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Research advances in expansins and expansion-like proteins involved in lignocellulose degradation

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An Erratum to this article was published on 01 March 2016

Abstract

Biofuel derived from lignocellulosic biomass has attracted considerable attention as a renewable energy source. Nevertheless, the conversion of lignocellulose into fermentable sugars is inherently difficult because of the complex structures of lignocelluloses. Accessory proteins, like expansins, have a non-hydrolytic disruptive effect on crystalline cellulose and can synergistically cooperate with cellulase to improve hydrolysis efficiency. This review summarizes recent studies on expansins and expansin-like proteins, in terms of their expression and purification, synergism in lignocellulose hydrolysis, structure–function studies and binding characteristics. Future research prospects are also presented. This review provides a discussion of expansins in the context of lignocellulose hydrolysis.

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References

  • Arantes V, Saddler JN (2010) Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of a morphogenesis. Biotechnol Biofuels 3:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Baccelli I, Luti S, Bernardi R, Scala A, Pazzagli L (2014) Cerato-platanin shows expansin-like activity on cellulosic materials. Appl Microbiol Biotechnol 98:175–184

    Article  CAS  PubMed  Google Scholar 

  • Baker JO, King MR, Adney WS (2000) Investigation of the cell-wall loosening protein expansin as a possible additive in the enzymatic saccharification of lignocellulosic biomass. Appl Biochem Biotechnol 84–86:217–223

    Article  PubMed  Google Scholar 

  • Beeson WT, Phillips CM, Cate JHD, Marletta MA (2012) Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J Am Chem Soc 134:890–892

    Article  CAS  PubMed  Google Scholar 

  • Bunterngsook B, Mhuantong W, Champreda V, Thamchaipenet A, Eurwilaichitr L (2014) Identification of novel bacterial expansins and their synergistic actions on cellulose degradation. Biores Technol 159:64–71

    Article  CAS  Google Scholar 

  • Bunterngsook B, Eurwilaichitr L, Thamchaipenet A, Champreda V (2015) Binding characteristics and synergistic effects of bacterial expansins on cellulosic and hemicellulosic substrates. Biores Technol 176:129–135

    Article  CAS  Google Scholar 

  • Chen XA, Ishida N, Todaka N, Nakamura R, Maruyama J, Takahashi H, Kitamoto K (2010) Promotion of efficient saccharification of crystalline cellulose by Aspergillus fumigatus Swo1. Appl Environ Microbiol 76:2556–2561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi D, Cho HT, Lee Y (2006) Expansins: expanding importance in plant growth and development. Physiol Plant 126:511–518

    CAS  Google Scholar 

  • Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol 38:109–124

    CAS  Google Scholar 

  • Cosgrove DJ (2001) Enhancement of accessibility of cellulose by expansins. US Patent 6326470 B1

  • Durachko DM, Cosgrove DJ (2009) Measuring plant cell wall extension (creep) induced by acidic pH and by alpha-expansin. J Vis Exp 11:1263

    Google Scholar 

  • Ekwe E, Morgenstern I, Tsang A, Storms R, Powlowski J (2013) Non-hydrolytic cellulose active proteins: research progress and potential application in biorefineries. Ind Biotechnol 9(3):123–131

    Article  CAS  Google Scholar 

  • Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ (2011) Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 286:16814–16823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georgelis N, Yennawar NH, Cosgrove DJ (2012) Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin. Proc Natl Acad Sci USA 109:14830–14835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georgelis N, Nikolaidis N, Cosgrove DJ (2014) Biochemical analysis of expansin-like proteins from microbes. Carbohydr Polym 100:17–23

    Article  CAS  PubMed  Google Scholar 

  • Gilbert H, Stalbrand H, Brumer H (2008) How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation. Curr Opin Plant Biol 11:338–348

    Article  CAS  PubMed  Google Scholar 

  • Gourlay K, Hu J, Arantes V, Andberg M, Saloheimo M, Penttila M, Saddler J (2013) Swollenin aids in the amorphogenesis step during the enzymatic hydrolysis of pretreated biomass. Biores Technol 142:498–503

    Article  CAS  Google Scholar 

  • Han Y, Chen H (2007) Synergism between corn stover protein and cellulase. Enzym Microb Technol 41:638–645

    Article  CAS  Google Scholar 

  • Haque MA, Cho KM, Barman DN, Kim MK, Yun HD (2015) A potential cellulose microfibril swelling enzyme isolated from Bacillus sp. AY8 enhances cellulose hydrolysis. Proc Biochem. doi:10.1016/j.procbio.2015.02.003

    Google Scholar 

  • Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807

    Article  CAS  PubMed  Google Scholar 

  • Hong J, Ye X, Zhang YH (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

    Article  CAS  PubMed  Google Scholar 

  • Huang C, Zong MH, Wu H, Liu QP (2009) Microbial oil production from rice straw hydrolysate by Trichosporon fermentans. Bioresour Technol 100:4535–4538

    Article  CAS  PubMed  Google Scholar 

  • Jäger G, Girfoglio M, Dollo F, Rinaldi R, Bongard H, Commandeur U, Fischer R, Spiess AC, Büchs J (2011) How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuel 4:33

    Article  Google Scholar 

  • Jungbauer A, Kaar W (2007) Current status of technical protein refolding. J Biotechnol 128:587–596

    Article  CAS  PubMed  Google Scholar 

  • Kang K, Wang SW, Lai GH, Liu G, Xing M (2013) Characterization of a novel swollenin from Penicillium oxalicum in facilitating enzymatic saccharification of cellulose. BMC Biotechnol 13:42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kende H, Bradford KJ, Brummell DA, Cho HT, Cosgrove DJ, Fleming AJ, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek LA (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314

    Article  CAS  PubMed  Google Scholar 

  • Kerff F, Amoroso A, Herman R et al (2008) Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci USA 105:16876–16881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim ES, Lee HJ, Bang WG, Choi IG, Kim KH (2009) Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose. Biotechnol Bioeng 102:1342–1353

    Article  CAS  PubMed  Google Scholar 

  • Kim IJ, Ko HJ, Kim TW, Choi IG, Kim KH (2013a) Characteristics of the binding of a bacterial expansin (BsEXLX1) to microcrystalline cellulose. Biotechnol Bioeng 110:401–407

    Article  CAS  PubMed  Google Scholar 

  • Kim IJ, Ko HJ, Kim TW, Nam KH, Choi IG, Kim KH (2013b) Binding characteristics of a bacterial expansin (BsEXLX1) for various types of pretreated lignocellulose. App Microbiol Biotechnol 97:5381–5388

    Article  CAS  Google Scholar 

  • Kim IJ, Lee HJ, Choi IG, Kim KH (2014) Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase. Appl Microbiol Biotechnol 98:8469–8480

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Lee S, Ko HJ, Kim KH, Choi IG (2010) An expansin-like protein from Hahella chejuensis binds cellulose and enhances cellulase activity. Mol Cell 29:379–385

    Article  CAS  Google Scholar 

  • Lee HJ, Kim IJ, Kim JF, Choi IG, Kim KH (2013) An expansin from the marine bacterium Hahella chejuensis acts synergistically with xylanase and enhances xylan hydrolysis. Biores Technol 149:516–519

    Article  CAS  Google Scholar 

  • Levasseur A, Saloheimo M, Navarro D, Andberg M, Monot F, Nakari-Setälä T, Asther M, Record E (2006) Production of a chimeric enzyme tool associating the Trichoderma reesei swollenin with the Aspergillus niger feruloyl esterase A for release of ferulic acid. App Microbiol Biotechnol 73:872–880

    Article  CAS  Google Scholar 

  • Levasseur A, Drula E, Lombard V, Coutinho P, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuel 6:41

    Article  CAS  Google Scholar 

  • Li LC, Bedinger PA, Volk C, Jones AD, Cosgrove DJ (2003) Purification and characterization of four β-expansins (Zea m 1 Isoforms) from maize pollen. Plant Physiol 132:2073–2085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin H, Shen Q, Zhan JM, Wang Q, Zhao YH (2013) Evaluation of bacterial expansin EXLX1 as a cellulase synergist for the saccharification of lignocellulosic agro-industrial wastes. PLoS ONE 8:e75022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Liu C, Ma Y, Hong J, Zhang M (2014) Heterologous expression and functional characterization of a novel cellulose-disruptive protein LeEXP2 from Lycopersicum esculentum. J Biotechnol 186:148–155

    Article  CAS  PubMed  Google Scholar 

  • Mansfield SD, Mooney C, Saddler JN (1999) Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol Prog 15:804–816

    Article  CAS  PubMed  Google Scholar 

  • Maurya DP, Singla A, Negi S (2015) An overview of key pretreatment processes for biological conversion of lignocellulosic biomass to bioethanol. 3 Biotech. doi:10.1007/s13205-015-0279-4

    PubMed Central  Google Scholar 

  • McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Ragauskas AJ (2014) Recent advances in understanding the role of cellulose accessibility in enzymatic hydrolysis of lignocellulosic substrates. Curr Opin Biotechnol 27:150–158

    Article  CAS  PubMed  Google Scholar 

  • Nikolaidis N, Doran N, Cosgrove DJ (2014) Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol Biol Evol 31:376–386

    Article  CAS  PubMed  Google Scholar 

  • Olarte-Lozano M, Mendoza-Nuñez MA, Pastor N, Segovia L, Folch-Mallol J, Martínez-Anaya C (2014) PcExl1 a novel acid expansin-like protein from the plant pathogen Pectobacterium carotovorum, binds cell walls differently to BsEXLX1. PLoS ONE 9:e95638

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin L, Kudla U, Roze EH et al (2004) Plant degradation: a nematode expansin acting on plants. Nature 427:30

    Article  CAS  PubMed  Google Scholar 

  • Quiroz-Castañeda RE, Martínez-Anaya C, Cuervo-Soto LI, Segovia L, Folch-Mallol JL (2011) Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta. Microb Cell Fact 10:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssönen E, Bhatia A, Ward M, Penttilä M (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269:4202–4211

    Article  CAS  PubMed  Google Scholar 

  • Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6:242

    Article  PubMed  PubMed Central  Google Scholar 

  • Seki Y, Kikuchi Y, Yoshimoto R, Aburai K, Kanai Y, Ruike T, Iwabata K, Goitsuka R, Sugawara F, Abe M, Sakaguchi K (2015) Promotion of crystalline cellulose degradation by expansins from Oryza sativa. Planta 241:83–93

    Article  CAS  PubMed  Google Scholar 

  • Singh P, Suman A, Tiwari P, Arya N, Gaur A, Shrivastava AK (2008) Biological pretreatment of sugarcane trash for its conversion to fermentable sugars. World J Microbiol Biotechnol 24:667–673

    Article  CAS  Google Scholar 

  • Suwannarangsee S, Bunterngsook B, Arnthong J, Paemanee A, Thamchaipenet A, Eurwilaichitr L, Laosiripojana N, Champreda V (2012) Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design. Biores Technol 119:252–261

    Article  CAS  Google Scholar 

  • Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villalonga ML, Díez P, Sánchez A, Gamella M, Pingarrón JM, Villalonga R (2014) Neoglycoenzymes. Chem Rev 114:4868–4917

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Cai J, Huang L, Lv Z, Zhang Y, Xu Z (2010) High-level expression and efficient purification of bioactive swollenin in Aspergillus oryzae. Appl Biochem Biotechnol 162:2027–2036

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Tang R, Tao J, Gao G, Wang X, Mu Y, Feng Y (2011) Quantitative investigation of non-hydrolytic disruptive activity on crystalline cellulose and application to recombinant swollenin. Appl Microbiol Biotechnol 91:1353–1363

    Article  CAS  PubMed  Google Scholar 

  • Wang WC, Liu C, Ma YY, Liu XW, Zhang K, Zhang MH (2014) Improved production of two expansin-like proteins in Pichia pastoris and investigation of their functional properties. Biochem Eng J 84:16–27

    Article  CAS  Google Scholar 

  • Whitney SE, Gidley MJ, McQueen-Mason SJ (2000) Probing expansin action using cellulose/hemicellulose composites. Plant J 22:327–334

    Article  CAS  PubMed  Google Scholar 

  • Yao Q, Sun TT, Liu WF, Chen GJ (2008) Gene cloning and heterologous expression of a novel endoglucanase, Swollenin, from Trichoderma pseudokoningii S38. Biosci Biotechnol Biochem 72(11):2799–2805

    Article  CAS  PubMed  Google Scholar 

  • Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ (2006) Crystal structure and activities of EXPB1 (Zea m1), a beta-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci USA 103:14664–14671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YH, Lynd LR (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol Bioeng 88:797–824

    Article  CAS  PubMed  Google Scholar 

  • Zhou QX, Lv XX, Zhang X, Meng XF, Chen GJ, Liu WF (2011) Evaluation of swollenin from Trichoderma pseudokoningii as a potential synergistic factor in the enzymatic hydrolysis of cellulose with low cellulase loadings. World J Microbiol Biotechnol 27:1905–1910

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by National Natural Science Foundation of China (NSFC-30900033).

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Correspondence to Yuanyuan Ma.

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Liu, X., Ma, Y. & Zhang, M. Research advances in expansins and expansion-like proteins involved in lignocellulose degradation. Biotechnol Lett 37, 1541–1551 (2015). https://doi.org/10.1007/s10529-015-1842-0

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