Abstract
The discovery of microbial expansins emerged from studies of the mechanism of plant cell growth and the molecular basis of plant cell wall extensibility. Expansins are wall-loosening proteins that are universal in the plant kingdom and are also found in a small set of phylogenetically diverse bacteria, fungi, and other organisms, most of which colonize plant surfaces. They loosen plant cell walls without detectable lytic activity. Bacterial expansins have attracted considerable attention recently for their potential use in cellulosic biomass conversion for biofuel production, as a means to disaggregate cellulosic structures by nonlytic means (“amorphogenesis”). Evolutionary analysis indicates that microbial expansins originated by multiple horizontal gene transfers from plants. Crystallographic analysis of BsEXLX1, the expansin from Bacillus subtilis, shows that microbial expansins consist of two tightly packed domains: the N-terminal domain D1 has a double-ψ β-barrel fold similar to glycosyl hydrolase family-45 enzymes but lacks catalytic residues usually required for hydrolysis; the C-terminal domain D2 has a unique β-sandwich fold with three co-linear aromatic residues that bind β-1,4-glucans by hydrophobic interactions. Genetic deletion of expansin in Bacillus and Clavibacter cripples their ability to colonize plant tissues. We assess reports that expansin addition enhances cellulose breakdown by cellulase and compare expansins with distantly related proteins named swollenin, cerato-platanin, and loosenin. We end in a speculative vein about the biological roles of microbial expansins and their potential applications. Advances in this field will be aided by a deeper understanding of how these proteins modify cellulosic structures.
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References
Andberg M, Penttila M, Saloheimo M (2015) Swollenin from Trichoderma reesei exhibits hydrolytic activity against cellulosic substrates with features of both endoglucanases and cellobiohydrolases. Bioresour Technol 181c:105–113. doi:10.1016/j.biortech.2015.01.024
Arantes V, Saddler JN (2010) Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis. Biotechnol Biofuels 3:4. doi:10.1186/1754-6834-3-4
Ashwini N, Srividya S (2013) Potentiality of Bacillus subtilis as biocontrol agent for management of anthracnose disease of chilli caused by Colletotrichum gloeosporioides OGC1. 3. Biotech 4(2):127–136. doi:10.1007/s13205-013-0134-4
Baccelli I, Luti S, Bernardi R, Scala A, Pazzagli L (2014) Cerato-platanin shows expansin-like activity on cellulosic materials. Appl Microbiol Biotechnol 98(1):175–184. doi:10.1007/s00253-013-4822-0
Baker JO, King MR, Adney WS, Decker SR, Vinzant TB, Lantz SE, Nieves RE, Thomas SR, Li LC, Cosgrove DJ, Himmel ME (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
Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A 110(17):E1621–E1630. doi:10.1073/pnas.1218984110
Boddi S, Comparini C, Calamassi R, Pazzagli L, Cappugi G, Scala A (2004) Cerato-platanin protein is located in the cell walls of ascospores, conidia and hyphae of Ceratocystis fimbriata f. sp. platani. FEMS Microbiol Lett 233(2):341–346. doi:10.1016/j.femsle.2004.03.001
Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382(Pt 3):769–781
Boron AK, Van Loock B, Suslov D, Markakis MN, Verbelen J-P, Vissenberg K (2014) Over-expression of AtEXLA2 alters etiolated arabidopsis hypocotyl growth. Ann Botany. doi:10.1093/aob/mcu221
Bouzarelou D, Billini M, Roumelioti K, Sophianopoulou V (2008) EglD, a putative endoglucanase, with an expansin like domain is localized in the conidial cell wall of Aspergillus nidulans. Fungal Gen Bio 45(6):839–850. doi:10.1016/j.fgb.2008.03.001
Bras JL, Cartmell A, Carvalho AL, Verze G, Bayer EA, Vazana Y, Correia MA, Prates JA, Ratnaparkhe S, Boraston AB, Romao MJ, Fontes CM, Gilbert HJ (2011) Structural insights into a unique cellulase fold and mechanism of cellulose hydrolysis. Proc Natl Acad Sci U S A 108(13):5237–5242
Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from trichoderma, in plant root colonization. Plant Physiol 147(2):779–789
Brunecky R, Alahuhta M, Xu Q, Donohoe BS, Crowley MF, Kataeva IA, Yang SJ, Resch MG, Adams MW, Lunin VV, Himmel ME, Bomble YJ (2013) Revealing nature’s cellulase diversity: the digestion mechanism of Caldicellulosiruptor bescii CelA. Science 342(6165):1513–1516. doi:10.1126/science.1244273
Bunterngsook B, Mhuantong W, Champreda V, Thamchaiphenet A, Eurwilaichitr L (2014) Identification of novel bacterial expansins and their synergistic actions on cellulose degradation. Bioresour Technol 159C:64–71. doi:10.1016/j.biortech.2014.02.004
Bunterngsook B, Eurwilaichitr L, Thamchaipenet A, Champreda V (2015) Binding characteristics and synergistic effects of bacterial expansins on cellulosic and hemicellulosic substrates. Bioresour Technol 176:129–135. doi:10.1016/j.biortech.2014.11.042
Carvalho CC, Phan NN, Chen Y, Reilly PJ (2014) Carbohydrate binding module tribes. Biopolymers. doi:10.1002/bip.22584
Chabre H, Gouyon B, Huet A, Baron-Bodo V, Nony E, Hrabina M, Fenaille F, Lautrette A, Bonvalet M, Maillere B, Bordas-Le Floch V, Van Overtvelt L, Jain K, Ezan E, Batard T, Moingeon P (2010) Molecular variability of group 1 and 5 grass pollen allergens between Pooideae species: implications for immunotherapy. Clin Exp Allergy 40(3):505–519. doi:10.1111/j.1365-2222.2009.03380.x
Cosgrove DJ (1996) Plant cell enlargement and the action of expansins. Bioessays 18:533–540
Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407(6802):321–326
Cosgrove DJ (2001) Enhancement of accessibility of cellulose by expansins. US Patent 6:326,470
Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22:122–131. doi:10.1016/j.pbi.2014.11.001
Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci U S A 94(12):6559–6564
da Silva AJ, Gomez-Mendoza DP, Junqueira M, Domont GB, Ximenes Ferreira Filho E, de Sousa MV, Ricart CA (2012) Blue native-PAGE analysis of Trichoderma harzianum secretome reveals cellulases and hemicellulases working as multienzymatic complexes. Proteomics 12(17):2729–2738. doi:10.1002/pmic.201200048
Darley CP, Li Y, Schaap P, McQueen-Mason SJ (2003) Expression of a family of expansin-like proteins during the development of Dictyostelium discoideum. FEBS Lett 546(2–3):416–418
Davies GJ, Tolley SP, Henrissat B, Hjort C, Schulein M (1995) Structures of oligosaccharide-bound forms of the endoglucanase V from Humicola insolens at 1.9 A resolution. Biochemistry 34(49):16210–16220
de Oliveira AL, Gallo M, Pazzagli L, Benedetti CE, Cappugi G, Scala A, Pantera B, Spisni A, Pertinhez TA, Cicero DO (2011) The structure of the elicitor cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double-psi beta-barrel fold and carbohydrate binding. J Biol Chem 286(20):17560–17568. doi:10.1074/jbc.M111.223644
Din N, Gilkes NR, Tekant B, Miller RC, Warren AJ, Kilburn DG (1991) Non-hydrolytic disruption of cellulose fibers by the binding domain of a bacterial cellulase. Bio Technol 9(11):1096–1099. doi:10.1038/Nbt1191-1096
Eibinger M, Ganner T, Bubner P, Rosker S, Kracher D, Haltrich D, Ludwig R, Plank H, Nidetzky B (2014) Cellulose surface degradation by a lytic polysaccharide monooxygenase and its effect on cellulase hydrolytic efficiency. J Biol Chem 289(52):35929–35938. doi:10.1074/jbc.M114.602227
Eriksson T, Borjesson J, Tjerneld F (2002) Mechanism of surfactant effect in enzymatic hydrolysis of lignocellulose. Enzyme Microbial Technol 31(3):353–364
Eriksson J, Malmsten M, Tiberg F, Callisen TH, Damhus T, Johansen KS (2005) Model cellulose films exposed to H. insolens glucoside hydrolase family 45 endo-cellulase—the effect of the carbohydrate-binding module. J Colloid Interface Sci 285(1):94–99
Frias M, Gonzalez C, Brito N (2011) BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 192(2):483–495. doi:10.1111/j.1469-8137.2011.03802.x
Frischmann A, Neudl S, Gaderer R, Bonazza K, Zach S, Gruber S, Spadiut O, Friedbacher G, Grothe H, Seidl-Seiboth V (2013) Self-assembly at air/water interfaces and carbohydrate binding properties of the small secreted protein EPL1 from the fungus Trichoderma atroviride. J Biol Chem 288(6):4278–4287. doi:10.1074/jbc.M112.427633
Gartemann KH, Kirchner O, Engemann J, Grafen I, Eichenlaub R, Burger A (2003) Clavibacter michiganensis subsp michiganensis: first steps in the understanding of virulence of a Gram-positive phytopathogenic bacterium. J Biotech 106(2–3):179–191
Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ (2011) Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 286(19):16814–16823
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 U S A 109(37):14830–14835. doi:10.1073/pnas.1213200109
Georgelis N, Nikolaidis N, Cosgrove DJ (2014) Biochemical analysis of expansin-like proteins from microbes. Carbohydr Polym 100:17–23. doi:10.1016/j.carbpol.2013.04.094
Gilbert HJ (2010) The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol 153(2):444–455. doi:10.1104/pp. 110.156646
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. Bioresour Technol 142:498–503. doi:10.1016/j.biortech.2013.05.053
Gourlay K, Hu J, Arantes V, Penttila M, Saddler JN (2014) The use of carbohydrate binding modules (CBMs) to monitor changes in fragmentation and cellulose fibre surface morphology during Cellulase and Swollenin induced deconstruction of lignocellulosic substrates. J Biol Chem. doi:10.1074/jbc.M114.627604
Habibi Y, Lucia LA, Rojas OJ (2010) Cellulose nanocrystals: chemistry, self-assembly, and applications. Chem Rev 110(6):3479–3500. doi:10.1021/cr900339w
Hemsworth GR, Davies GJ, Walton PH (2013) Recent insights into copper-containing lytic polysaccharide mono-oxygenases. Curr Opin Struct Biol 23(5):660–668. doi:10.1016/j.sbi.2013.05.006
Hemsworth GR, Henrissat B, Davies GJ, Walton PH (2014) Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nature Chem Biol 10(2):122–126. doi:10.1038/nchembio.1417
Henrissat B, Teeri TT, Warren RAJ (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett 425(2):352–354
Herve C, Rogowski A, Blake AW, Marcus SE, Gilbert HJ, Knox JP (2010) Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Proc Natl Acad Sci U S A 107(34):15293–15298. doi:10.1073/pnas.1005732107
Jager G, Girfoglio M, Dollo F, Rinaldi R, Bongard H, Commandeur U, Fischer R, Spiess AC, Buchs J (2011) How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels 4(1):33. doi:10.1186/1754-6834-4-33
Jahr H, Dreier J, Meletzus D, Bahro R, Eichenlaub R (2000) The endo-beta-1,4-glucanase CelA of Clavibacter michiganensis subsp michiganensis is a pathogenicity determinant required for induction of bacterial wilt of tomato. Mol Plant Microbe Inter 13(7):703–714
Kang K, Wang S, Lai G, Liu G, Xing M (2013) Characterization of a novel swollenin from Penicillium oxalicum in facilitating enzymatic saccharification of cellulose. BMC Biotechnol 13:42. doi:10.1186/1472-6750-13-42
Kende H, Bradford K, Brummell D, Cho HT, Cosgrove D, Fleming A, 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(3):311–314. doi:10.1007/s11103-004-0158-6
Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S, Filee P, Charlier P, Joris B, Tabuchi A, Nikolaidis N, Cosgrove DJ (2008) Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci U S A 105(44):16876–16881
Kikuchi T, Li HM, Karim N, Kennedy MW, Moens M, Jones JT (2009) Identification of putative expansin-like genes from the pine wood nematode, Bursaphelenchus xylophilus, and evolution of the expansin gene family within the Nematoda. Nematol 11:355–364. doi:10.1163/156854109x446953
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(5):1342–1353. doi:10.1002/bit.22193
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(2):401–407
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. Appl Microbiol Biotechnol 97(12):5381–5388. doi:10.1007/s00253-012-4412-6
Kim IJ, Lee HJ, Choi IG, Kim KH (2014) Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-6001-3
Klemm D, Kramer F, Moritz S, Lindstrom T, Ankerfors M, Gray D, Dorris A (2011) Nanocelluloses: a new family of nature-based materials. Angewandte Chem Internl Ed 50(24):5438–5466
Laine MJ, Haapalainen M, Wahlroos T, Kankare K, Nissinen R, Kassuwi S, Metzler MC (2000) The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp sepedonicus plays a role in virulence and contains an expansin-like domain. Physiol Mol Plant Path 57(5):221–233. doi:10.1006/pmpp.2000.0301
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 Cells 29(4):379–385. doi:10.1007/s10059-010-0033-z
Lee DW, Seo JB, Kang JS, Koh SH, Lee SH, Koh YH (2012) Identification and characterization of expansins from Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae). Plant Path J 28(4):409–417. doi:10.5423/Ppj.Oa.08.2012.0122
Lehtio J, Sugiyama J, Gustavsson M, Fransson L, Linder M, Teeri TT (2003) The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc Natl Acad Sci U S A 100(2):484–489
Li ZC, Durachko DM, Cosgrove DJ (1993) An oat coleoptile wall protein that induces wall extension in vitro and that is antigenically related to a similar protein from cucumber hypocotyls. Planta 191:349–356
Li Y, Darley CP, Ongaro V, Fleming A, Schipper O, Baldauf SL, McQueen-Mason SJ (2002) Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol 128(3):854–864
Li LC, Bedinger PA, Volk C, Jones AD, Cosgrove DJ (2003) Purification and characterization of four beta-expansins (Zea m 1 isoforms) from maize pollen. Plant Physiol 132(4):2073–2085
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(9):e75022
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. doi:10.1016/j.jbiotec.2014.07.013
Maly T, Cui D, Griffin RG, Miller AF (2012) 1H dynamic nuclear polarization based on an endogenous radical. J Phys Chem B 116(24):7055–7065. doi:10.1021/jp300539j
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 U S A 91(14):6574–6578
McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107(1):87–100
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall expansion in plants. Plant Cell 4:1425–1433
Nakatani Y, Yamada R, Ogino C, Kondo A (2013) Synergetic effect of yeast cell-surface expression of cellulase and expansin-like protein on direct ethanol production from cellulose. Microb Cell Fact 12(1):66. doi:10.1186/1475-2859-12-66
Nardi C, Escudero C, Villarreal N, Martinez G, Civello PM (2013) The carbohydrate-binding module of Fragaria x ananassa expansin 2 (CBM-FaExp2) binds to cell wall polysaccharides and decreases cell wall enzyme activities “in vitro”. J Plant Res 126(1):151–159
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(2):376–386. doi:10.1093/molbev/mst206
Ogasawara S, Shimada N, Kawata T (2009) Role of an expansin-like molecule in Dictyostelium morphogenesis and regulation of its gene expression by the signal transducer and activator of transcription protein Dd-STATa. Devel Growth Diff 51(2):109–122. doi:10.1111/j.1440-169X.2009.01086.x
Olarte-Lozano M, Mendoza-Nunez MA, Pastor N, Segovia L, Folch-Mallol J, Martinez-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(4):e95638. doi:10.1371/journal.pone.0095638
Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158(4):1933–1943
Pastor N, Davila S, Perez-Rueda E, Segovia L, Martinez-Anaya C (2014) Electrostatic analysis of bacterial expansins. Proteins. doi:10.1002/prot.24718
Pazzagli L, Cappugi G, Manao G, Camici G, Santini A, Scala A (1999) Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani. J Biol Chem 274(35):24959–24964
Qin L, Kudla U, Roze EH, Goverse A, Popeijus H, Nieuwland J, Overmars H, Jones JT, Schots A, Smant G, Bakker J, Helder J (2004) Plant degradation: a nematode expansin acting on plants. Nature 427(6969):30
Quiroz-Castaneda RE, Martinez-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. doi:10.1186/1475-2859-10-8
Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99(4):1271–1274
Reid CW, Legaree BA, Clarke AJ (2007) Role of Ser216 in the mechanism of action of membrane-bound lytic transglycosylase B: further evidence for substrate-assisted catalysis. FEBS Lett 581(25):4988–4992. doi:10.1016/j.febslet.2007.09.037
Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssonen E, Bhatia A, Ward M, Penttila M (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269(17):4202–4211
Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6(12):242
Sampedro J, Guttman M, Li LC, Cosgrove DJ (2015) Evolutionary divergence of beta-expansin structure and function in grasses parallels emergence of distinctive primary cell wall traits. Plant J 81(1):108–120. doi:10.1111/tpj.12715
Scheurwater E, Reid CW, Clarke AJ (2008) Lytic transglycosylases: bacterial space-making autolysins. Internl J Biochem Cell Biol 40(4):586–591. doi:10.1016/j.biocel.2007.03.018
Seki Y, Kikuchi Y, Yoshimoto R, Aburai K, Kanai Y, Ruike T, Iwabata K, Goitsuka R, Sugawara F, Abe M, Sakaguchi K (2014) Promotion of crystalline cellulose degradation by expansins from Oryza sativa. Planta. doi:10.1007/s00425-014-2163-6
Shcherban TY, Shi J, Durachko DM, Guiltinan MJ, Mcqueen-Mason SJ, Shieh M, Cosgrove DJ (1995) Molecular cloning and sequence analysis of expansins—a highly conserved, multigene family of proteins that mediate cell wall extension in plants. Proc Natl Acad Sci U S A 92(20):9245–9249. doi:10.1073/pnas.92.20.9245
Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70(2):283–295. doi:10.1128/MMBR. 00028-05
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. Bioresource Technol 119:252–261. doi:10.1016/j.biortech.2012.05.098
Suzuki H, Vuong TV, Gong Y, Chan K, Ho CY, Master ER, Kondo A (2014) Sequence diversity and gene expression analyses of expansin-related proteins in the white-rot basidiomycete, Phanerochaete carnosa. Fungal Gen Biol 72:115–123. doi:10.1016/j.fgb.2014.05.008
Tabuchi A, Li LC, Cosgrove DJ (2011) Matrix solubilization and cell wall weakening by beta-expansin (group-1 allergen) from maize pollen. Plant J68(3):546–559
Takahashi H, Ayala I, Bardet M, De Paepe G, Simorre JP, Hediger S (2013) Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J Am Chem Soc 135(13):5105–5110. doi:10.1021/ja312501d
Thimm JC, Burritt DJ, Sims IM, Newman RH, Ducker WA, Melton LD (2002) Celery (Apium graveolens) parenchyma cell walls: cell walls with minimal xyloglucan. Physiol Plant 116(2):164–171
Tovar-Herrera OE, Batista-Garcia RA, Sanchez-Carbente Mdel R, Iracheta-Cardenas MM, Arevalo-Nino K, Folch-Mallol JL (2015) A novel expansin protein from the white-rot fungus Schizophyllum commune. PLoS One 10(3):e0122296 doi:10.1371/journal.pone.0122296
van Straaten KE, Dijkstra BW, Vollmer W, Thunnissen AM (2005) Crystal structure of MltA from Escherichia coli reveals a unique lytic transglycosylase fold. J Mol Biol 352(5):1068–1080. doi:10.1016/j.jmb.2005.07.067
Veneault-Fourrey C, Commun C, Kohler A, Morin E, Balestrini R, Plett J, Danchin E, Coutinho P, Wiebenga A, de Vries RP, Henrissat B, Martin F (2014) Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Gen Biol 72:168–181. doi:10.1016/j.fgb.2014.08.007
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(5):1353–1363. doi:10.1007/s00253-011-3421-1
Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M (2013) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci U S A 110(41):16444–16449. doi:10.1073/pnas.1316290110
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. doi:10.1016/j.bej.2013.12.018
Whitney SE, Gidley MJ, McQueen-Mason SJ (2000) Probing expansin action using cellulose/hemicellulose composites. Plant J 22(4):327–334
Wolf S, Hematy K, Hofte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407. doi:10.1146/annurev-arplant-042811-105449
Yan Z, He M-X, Bo W, Hu Q-C, Li Q, Zhao J (2012) Recombinant EXLX1 from Bacillus subtilis for enhancing enzymatic hydrolysis of corn stover with low cellulase loadings. African J Biotech 11:11126–11131. doi:10.5897/AJB11.3395
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. doi:10.1271/bbb.80124
Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ (2006) Crystal structure and activities of EXPB1 (Zea m 1), a beta-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci U S A 103(40):14664–14671
Yu H, Li L (2014) Phylogeny and molecular dating of the cerato-platanin-encoding genes. Gen Mol Biol 37(2):423–427
Zhang T, Mahgsoudy-Louyeh S, Tittmann B, Cosgrove DJ (2014) Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis. Cellulose 21:853–862
Zhao Z, Shklyaev OE, Nili A, Mohamed MNA, Kubicki JD, Crespi VH, Zhong LH (2013) Cellulose microfibril twist, mechanics, and implication for cellulose biosynthesis. J Phys Chem A 117(12):2580–2589. doi:10.1021/Jp3089929
Zhao Z, Crespi VH, Kubicki JD, Cosgrove DJ, Zhong L (2014) Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation. Cellulose 21:1025–1039. doi:10.1007/s10570-013-0041-1
Acknowledgments
This work was supported by United States Department of Energy Grant DE-FG02-84ER13179 to D.J.C. from the Office of Basic Energy Sciences.
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Georgelis, N., Nikolaidis, N. & Cosgrove, D.J. Bacterial expansins and related proteins from the world of microbes. Appl Microbiol Biotechnol 99, 3807–3823 (2015). https://doi.org/10.1007/s00253-015-6534-0
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DOI: https://doi.org/10.1007/s00253-015-6534-0