar 

  104. Hasunuma T, Fukusaki E, Kobayashi A (2004) Expression of fungal pectin methylesterase in transgenic tobacco leads to alteration in cell wall metabolism and a dwarf phenotype. J Biotechnol 111(3):241–251

    CAS  PubMed  Google Scholar 

  105. Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D et al (2008) Transgenic expressionof a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146(2):669–681

    PubMed Central  CAS  PubMed  Google Scholar 

  106. Tsuji Y, Vanholme R, Tobimatsu Y, Ishikawa Y, Foster CE, Kamimura N et al (2015) Introduction of chemically labile substructures into Arabidopsis lignin through the use of LigD, the Cα-dehydrogenase from Sphingobium sp. strain SYK-6. Plant Biotechnol J. doi:10.1111/pbi.12316

    PubMed  Google Scholar 

  107. Eudes A, Sathitsuksanoh N, Baidoo EEK, George A, Liang Y, Yang F et al (2015) Expression of a bacterial 3-dehydroshikimate dehydratase reduces lignin content and improves biomass saccharification efficiency. Plant Biotechnol J. doi:10.1111/pbi.12310

    PubMed  Google Scholar 

  108. Obembe OO, Jacobsen E, Timmers J, Gilbert H, Blake AW, Knox JP et al (2007) Promiscuous, non-catalytic, tandem carbohydrate-binding modules modulate the cell-wall structure and development of transgenic tobacco (Nicotiana tabacum) plants. J Plant Res 120(5):605–17

    PubMed Central  CAS  PubMed  Google Scholar 

  109. Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL et al (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20(11):3080–3093

    PubMed Central  CAS  PubMed  Google Scholar 

  110. Safra-Dassa L, Shani Z, Danin A, Roiz L, Shoseyov O, Wolf S (2006) Growth modulation of transgenic potato plants by heterologous expression of bacterial carbohydrate-binding module. Mol Breed 17(4):355–364

    CAS  Google Scholar 

  111. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45

    PubMed Central  CAS  PubMed  Google Scholar 

  112. Fushinobu S (2014) Metalloproteins: A new face for biomass breakdown. Nat Chem Biol 10:88–99

    CAS  PubMed  Google Scholar 

  113. Menkhaus TJ, Bai Y, Zhang Z, Nikolov L, Glatz CE (2004) Considerations for the recovery of recombinant proteins from plants. Biotechnol Prog 20(4):1001–14

    CAS  PubMed  Google Scholar 

  114. Brunecky R, Selig MJ, Vinzant TB, Himmel ME, Lee D, Blaylock MJ et al (2011) In planta expression of A. Cellulolyticus Cel5A endocellulase reduces cell wall recalcitrance in tobacco and maize. Biotechnol Biofuels 4(1):1

    PubMed Central  CAS  PubMed  Google Scholar 

  115. Klose H, Röder J, Girfoglio M, Fischer R, Commandeur U (2012) Hyperthermophilic endoglucanase for in planta lignocellulose conversion. Biotechnol Biofuels 5:63

    PubMed Central  CAS  PubMed  Google Scholar 

  116. Guerriero G, Fugelstad J, Bulone V (2010) What do we really know about cellulose biosynthesis in higher plants? J Integr Plant Biol 52(2):161–75

    CAS  PubMed  Google Scholar 

  117. Harris D, Stork J, DeBolt S (2009) Genetic modification in cellulose-synthase reduces crystallinity and improves biochemical conversion to fermentable sugar. Glob Chang Biol Bioenergy 1:51–61

    CAS  Google Scholar 

  118. Shrinivas D, Savitha G, Raviranjan K, Naik GR (2010) A highly thermostable alkaline cellulase- free xylanase from thermoalkalophilic bacillus sp. JB 99 suitable for paper and pulp industry: purification and characterization. Appl Biochem Biotechnol 162:2049–57

    CAS  PubMed  Google Scholar 

  119. Wu AM, Hornblad E, Voxeur A, Gerber L, Rihouey C, Lerouge P et al (2010) Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiol 153:542–54

    PubMed Central  CAS  PubMed  Google Scholar 

  120. Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326–38

    CAS  PubMed  Google Scholar 

  121. Subramaniyan S, Prema P (2002) Biotechnology of microbial xylanases: enzymology, molecular biology, and application. Crit Rev Biotechnol 22:33–64

    CAS  PubMed  Google Scholar 

  122. Jabbour D, Borrusch MS, Banerjee G, Walton JD (2013) Enhancement of fermentable sugar yields by alpha-xylosidase supplementation of commercial cellulases. Biotechnol Biofuels 6(1):58

    PubMed Central  CAS  PubMed  Google Scholar 

  123. Alvira P, Negro MJ, Ballesteros M (2011) Effect of endoxylanase and a-L-arabinofuranosidase supplementation on the enzymatic hydrolysis of steam exploded wheat straw. Bioresour Technol 102:4552–8

    CAS  PubMed  Google Scholar 

  124. Latha Gandla M, Derba-Maceluch M, Liu X, Gerber L, Master ER, Mellerowicz EJ et al (2014) Expression of a fungal glucuronoyl esterase in populus: effects on wood properties and saccharification efficiency. Phytochemistry 112:210–20

    PubMed  Google Scholar 

  125. Brummel DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–40

    Google Scholar 

  126. Willats WG, Orfila C, Limberg G, Buchholt HC, van Alebeek GJ, Voragen AG et al (2001) Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem 276(22):19404–13

    CAS  PubMed  Google Scholar 

  127. Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12(6):267–77

    CAS  PubMed  Google Scholar 

  128. Francocci F, Bastianelli E, Lionetti V, Ferrari S, De Lorenzo G, Bellincampi D et al (2013) Analysis of pectin mutants and natural accessions of Arabidopsis highlights the impact of de-methyl-esterified homogalacturonan on tissue saccharification. Biotechnol Biofuels 6:163

    PubMed Central  CAS  PubMed  Google Scholar 

  129. Vincken JP (2003) If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol 132(4):1781–9

    PubMed Central  CAS  PubMed  Google Scholar 

  130. Ulskov P, Wium H, Bruce D, Jorgensen B, Qvist KB, Skjøt M et al (2005) Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 230:609–20

    Google Scholar 

  131. Van Acker R, Vanholme R, Storme V, Mortimer JC, Dupree P, Boerjan W (2013) Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana. Biotechnol Biofuels 6:46

    PubMed Central  PubMed  Google Scholar 

  132. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11(3):278–85

    CAS  PubMed  Google Scholar 

  133. Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber J, Ralph J et al (2012) Metabolic engineering of novel lignin in biomass crops. New Phytol 196:978–1000

    CAS  PubMed  Google Scholar 

  134. Poovaiah CR, Nageswara-Rao M, Soneji JR, Baxter HL, Stewart CN (2014) Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks. Plant Biotechnol J 12(9):1163–73

    CAS  PubMed  Google Scholar 

  135. Vanholme R, Cesarino I, Rataj K, Xiao Y, Sundin L, Goeminne G et al (2013) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway. Science 341:1103–1106

    CAS  PubMed  Google Scholar 

  136. Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25(7):759–61

    CAS  PubMed  Google Scholar 

  137. Grabber JH (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci 45(3):820

    CAS  Google Scholar 

  138. Ciesielski PN, Resch MG, Hewetson B, Killgore JP, Curtin A, Anderson N et al (2014) Engineering plant cell walls: tuning lignin monomer composition for deconstructable biofuel feedstocks or resilient biomaterials. Green Chem 16(5):2627–35

    CAS  Google Scholar 

  139. 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 Biofuels 3:27

    PubMed Central  CAS  PubMed  Google Scholar 

  140. Wilkerson CG, Mansfield SD, Lu F, Withers S, Park J-Y, Karlen SD et al (2014) Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 344(6179):90–3

    CAS  PubMed  Google Scholar 

  141. Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407(6802):321–6

    CAS  PubMed  Google Scholar 

  142. Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev MMBR 70(2):283–95

    CAS  PubMed  Google Scholar 

  143. Levy I, Shoseyov O (2002) Cellulose-binding domains: biotechnological applications. Biotechnol Adv 20:191–213

    CAS  PubMed  Google Scholar 

  144. Shani Z, Shpigel E, Roiz L, Goren R, Vinocur B, Tzfira T et al (1999) Cellulose-binding domain increases cellulose synthase activity in acetobacter xylinum and biomass of transgenic plants. In: Altman A, Ziv M, Izhar S (eds) Plant biotechnology and in vitro biology in the 21st century. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 213–8

    Google Scholar 

  145. Shoseyov O, Levy I, Shani Z, Mansfield SD (2003) Modulation of wood fibers and paper by cellulose-binding domains. In S D Mansfield and J N Saddler (eds), Application of enzymes to lignocellulosics ACS symposium series 855 American Chemical Society, Washington DC, 116–31

  146. Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A 97:9783–8

    PubMed Central  CAS  PubMed  Google Scholar 

  147. Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–98

    PubMed Central  CAS  PubMed  Google Scholar 

  148. Madoka Gray M, Blomquist K, McQueen-Mason SJ, Teeri TT, Sundberg B, Mellerowicz EJ (2008) Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotechnol J 6(1):62–72

    Google Scholar 

  149. Shoseyov O, Shani Z, Abramson M, Barimboim N, Dekel M, Lapidot S (2008) Transgenic plants containing soluble cell wall polysaccharides. WO 2008120194 A2

  150. Preis I, Lapidot S, Abramson M, Shoseyov (2013) Modifications of cell wall properties by production of recombinant resilin composites in transgenic plants. XIII Cell Wall Meeting, Nantes, France

  151. Barimbiom-Moshe N (2008) Cloning and characterization of levansucrase from Erwina amylovora in Eucalyptus, Ph.D. thesis, Hebrew University of Jerusalem

  152. Vanholme B, Vanholme R, Turumtay H, Goeminne G, Cesarino I, Goubet F et al (2014) Accumulation of N-acetylglucosamine oligomers in the plant cell wall affects plant architecture in a dose-dependent and conditional manner. Plant Physiol 165(1):290–308

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author would like to thank Bartel Vanholme and Godelieve Gheysen for help  in formatting the manuscript and Ali Akyüz for formatting drawing. HT is indebted to the Scientific and Technological Research Council of Turkey (TUBITAK) for a partial predoctoral fellowship.

Author information

Author notes

  1. Halbay Turumtay

    Present address: Department of Energy System Engineering, Karadeniz Technical University, 61830, Trabzon, Turkey

Authors and Affiliations

  1. Department of Molecular Biotechnology, Ghent University, Coupure links 653, 9000, Ghent, Belgium

    Halbay Turumtay

Authors
  1. Halbay Turumtay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Halbay Turumtay.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turumtay, H. Cell Wall Engineering by Heterologous Expression of Cell Wall-Degrading Enzymes for Better Conversion of Lignocellulosic Biomass into Biofuels. Bioenerg. Res. 8, 1574–1588 (2015). https://doi.org/10.1007/s12155-015-9624-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12155-015-9624-z

Keywords

Search

Navigation