1932

Abstract

Expansins are small proteins that loosen plant cell walls and cellulosic materials without lytic activity. First discovered in plants, expansin genes are found in the genomes of numerous bacteria and fungi that interact with plants in pathogenic and mutualistic patterns, as well as in microbes that feed on plant debris. Horizontal gene transfer from plants to microbes and between microbes accounts for expansins’ irregular taxonomic distribution. Expansins facilitate plant colonization by , , and species, a list likely to grow as knowledge of microbial expansin function deepens. Studies have documented a synergistic action of expansins for cellulose digestion by cellulases, but only rarely to an extent that is commercially relevant. Expansins’ biophysical actions remain enigmatic because of limited understanding of cell wall structure. Deeper understanding of microbial expansins may lead to novel approaches for biomass deconstruction and biocontrol of plant diseases.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090816-093315
2017-09-08
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/71/1/annurev-micro-090816-093315.html?itemId=/content/journals/10.1146/annurev-micro-090816-093315&mimeType=html&fmt=ahah

Literature Cited

  1. Abbott DW, van Bueren AL. 1.  2014. Using structure to inform carbohydrate binding module function. Curr. Opin. Struct. Biol. 28:32–40 [Google Scholar]
  2. Allard-Massicotte R, Tessier L, Lecuyer F, Lakshmanan V, Lucier JF. 2.  et al. 2016. Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. mBio 7:e01664–16 [Google Scholar]
  3. Andberg M, Penttila M, Saloheimo M. 3.  2015. Swollenin from Trichoderma reesei exhibits hydrolytic activity against cellulosic substrates with features of both endoglucanases and cellobiohydrolases. Bioresour. Technol. 181:105–13 [Google Scholar]
  4. Arantes V, Saddler JN. 4.  2010. Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis. Biotechnol. Biofuels 3:4 [Google Scholar]
  5. Artzi L, Bayer EA, Morais S. 5.  2017. Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat. Rev. Microbiol. 15:83–95 [Google Scholar]
  6. Artzi L, Morag E, Shamshoum M, Bayer EA. 6.  2016. Cellulosomal expansin: functionality and incorporation into the complex. Biotechnol. Biofuels 9:61 [Google Scholar]
  7. Asaka O, Shoda M. 7.  1996. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl. Environ. Microbiol 62:4081–5 [Google Scholar]
  8. Baccelli I, Luti S, Bernardi R, Scala A, Pazzagli L. 8.  2014. Cerato-platanin shows expansin-like activity on cellulosic materials. Appl. Microbiol. Biotechnol. 98:175–84 [Google Scholar]
  9. Bais HP, Fall R, Vivanco JM. 9.  2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–19 [Google Scholar]
  10. Baker JO, King MR, Adney WS, Decker SR, Vinzant TB. 10.  et al. 2000. Investigation of the cell-wall loosening protein expansin as a possible additive in the enzymatic saccharification of lignocellulosic biomass. Appl. Biochem. Biotechnol. 84–86:217–23 [Google Scholar]
  11. Balestrini R, Bonfante P. 11.  2014. Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front. Plant Sci. 5:237 [Google Scholar]
  12. Balestrini R, Cosgrove DJ, Bonfante P. 12.  2005. Differential location of alpha-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220:889–99 [Google Scholar]
  13. Beckham GT, Matthews JF, Peters B, Bomble YJ, Himmel ME, Crowley MF. 13.  2011. Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs. J. Phys. Chem. B 115:4118–27 [Google Scholar]
  14. Benitez T, Rincon AM, Limon MC, Codon AC. 14.  2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7:249–60 [Google Scholar]
  15. Bergenstrahle M, Wohlert J, Himmel ME, Brady JW. 15.  2010. Simulation studies of the insolubility of cellulose. Carbohydr. Res. 345:2060–66 [Google Scholar]
  16. Bohlmann H, Sobczak M. 16.  2014. The plant cell wall in the feeding sites of cyst nematodes. Front. Plant Sci. 5:89 [Google Scholar]
  17. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 17.  2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382:769–81 [Google Scholar]
  18. Brotman Y, Briff E, Viterbo A, Chet I. 18.  2008. Role of swollenin, an expansin-like protein from trichoderma, in plant root colonization. Plant Physiol 147:779–89 [Google Scholar]
  19. Bunterngsook B, Eurwilaichitr L, Thamchaipenet A, Champreda V. 19.  2015. Binding characteristics and synergistic effects of bacterial expansins on cellulosic and hemicellulosic substrates. Bioresour. Technol. 176:129–35 [Google Scholar]
  20. Bunterngsook B, Mhuantong W, Champreda V, Thamchaipenet A, Eurwilaichitr L. 20.  2014. Identification of novel bacterial expansins and their synergistic actions on cellulose degradation. Bioresour. Technol. 159C:64–71 [Google Scholar]
  21. Carmona C, Langan P, Smith JC, Petridis L. 21.  2015. Why genetic modification of lignin leads to low-recalcitrance biomass. Phys. Chem. Chem. Phys. 17:358–64 [Google Scholar]
  22. Castillo RM, Mizuguchi K, Dhanaraj V, Albert A, Blundell TL, Murzin AG. 22.  1999. A six-stranded double-psi beta barrel is shared by several protein superfamilies. Structure 7:227–36 [Google Scholar]
  23. Cazorla FM, Romero D, Pérez-García A, Lugtenberg BJJ, de Vicente A, Bloemberg G. 23.  2007. Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J. Appl. Microbiol. 103:1950–59 [Google Scholar]
  24. Chen C, Cui Z, Song X, Liu YJ, Cui Q, Feng Y. 24.  2016. Integration of bacterial expansin-like proteins into cellulosome promotes the cellulose degradation. Appl. Microbiol. Biotechnol. 100:2203–12 [Google Scholar]
  25. Cosgrove DJ. 25.  2014. Re-constructing our models of cellulose and primary cell wall assembly. Curr. Opin. Plant Biol. 22C:122–31 [Google Scholar]
  26. Cosgrove DJ. 26.  2015. Plant expansins: diversity and interactions with plant cell walls. Curr. Opin. Plant Biol. 25:162–72 [Google Scholar]
  27. Cosgrove DJ. 27.  2016. Catalysts of plant cell wall loosening. F1000Research 5:119 https://doi.org/10.12688/f1000research.7180.1 [Crossref] [Google Scholar]
  28. Cosgrove DJ. 28.  2016. Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J. Exp. Bot. 67:463–76 [Google Scholar]
  29. Cosgrove DJ, Hepler NK, Wagner ER, Durachko DM. 29.  2017. Measuring the biomechanical loosening action of bacterial expansins on paper and plant cell walls. Protein-Carbohydrate Interactions: Methods and Protocols 1588 DB Abbott, A Lammerts van Bueren 157–65 New York: Springer [Google Scholar]
  30. Crutcher FK, Moran-Diez ME, Ding S, Liu J, Horwitz BA. 30.  et al. 2015. A paralog of the proteinaceous elicitor SM1 is involved in colonization of maize roots by Trichoderma virens. Fungal Biol. 119:476–86 [Google Scholar]
  31. Danhorn T, Fuqua C. 31.  2007. Biofilm formation by plant-associated bacteria. Annu. Rev. Microbiol. 61:401–22 [Google Scholar]
  32. Darley CP, Li Y, Schaap P, McQueen-Mason SJ. 32.  2003. Expression of a family of expansin-like proteins during the development of Dictyostelium discoideum. FEBS Lett. 546:416–18 [Google Scholar]
  33. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A. 33.  et al. 2012. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414–30 [Google Scholar]
  34. Dermatsev V, Weingarten-Baror C, Resnick N, Gadkar V, Wininger S. 34.  et al. 2010. Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Mol. Plant Pathol 11:121–35 [Google Scholar]
  35. Durachko DM, Cosgrove DJ. 35.  2009. Measuring plant cell wall extension (creep) induced by acidic pH and by alpha-expansin. J. Vis. Exp. 11:1263 [Google Scholar]
  36. Eibinger M, Sigl K, Sattelkow J, Ganner T, Ramoni J. 36.  et al. 2016. Functional characterization of the native swollenin from Trichoderma reesei: study of its possible role as C1 factor of enzymatic lignocellulose conversion. Biotechnol. Biofuels 9:178 [Google Scholar]
  37. Eichenlaub R, Gartemann KH. 37.  2011. The Clavibacter michiganensis subspecies: molecular investigation of gram-positive bacterial plant pathogens. Annu. Rev. Phytopathol. 49:445–64 [Google Scholar]
  38. Frias M, Gonzalez C, Brito N. 38.  2011. BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 192:483–95 [Google Scholar]
  39. Gal TZ, Aussenberg ER, Burdman S, Kapulnik Y, Koltai H. 39.  2006. Expression of a plant expansin is involved in the establishment of root knot nematode parasitism in tomato. Planta 224:155–62 [Google Scholar]
  40. Gartemann KH, Kirchner O, Engemann J, Grafen I, Eichenlaub R, Burger A. 40.  2003. Clavibacter michiganensis subsp. michiganensis: first steps in the understanding of virulence of a gram-positive phytopathogenic bacterium. J. Biotechnol 106:179–91 [Google Scholar]
  41. Georgelis N, Nikolaidis N, Cosgrove DJ. 41.  2014. Biochemical analysis of expansin-like proteins from microbes. Carbohydr. Polym. 100:17–23 [Google Scholar]
  42. Georgelis N, Nikolaidis N, Cosgrove DJ. 42.  2015. Bacterial expansins and related proteins from the world of microbes. Appl. Microbiol. Biotechnol. 99:3807–23 [Google Scholar]
  43. Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ. 43.  2011. Structure-function analysis of the bacterial expansin EXLX1. J. Biol. Chem. 286:16814–23 [Google Scholar]
  44. Georgelis N, Yennawar NH, Cosgrove DJ. 44.  2012. Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin. PNAS 109:14830–35 [Google Scholar]
  45. Gomes EV, Costa MdN, Paula RGd, Azevedo RRd, Silva FLd. 45.  et al. 2015. The Cerato-Platanin protein Epl-1 from Trichoderma harzianum is involved in mycoparasitism, plant resistance induction and self cell wall protection. Sci. Rep. 5:17998 [Google Scholar]
  46. Gourlay K, Hu J, Arantes V, Andberg M, Saloheimo M. 46.  et al. 2013. Swollenin aids in the amorphogenesis step during the enzymatic hydrolysis of pretreated biomass. Bioresour. Technol. 142:498–503 [Google Scholar]
  47. Gourlay K, Hu J, Arantes V, Penttila M, Saddler JN. 47.  2015. The use of carbohydrate binding modules (CBMs) to monitor changes in fragmentation and cellulose fiber surface morphology during cellulase- and swollenin-induced deconstruction of lignocellulosic substrates. J. Biol. Chem. 290:2938–45 [Google Scholar]
  48. Grijseels S, Nielsen JC, Randelovic M, Nielsen J, Nielsen KF. 48.  et al. 2016. Penicillium arizonense, a new, genome sequenced fungal species, reveals a high chemical diversity in secreted metabolites. Sci. Rep. 6:35112 [Google Scholar]
  49. Haegeman A, Kyndt T, Gheysen G. 49.  2010. The role of pseudo-endoglucanases in the evolution of nematode cell wall-modifying proteins. J. Mol. Evol. 70:441–52 [Google Scholar]
  50. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 50.  2004. Trichoderma species—opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2:43–56 [Google Scholar]
  51. Hervé C, Rogowski A, Blake AW, Marcus SE, Gilbert HJ, Knox JP. 51.  2010. Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. PNAS 107:15293–98 [Google Scholar]
  52. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR. 52.  et al. 2007. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–7 [Google Scholar]
  53. Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR. 53.  2015. Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol. Rev. 39:649–69 [Google Scholar]
  54. Inoue H, Decker SR, Taylor LE, Yano S, Sawayama S. 54.  2014. Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus) critical for hydrolysis of lignocellulosic biomass. Biotechnol. Biofuels 7:151 [Google Scholar]
  55. Jahr H, Dreier J, Meletzus D, Bahro R, Eichenlaub R. 55.  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 Interact 13:703–14 [Google Scholar]
  56. Johnson P, Marsh DG. 56.  1965. Isoallergens from rye grass pollen. Nature 206:935–37 [Google Scholar]
  57. Junior AT, Dolce LG, de Oliveira Neto M, Polikarpov I. 57.  2015. Xanthomonas campestris expansin-like X domain is a structurally disordered beta-sheet macromolecule capable of synergistically enhancing enzymatic efficiency of cellulose hydrolysis. Biotechnol. Lett. 37:2419–26 [Google Scholar]
  58. Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS. 58.  et al. 2015. The Top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16:413–34 [Google Scholar]
  59. Karnaouri A, Topakas E, Antonopoulou I, Christakopoulos P. 59.  2014. Genomic insights into the fungal lignocellulolytic system of Myceliophthora thermophila. Front. Microbiol. 5:281 [Google Scholar]
  60. Kawata T, Nakamura Y, Saga Y, Iwade Y, Ishikawa M. 60.  et al. 2015. Implications of expansin-like 3 gene in Dictyostelium morphogenesis. SpringerPlus 4:190 [Google Scholar]
  61. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. 61.  2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10:845–58 [Google Scholar]
  62. Kende H, Bradford K, Brummell D, Cho HT, Cosgrove D. 62.  et al. 2004. Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol. Biol. 55:311–14 [Google Scholar]
  63. Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S. 63.  et al. 2008. Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. PNAS 105:16876–81 [Google Scholar]
  64. Kikuchi T, Li HM, Karim N, Kennedy MW, Moens M, Jones JT. 64.  2009. Identification of putative expansin-like genes from the pine wood nematode, Bursaphelenchus xylophilus, and evolution of the expansin gene family within the Nematoda. Nematology 11:355–64 [Google Scholar]
  65. Kim ES, Lee HJ, Bang WG, Choi IG, Kim KH. 65.  2009. Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose. Biotechnol. Bioeng. 102:1342–53 [Google Scholar]
  66. Kim IJ, Ko HJ, Kim TW, Choi IG, Kim KH. 66.  2013. Characteristics of the binding of a bacterial expansin (BsEXLX1) to microcrystalline cellulose. Biotechnol. Bioeng. 110:401–7 [Google Scholar]
  67. Kim IJ, Ko HJ, Kim TW, Nam KH, Choi IG, Kim KH. 67.  2013. Binding characteristics of a bacterial expansin (BsEXLX1) for various types of pretreated lignocellulose. Appl. Microbiol. Biotechnol. 97:5381–88 [Google Scholar]
  68. Kim IJ, Lee HJ, Choi IG, Kim KH. 68.  2014. Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase. Appl. Microbiol. Biotechnol. 98:8469–80 [Google Scholar]
  69. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW. 69.  et al. 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47:410–15 [Google Scholar]
  70. Kumar M, Singh P, Sukla LB. 70.  2016. Addition of expansin to cellulase enhanced bioethanol production. Process Biochem 51:2097–103 [Google Scholar]
  71. Laine MJ, Haapalainen M, Wahlroos T, Kankare K, Nissinen R. 71.  et al. 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 Pathol 57:221–33 [Google Scholar]
  72. Langan P, Petridis L, O'Neill HM, Pingali SV, Foston M. 72.  et al. 2014. Common processes drive the thermochemical pretreatment of lignocellulosic biomass. Green Chem 16:63–68 [Google Scholar]
  73. Lee HJ, Kim IJ, Kim JF, Choi IG, Kim KH. 73.  2013. An expansin from the marine bacterium Hahella chejuensis acts synergistically with xylanase and enhances xylan hydrolysis. Bioresour. Technol. 149:516–19 [Google Scholar]
  74. Lee HJ, Lee S, Ko HJ, Kim KH, Choi IG. 74.  2010. An expansin-like protein from Hahella chejuensis binds cellulose and enhances cellulase activity. Mol. Cells 29:379–85 [Google Scholar]
  75. Li Y, Darley CP, Ongaro V, Fleming A, Schipper O. 75.  et al. 2002. Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol 128:854–64 [Google Scholar]
  76. Li ZC, Durachko DM, Cosgrove DJ. 76.  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 191:349–56 [Google Scholar]
  77. Lipchinsky A. 77.  2013. How do expansins control plant growth? A model for cell wall loosening via defect migration in cellulose microfibrils. Acta Physiol. Plant 35:3277–84 [Google Scholar]
  78. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 78.  2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–95 [Google Scholar]
  79. Madej T, Lanczycki CJ, Zhang D, Thiessen PA, Geer RC. 79.  et al. 2014. MMDB and VAST+: tracking structural similarities between macromolecular complexes. Nucleic Acids Res 42:D297–303 [Google Scholar]
  80. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M. 80.  et al. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614–29 [Google Scholar]
  81. Martin F, Aerts A, Ahren D, Brun A, Danchin EG. 81.  et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92 [Google Scholar]
  82. Martinez-Anaya C. 82.  2016. Understanding the structure and function of bacterial expansins: a prerequisite towards practical applications for the bioenergy and agricultural industries. Microb. Biotechnol. 9:727–36 [Google Scholar]
  83. McCann MC, Carpita NC. 83.  2015. Biomass recalcitrance: a multi-scale, multi-factor, and conversion-specific property. J. Exp. Bot. 66:4109–18 [Google Scholar]
  84. McQueen-Mason S, Cosgrove DJ. 84.  1994. Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. PNAS 91:6574–78 [Google Scholar]
  85. McQueen-Mason S, Durachko DM, Cosgrove DJ. 85.  1992. Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–33 [Google Scholar]
  86. McQueen-Mason SJ, Cosgrove DJ. 86.  1995. Expansin mode of action on cell walls: analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107:87–100 [Google Scholar]
  87. Mielich-Suss B, Lopez D. 87.  2015. Molecular mechanisms involved in Bacillus subtilis biofilm formation. Environ. Microbiol. 17:555–65 [Google Scholar]
  88. Nikolaidis N, Doran N, Cosgrove DJ. 88.  2014. Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol. Biol. Evol. 31:376–86 [Google Scholar]
  89. Ogasawara S, Shimada N, Kawata T. 89.  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. Dev. Growth Differ. 51:109–22 [Google Scholar]
  90. Olarte-Lozano M, Mendoza-Nunez MA, Pastor N, Segovia L, Folch-Mallol J, Martinez-Anaya C. 90.  2014. PcExl1 a novel acid expansin-like protein from the plant pathogen Pectobacterium carotovorum, binds cell walls differently to BsEXLX1. PLOS ONE 9:e95638 [Google Scholar]
  91. Palomares-Rius JE, Hirooka Y, Tsai IJ, Masuya H, Hino A. 91.  et al. 2014. Distribution and evolution of glycoside hydrolase family 45 cellulases in nematodes and fungi. BMC Evol. Biol. 14:69 [Google Scholar]
  92. Park YB, Cosgrove DJ. 92.  2012. A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158:1933–43 [Google Scholar]
  93. Pastor N, Davila S, Perez-Rueda E, Segovia L, Martinez-Anaya C. 93.  2014. Electrostatic analysis of bacterial expansins. Proteins 83:215–23 [Google Scholar]
  94. Payne CM, Himmel ME, Crowley MF, Beckham GT. 94.  2011. Decrystallization of oligosaccharides from the cellulose Iβ surface with molecular simulation. J. Phys. Chem. Lett. 2:131546–50 https://doi.org/10.1021/jz2005122 [Crossref] [Google Scholar]
  95. Perini MA, Sin IN, Martinez GA, Civello PM. 95.  2017. Measurement of expansin activity and plant cell wall creep by using a commercial texture analyzer. Electron. J. Biotechnol. 26:12–19 https://dx.doi.org/10.1016/j.ejbt.2016.12.003 [Crossref] [Google Scholar]
  96. Qin L, Kudla U, Roze EH, Goverse A, Popeijus H. 96.  et al. 2004. Plant degradation: a nematode expansin acting on plants. Nature 427:30 [Google Scholar]
  97. Quiroz-Castaneda RE, Martinez-Anaya C, Cuervo-Soto LI, Segovia L, Folch-Mallol JL. 97.  2011. Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta. Microb. Cell Fact. 10:8 [Google Scholar]
  98. Radauer C, Breiteneder H. 98.  2006. Pollen allergens are restricted to few protein families and show distinct patterns of species distribution. J. Allergy Clin. Immunol. 117:141–47 [Google Scholar]
  99. Rayle DL, Cleland RE. 99.  1992. The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–74 [Google Scholar]
  100. Rocha VAL, Maeda RN, Pereira N, Kern MF, Elias L. 100.  et al. 2016. Characterization of the cellulolytic secretome of Trichoderma harzianum during growth on sugarcane bagasse and analysis of the activity boosting effects of swollenin. Biotechnol. Prog. 32:327–36 [Google Scholar]
  101. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B. 101.  et al. 2002. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur. J. Biochem. 269:4202–11 [Google Scholar]
  102. Sampedro J, Cosgrove DJ. 102.  2005. The expansin superfamily. Genome Biol 6:242 [Google Scholar]
  103. Sampedro J, Guttman M, Li LC, Cosgrove DJ. 103.  2015. Evolutionary divergence of beta-expansin structure and function in grasses parallels emergence of distinctive primary cell wall traits. Plant J 81:108–20 [Google Scholar]
  104. Shcherban TY, Shi J, Durachko DM, Guiltinan MJ, McQueen-Mason SJ. 104.  et al. 1995. Molecular cloning and sequence analysis of expansins—a highly conserved, multigene family of proteins that mediate cell wall extension in plants. PNAS 92:9245–49 [Google Scholar]
  105. Siciliano V, Genre A, Balestrini R, Cappellazzo G, Dewit PJ, Bonfante P. 105.  2007. Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–66 [Google Scholar]
  106. Silveira RL, Skaf MS. 106.  2016. Molecular dynamics of the Bacillus subtilis expansin EXLX1: interaction with substrates and structural basis of the lack of activity of mutants. Phys. Chem. Chem. Phys. 18:3510–21 [Google Scholar]
  107. Silveira RL, Stoyanov SR, Kovalenko A, Skaf MS. 107.  2016. Cellulose aggregation under hydrothermal pretreatment conditions. Biomacromolecules 17:2582–90 [Google Scholar]
  108. Stare BG, Lamovsek J, Sirca S, Urek G. 108.  2012. Assessment of sequence variability in putative parasitism factor, expansin (expB2) from diverse populations of potato cyst nematode Globodera rostochiensis. Physiol. Mol. Plant Pathol. 79:49–54 [Google Scholar]
  109. Sulova Z, Farkas V. 109.  1999. Purification of xyloglucan endotransglycosylase based on affinity sorption of the active glycosyl-enzyme intermediate complex to cellulose. Protein Expr. Purif. 16:231–35 [Google Scholar]
  110. Sulova Z, Takacova M, Steele NM, Fry SC, Farkas V. 110.  1998. Xyloglucan endotransglycosylase: evidence for the existence of a relatively stable glycosyl-enzyme intermediate. Biochem. J. 330:Part 31475–80 [Google Scholar]
  111. Suwannarangsee S, Bunterngsook B, Arnthong J, Paemanee A, Thamchaipenet A. 111.  et al. 2012. Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design. Bioresour. Technol. 119:252–61 [Google Scholar]
  112. Suzuki H, Vuong TV, Gong YC, Chan K, Ho CY. 112.  et al. 2014. Sequence diversity and gene expression analyses of expansin-related proteins in the white-rot basidiomycete. Phanerochaete carnosa. Fungal Genet. Biol. 72:115–23 [Google Scholar]
  113. Tovar-Herrera OE, Batista-Garcia RA, del Rayo Sanchez-Carbente M, Iracheta-Cardenas MM, Arevalo-Nino K, Folch-Mallol JL. 113.  2015. A novel expansin protein from the white-rot fungus Schizophyllum commune. PLOS ONE 10:e0122296 [Google Scholar]
  114. Veneault-Fourrey C, Commun C, Kohler A, Morin E, Balestrini R. 114.  et al. 2014. Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Genet. Biol. 72:168–81 [Google Scholar]
  115. Vincent D, Kohler A, Claverol S, Solier E, Joets J. 115.  et al. 2012. Secretome of the free-living mycelium from the ectomycorrhizal basidiomycete Laccaria bicolor. J. Proteome Res. 11:157–71 [Google Scholar]
  116. Voxeur A, Hofte H. 116.  2016. Cell wall integrity signaling in plants: “To grow or not to grow that's the question.”. Glycobiology 26:950–60 [Google Scholar]
  117. Wang Q, Chen L, Lin H, Yu D, Shen Q. 117.  et al. 2016. The binding, synergistic and structural characteristics of BsEXLX1 for loosening the main components of lignocellulose: lignin, xylan, and cellulose. Enzyme Microb. Technol. 92:67–75 [Google Scholar]
  118. Wang T, Chen Y, Tabuchi A, Cosgrove DJ, Hong M. 118.  2016. The target of beta-expansin EXPB1 in maize cell walls from binding and solid-state NMR studies. Plant Physiol 172:2107–19 [Google Scholar]
  119. Wang T, Park YB, Caporini MA, Rosay M, Zhong L. 119.  et al. 2013. Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls. PNAS 110:16444–49 [Google Scholar]
  120. Wang T, Yang H, Kubicki JD, Hong M. 120.  2016. Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17:2210–22 [Google Scholar]
  121. Wang WC, Liu C, Ma YY, Liu XW, Zhang K, Zhang MH. 121.  2014. Improved production of two expansin-like proteins in Pichia pastoris and investigation of their functional properties. Biochem. Eng. J. 84:16–27 [Google Scholar]
  122. Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D. 122.  et al. 2006. Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J. 48:98–112 [Google Scholar]
  123. Wiśniewska M, Golinowski W. 123.  2011. Immunolocalization of α-expansin protein (NtEXPA5) in tobacco roots in the presence of the arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. Acta Biol. Cracov. Ser. Bot. 53:113–23 [Google Scholar]
  124. Yadeta K, Thomma B. 124.  2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 4:97 [Google Scholar]
  125. Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ. 125.  2006. Crystal structure and activities of EXPB1 (Zea m 1), a β-expansin and group-1 pollen allergen from maize. PNAS 103:14664–71 [Google Scholar]
  126. Yu Y, Yan F, Chen Y, Jin C, Guo JH, Chai Y. 126.  2016. Poly-γ-glutamic acids contribute to biofilm formation and plant root colonization in selected environmental isolates of Bacillus subtilis. Front. Microbiol. 7:1811 [Google Scholar]
  127. Yuan S, Wu Y, Cosgrove DJ. 127.  2001. A fungal endoglucanase with plant cell wall extension activity. Plant Physiol 127:324–33 [Google Scholar]
/content/journals/10.1146/annurev-micro-090816-093315
Loading
/content/journals/10.1146/annurev-micro-090816-093315
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error