Applied Microbiology and Biotechnology

, Volume 99, Issue 9, pp 3807–3823 | Cite as

Bacterial expansins and related proteins from the world of microbes

  • Nikolaos Georgelis
  • Nikolas Nikolaidis
  • Daniel J. CosgroveEmail author


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.


Amorphogenesis Biofuels Cellulase synergism Expansin Plant-microbe interactions Swollenin 



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.


  1. 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 Google Scholar
  2. 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 PubMedCentralPubMedGoogle Scholar
  3. 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 Google Scholar
  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 PubMedGoogle Scholar
  5. 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 84–86:217–223PubMedGoogle Scholar
  6. 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 PubMedCentralPubMedGoogle Scholar
  7. 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 PubMedGoogle Scholar
  8. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382(Pt 3):769–781PubMedCentralPubMedGoogle Scholar
  9. 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 Google Scholar
  10. 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 Google Scholar
  11. 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):5237–5242PubMedCentralPubMedGoogle Scholar
  12. 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):779–789PubMedCentralPubMedGoogle Scholar
  13. 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 PubMedGoogle Scholar
  14. 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 Google Scholar
  15. 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 PubMedGoogle Scholar
  16. Carvalho CC, Phan NN, Chen Y, Reilly PJ (2014) Carbohydrate binding module tribes. Biopolymers. doi: 10.1002/bip.22584 Google Scholar
  17. 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 PubMedGoogle Scholar
  18. Cosgrove DJ (1996) Plant cell enlargement and the action of expansins. Bioessays 18:533–540PubMedGoogle Scholar
  19. Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407(6802):321–326PubMedGoogle Scholar
  20. Cosgrove DJ (2001) Enhancement of accessibility of cellulose by expansins. US Patent 6:326,470Google Scholar
  21. 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 PubMedGoogle Scholar
  22. 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):6559–6564PubMedCentralPubMedGoogle Scholar
  23. 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 PubMedGoogle Scholar
  24. 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):416–418PubMedGoogle Scholar
  25. 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):16210–16220PubMedGoogle Scholar
  26. 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 PubMedCentralPubMedGoogle Scholar
  27. 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 Google Scholar
  28. 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 PubMedCentralPubMedGoogle Scholar
  29. Eriksson T, Borjesson J, Tjerneld F (2002) Mechanism of surfactant effect in enzymatic hydrolysis of lignocellulose. Enzyme Microbial Technol 31(3):353–364Google Scholar
  30. 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):94–99PubMedGoogle Scholar
  31. 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 PubMedGoogle Scholar
  32. 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 PubMedCentralPubMedGoogle Scholar
  33. 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):179–191Google Scholar
  34. Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ (2011) Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 286(19):16814–16823PubMedCentralPubMedGoogle Scholar
  35. 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 PubMedCentralPubMedGoogle Scholar
  36. 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 PubMedGoogle Scholar
  37. 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 PubMedCentralPubMedGoogle Scholar
  38. 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 PubMedGoogle Scholar
  39. 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 PubMedGoogle Scholar
  40. Habibi Y, Lucia LA, Rojas OJ (2010) Cellulose nanocrystals: chemistry, self-assembly, and applications. Chem Rev 110(6):3479–3500. doi: 10.1021/cr900339w PubMedGoogle Scholar
  41. 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/ PubMedGoogle Scholar
  42. 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 Google Scholar
  43. 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):352–354PubMedGoogle Scholar
  44. 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 PubMedCentralPubMedGoogle Scholar
  45. 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 PubMedCentralPubMedGoogle Scholar
  46. 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):703–714Google Scholar
  47. 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 PubMedCentralPubMedGoogle Scholar
  48. 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 PubMedGoogle Scholar
  49. 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):16876–16881PubMedCentralPubMedGoogle Scholar
  50. 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 Google Scholar
  51. 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 PubMedGoogle Scholar
  52. 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):401–407PubMedGoogle Scholar
  53. 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 PubMedGoogle Scholar
  54. 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 Google Scholar
  55. 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):5438–5466Google Scholar
  56. 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 Google Scholar
  57. 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 PubMedGoogle Scholar
  58. 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 Google Scholar
  59. 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):484–489PubMedCentralPubMedGoogle Scholar
  60. 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 191:349–356Google Scholar
  61. 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):854–864PubMedCentralPubMedGoogle Scholar
  62. 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):2073–2085PubMedCentralPubMedGoogle Scholar
  63. 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):e75022PubMedCentralPubMedGoogle Scholar
  64. 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 PubMedGoogle Scholar
  65. 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 PubMedGoogle Scholar
  66. 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):6574–6578PubMedCentralPubMedGoogle Scholar
  67. 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):87–100PubMedCentralPubMedGoogle Scholar
  68. McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall expansion in plants. Plant Cell 4:1425–1433PubMedCentralPubMedGoogle Scholar
  69. 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 PubMedCentralPubMedGoogle Scholar
  70. 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):151–159PubMedGoogle Scholar
  71. 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 PubMedGoogle Scholar
  72. 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 Google Scholar
  73. 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 PubMedCentralPubMedGoogle Scholar
  74. 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):1933–1943PubMedCentralPubMedGoogle Scholar
  75. Pastor N, Davila S, Perez-Rueda E, Segovia L, Martinez-Anaya C (2014) Electrostatic analysis of bacterial expansins. Proteins. doi: 10.1002/prot.24718 Google Scholar
  76. 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):24959–24964PubMedGoogle Scholar
  77. 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):30PubMedGoogle Scholar
  78. 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 PubMedCentralPubMedGoogle Scholar
  79. Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99(4):1271–1274PubMedCentralPubMedGoogle Scholar
  80. 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 PubMedGoogle Scholar
  81. 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):4202–4211PubMedGoogle Scholar
  82. Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6(12):242PubMedCentralPubMedGoogle Scholar
  83. 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 PubMedGoogle Scholar
  84. 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 Google Scholar
  85. 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 PubMedGoogle Scholar
  86. 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 PubMedCentralPubMedGoogle Scholar
  87. 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 PubMedCentralPubMedGoogle Scholar
  88. 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 Google Scholar
  89. 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 Google Scholar
  90. 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):546–559Google Scholar
  91. 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 PubMedGoogle Scholar
  92. 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):164–171PubMedGoogle Scholar
  93. 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
  94. 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 PubMedGoogle Scholar
  95. 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 Google Scholar
  96. 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 PubMedGoogle Scholar
  97. 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 PubMedCentralPubMedGoogle Scholar
  98. 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 Google Scholar
  99. Whitney SE, Gidley MJ, McQueen-Mason SJ (2000) Probing expansin action using cellulose/hemicellulose composites. Plant J 22(4):327–334PubMedGoogle Scholar
  100. 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 PubMedGoogle Scholar
  101. 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 Google Scholar
  102. 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 PubMedGoogle Scholar
  103. 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):14664–14671PubMedCentralPubMedGoogle Scholar
  104. Yu H, Li L (2014) Phylogeny and molecular dating of the cerato-platanin-encoding genes. Gen Mol Biol 37(2):423–427Google Scholar
  105. 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 21:853–862Google Scholar
  106. 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 PubMedGoogle Scholar
  107. 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 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  • Nikolaos Georgelis
    • 1
  • Nikolas Nikolaidis
    • 2
  • Daniel J. Cosgrove
    • 3
    Email author
  1. 1.Simplot Plant SciencesJ.R. Simplot CompanyBoiseUSA
  2. 2.Department of Biological ScienceCalifornia State UniversityFullertonUSA
  3. 3.Department of BiologyPenn State UniversityUniversity ParkUSA

Personalised recommendations